Biotechnology Advances 43 (2020) 107570

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Biotechnology Advances
journal homepage: www.elsevier.com/locate/biotechadv

Research review paper

Technologies for biological removal and recovery of nitrogen from T

wastewater
Shadi Rahimia, , Oskar Modinb, Ivan Mijakovica,c,
⁎ ⁎

a
Division of Systems and Synthetic Biology, Department of Biology and Biological Engineering, Chalmers University of Technology, Gothenburg, Sweden
b
Division of Water Environment Technology, Department of Architecture and Civil Engineering, Chalmers University of Technology, Gothenburg, Sweden
c
The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark

ARTICLE INFO ABSTRACT

Keywords: Water contamination is a growing environmental issue. Several harmful effects on human health and the en-
Nitrogen vironment are attributed to nitrogen contamination of water sources. Consequently, many countries have strict
Nitrate regulations on nitrogen compound concentrations in wastewater effluents. Wastewater treatment is carried out
Ammonium using energy- and cost-intensive biological processes, which convert nitrogen compounds into innocuous dini-
Wastewater
trogen gas. On the other hand, nitrogen is also an essential nutrient. Artificial fertilizers are produced by fixing
Recovery
dinitrogen gas from the atmosphere, in an energy-intensive chemical process. Ideally, we should be able to spend
less energy and chemicals to remove nitrogen from wastewater and instead recover a fraction of it for use in
fertilizers and similar applications. In this review, we present an overview of various technologies of biological
nitrogen removal including nitrification, denitrification, anaerobic ammonium oxidation (anammox), as well as
bioelectrochemical systems and microalgal growth for nitrogen recovery. We highlighted the nitrogen removal
efficiency of these systems at different temperatures and operating conditions. The advantages, practical chal-
lenges, and potential for nitrogen recovery of different treatment methods are discussed.

1. Introduction and domestic, result in contamination of water with nitrogen when

those wastes get discharged in water sources without treatment. Mu-
Ground- and surface waters are contaminated by nitrogen via nu- nicipal wastewater treatment plants (WWTPs) also contribute to ni-
merous routes (Fig. 1). Increasing application of fertilizers in agri- trogen loading into the surface and ground waters with approximately
culture was reported to contaminate surface and ground water sources 80,000 tonnes/yr (Ritter et al., 2002). Strict nitrogen discharge stan-
with around 293,000 tonnes/yr of nitrogen in Canada (Ritter et al., dards are enforced by many countries. For example, municipal WWTPs
2002). Moreover, different types of waste, including industrial, animal, are allowed to discharge less than 5 mg L-1 ammonium and 15 mg L-1

Abbreviations: AB, algal biofilm; ABMFC, algae biofilm microbial fuel cell; AHL, acyl homoserine lactone; ALE, adaptive laboratory evolution; AMO, ammonia
monooxygenase; AnAOB, anaerobic ammonia oxidation bacteria; AOB, ammonium oxidizing bacteria; CANON, completely autotrophic nitrogen removal over nitrite;
C/N, carbon to nitrogen ratio; 2C4NP, 2-chloro-4-nitrophenol; Comammox, complete ammonia oxidizers; COD, chemical oxygen demand; CSTR, continuous stirred
tank reactor; DAMO, denitrifying anaerobic methane oxidation; DEA, diethylamine-functionalized polymer; DEAMOX, denitrifying ammonium oxidation; DO,
dissolved oxygen; DSA, dimensionally stable anodes; EPS, extracellular polymeric substance; FA-MFC, flat-panel air-cathode MFC; GMM, genetically modified
microorganism; HAO, hydroxylamine oxidoreductase; HF-MBfR, H2-based hollow-fiber membrane biofilm reactor; HRAP, high rate algal pond; HRT, hydraulic
retention time; LUC, land use change; MABR, membrane-aerated biofilm reactor; MBBR, moving bed biofilm reactor; MBfR, membrane-biofilm reactor; MEC,
microbial electrolysis cells; MFCs, microbial fuel cells; m-WWTPs, municipal wastewater treatment plants; NADH, nicotinamide adenine dinucleotide; NADPH,
nicotinamide adenine dinucleotide phosphate; N/P, nitrogen to phosphorus molar ratio; NPs, nitrophenols; NOB, nitrite oxidizing bacteria; 3NT, 3-nitrotoluene; 4NT,
4-nitrotoluene; 2NTDO, 2-nitrotoluenene 2,3-dioxygenase; NTR, nitrate-to-nitrite transformation ratio; NXR, nitrite oxidoreductases; OLAND, oxygen-limited ni-
trification and denitrification; PAC, poly-aluminium chloride; PAOs, polyphosphate-accumulating organisms; PBRs, photobioreactors; PBS, poly(butylene succinate);
PCL, poly(ε-caprolactone); PHAs, polyhydroxyalkanoates; PHBV, poly3-hydroxybutyrate-co-3-hydroxyvalerate; PLA, poly(lactic acid); PLLA, poly(l-lactic acid); PQS,
Pseudomonas quinolone signal; PVA, polyvinyl alcohol; QS, quorum sensing; rhl, acyl-homoserine-lactone synthase; SHARON, single reactor high activity ammonia
removal over nitrite; SNAD, simultaneous nitrification anammox and denitrification; SND, Simultaneous nitrification and denitrification; SRT, sludge retention time;
VHb, Vitreoscilla Hemoglobin b
⁎
Corresponding authors.
E-mail addresses: [email protected] (S. Rahimi), [email protected] (I. Mijakovic).

https://doi.org/10.1016/j.biotechadv.2020.107570
Received 1 November 2019; Received in revised form 22 May 2020; Accepted 22 May 2020
Available online 10 June 2020
0734-9750/ © 2020 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/BY/4.0/).
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Fig. 1. Nitrogen loading (103 tonnes/yr) to the surface water and groundwater in Canada from various sources. The nitrogen loading rates values are provided from
Ritter et al., 2002. It should be pointed out that not all atmospheric nitrogen deposition can be considered as contamination.

total nitrogen in China (GB18918-2002) (Du et al., 2015). Thus, ni- ammonium oxidation (anammox). We then present a comparative
trogen removal from wastewaters is extremely important to protect overview on the advantages and challenges presented by different
water resources, especially for regions facing water shortage. Eu- biological nitrogen removal processes, including their potential for
trophication in freshwater ecosystems is one of the direct and harmful obtaining high effluent quality as well as for chemical/energy recovery.
consequences of excessive nitrogen loading. The eutrophication phe- We also discuss various physico-chemical factors that may affect the
nomenon degrades freshwater ecosystems by developing algal blooms, efficiency of the biological nitrogen removal methods.
spreading aquatic plants, oxygen depletion and hence loss of key spe-
cies (Taziki et al., 2015). Furthermore, blue green algae blooms can 2. Major biological enzymatic processes of nitrogen cycle that
produce natural toxins that pose risks to the human health (Ritter et al., transform nitrogen into various oxidation states
2002; Taziki et al., 2015).
Nitrogen exists in different oxidation states which makes the process Stein and Klotz (2016) suggested five nitrogen-transformation flows
of its removal from water complex and challenging. Adsorption or co- (coloured arrows in Fig. 2A) which are the following: ammonification,
precipitation treatment is most often not feasible due to the stability including reduction of dinitrogen or nitrogen fixation (red), assim-
and high solubility of nitrate, resulting in high energy and cost for ilatory and dissimilatory reduction of nitrite to ammonium (DNRA)
treatment of nitrate-contaminated water (Rezvani et al., 2019). Most (blue); nitrification (green and orange) composed of ammonia oxida-
wastewater treatment systems have two levels of treatment: primary tion to nitrite (nitritation), and oxidation of nitrite to nitrate (nitrata-
(physical settling of solids) and secondary (various forms of biological tion); denitrification (purple); anammox, as a form of coupled ni-
oxidation e.g. activated sludge or trickling filters). In regions where trification–denitrification (pink); and nitrite–nitrate interconversion
regulations mandate higher effluent quality, tertiary treatment is also (orange and cyan). The general processes of organic matter miner-
used for nutrient removal and disinfection. Tertiary treatment as the alization and assimilation by cellular life completes the movement of
final cleaning process removes inorganic compounds and improves the reactive nitrogen through the biosphere. Microorganisms that partici-
effluent quality before it is reused, recycled or discharged to the en- pate in the above-mentioned biological processes of nitrogen cycle in-
vironment. clude heterotrophic denitrifying bacteria, autotrophic nitrifying bac-
Biological approaches are known to effectively remove nitrogen teria, anammox bacteria, and microalgae (Fig. 2B).
compounds in wastewater (EPA, 1993). The activated sludge process, as In primary wastewater treatment, the major forms of nitrogen pre-
the most common biological wastewater treatment method, was de- sent in the water are organic nitrogen and ammonium. During sec-
veloped to enhance the effectiveness of nutrient removal. In a con- ondary treatment, these two major forms of nitrogen are rapidly con-
ventional nitrogen removal process, wastewater goes through the ni- verted to nitrate by nitrifying bacteria, including ammonium oxidizing
trification and then the denitrification process. Nitrification is the bacteria (AOB) and nitrite oxidizing bacteria (NOB) (Taziki et al.,
biological oxidation of ammonia or ammonium to nitrite followed by 2015). Newly identified complete ammonia oxidizers (Comammox) can
oxidation of nitrite to nitrate, however, denitrification reduces nitrate perform ammonia oxidation to nitrate (Daims et al., 2015) (Fig. 2B).
and ultimately produces N2 through a series of intermediate gaseous Nitrite is the most ephemeral form of nitrogen in the environment. In
nitrogen oxide products. When there is not sufficient organic carbon both wastewater treatment systems and surface waters, it occurs as the
source in wastewater for denitrification, this negatively affects the ni- least prevalent form of inorganic nitrogen. Among the above-mentioned
trogen removal efficiency (Blackburne et al., 2008). Various technolo- biological processes of nitrogen cycle, nitrification, denitrification,
gies for nitrification and denitrification of wastewater have been re- anammox, and nitrogen assimilation are discussed here.
viewed previously (Ali and Okabe, 2015; Rodríguez Arredondo et al.,
2015; Gonçalves et al., 2017; Ma et al., 2016; Taziki et al., 2015;
Tomaszewski et al., 2017). In this review, we aim to compare the ef- 3. Fundamental nitrogen removal processes
ficiency and energy cost of different methods to hopefully facilitate
decisions on wastewater treatment policies based on local conditions. Biological wastewater treatment is operated based on the combined
We first describe the fundamental biological nitrogen removal pro- activity of microorganisms in microbial community. Thus, it is im-
cesses in WWTPs, such as nitrification, denitrification, and anaerobic portant to know about the nitrogen removal processes along with the
microbial communities involved in the processes. Proteobacteria are a

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S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Fig. 2. Major biological processes of the nitrogen cycle (A). Arrows with different colours are the major processes in nitrogen cycle including, ammonification (red),
assimilatory and dissimilatory reduction of nitrite to ammonium (DNRA) (blue), nitrification (green and orange), denitrification (purple), anammox (pink), ni-
trite–nitrate interconversion (orange and cyan). Organisms participated in the biological processes of nitrogen cycle (B). The coloured arrows and enzymes follow the
rules in figure (A). Both ammonification and assimilatory reduction of nitrite to ammonium are performed by microalgae. It should be pointed out that archaea can
also carry out nitrification and denitrification. AOB, ammonium oxidizing bacteria; NOB, nitrite oxidizing bacteria; AMO, ammonia monooxygenase; HAO; hy-
droxylamine oxidoreductase; HH, hydrazine hydrolase; HZO, hydrazine-oxidizing enzyme. (For interpretation of the references to color in this figure legend, the
reader is referred to the web version of this article.)

dominant phylum in activated sludge as the most common technology processes including membrane bioreactors and cell-immobilization (Ge
for sewage treatment, followed by other groups such as Bacteroidetes, et al., 2015; Shoda, 2017) (Table 2). Partial nitrification via nitrite
Chloroflexi, Actinobacteria, Planctomycetes, Firmicutes, etc (Ferrera offers several significant advantages in biological wastewater treatment
and Sánchez, 2016). Here we discuss the nitrogen removal processes compared to the conventional nitrification including: i) 40% reduction
driven by specific microbes. Table 1 presents total nitrogen removal of chemical oxygen demand (COD) and 1.5–2 fold increase of nitrite
efficiency, chemical input, economic evaluation and main technical reduction rates in the subsequent denitrification stage, ii) saving 25%
parameters of different nitrogen removal processes compared to the oxygen consumption, 300% biomass reduction, and 20% CO2 emission
conventional process. during denitrification. When partial nitrification is combined with
anammox, ammonium partially oxidizes to nitrite aerobically, and re-
maining ammonium subsequently reacts with nitrite to form nitrogen
3.1. Nitrification gas anaerobically. This has several benefits, such as no requirement of
external carbon source, 80% reduced sludge production, and less en-
Nitrification consists of two sequential biological oxidation pro- ergy and 60% reduced oxygen requirement compared to the conven-
cesses. The first step is NH4+ oxidation to NO2−, which is the limiting tional nitrification/denitrification (Ge et al., 2015; Cao et al., 2017).
step and is carried out by the AOB. This reaction is catalysed by am- The partial nitrification is based on the condition favouring AOB bac-
monia monooxygenase (AMO) and hydroxylamine oxidoreductase teria but preventing NOB bacteria. Therefore, there are several para-
(HAO), along with hydroxylamine (NH2OH) formation as the inter- meters preferred by AOB bacteria positively affected partial nitrifica-
mediate product. The NO2− produced in the first step is rapidly con- tion including i) pH (7.5 to 8.5) (Ge et al., 2015), ii) temperature
verted to NO3− in the second step, carried out by the NOB, in the (higher than 25.0 °C) (Paredes et al., 2007), iii) dissolved oxygen (DO)
presence of molecular oxygen. The conversion is catalysed by nitrite concentration (1.5 mg L−1) (Ruiz et al., 2006), iv) real-time control of
oxidoreductases (NXR) and nitrite-oxidizing systems, which are one- aeration and periodic anoxic and aerobic operation (Ge et al., 2014), v)
step oxidation enzymes found in Nitrobacter and in the genera of sludge retention time (SRT) (5 d) (Galí et al., 2007), vi) C/N ratio
Nitrococcus, Nitrospina and Nitrospira, respectively (Fig. 2B). (0.3 < C/N < 6) (Zafarzadeh et al., 2011; Mosquera-Corral et al.,
In comparison with the physicochemical processes for wastewater 2005), vii) NOB inhibitor (such as sulfide, hydroxylamine, salt, heavy
treatment, biological nitrogen removal via nitrification and deni- metals, chlorate, cyanate, halide, azide, hydrazine, and organic che-
trification is more cost-effective. However, several drawbacks remain, micals) (Sinha and Annachhatre, 2007), and viii) ultrasonic treatment
such as slow nitrification reaction, decreasing nitrification activity by (frequency 40 kHz and density ultrasound 0.027 W mL−1 for 2 h
ammonium and organic matter overload, necessity of oxygen control, (Zheng et al., 2013) (Fig. 3A).
and the demand for two reactors: an aerobic one for nitrification and an The moving bed biofilm reactor (MBBR) is composed of an aeration
anaerobic one for denitrification. Also, large size reactor or long hy- tank with special plastic carriers for fixing biomass as the biofilm. The
draulic retention time (HRT) are required to complete NH4+ removal carriers are mixed in the tank by the aeration system and thereby
due to low nitrification rate, resulting in high operational cost (Shoda, leading a good contact between the biomass on the carriers and the
2017). Several biological nitrogen removal process systems have been substrate present in the influent wastewater. Recently, combination of
developed to reduce energy input into the process. These include si- nitrification and poly-aluminium chloride (PAC) adsorption of organic
multaneous nitrification and denitrification, anammox, partial ni- micropollutants were simultaneously performed in a nitrifying MBBR
trification and denitrification, complete autotrophic nitrogen removal (Cimbritz et al., 2019). However, due to inhibitory effect of nitrite on
over nitrite (CANON), aerobic deammonification, oxygen-limited ni- polyphosphate-accumulating organisms (PAOs), the simultaneous
trification and denitrification (OLAND), as well as combination of these

3
 S. Rahimi, et al.

Table 1
Total nitrogen removal efficiency, chemical input, economic evaluation, main technical parameters of different nitrogen removal process compared to conventional process.
Operation technique Total nitrogen removal Chemical input Economic evaluation Main technical parameters References
efficiency

Partial nitrification via nitrite 1.5–2 fold increase of nitrite 40% reduction of COD 25% reduced oxygen demand, 300% biomass pH, temperature, DO, real-time aeration control, Ge et al. (2015)
reduction rates in the reduction, 20% CO2 emission during denitrification sludge retention time, substrate concentration,
subsequent denitrification stage alternating anoxic and aerobic operation, inhibitor,
ultrasonic treatment
Partial nitritation /anammox ≥85% of nitrogen removal No need of external carbon 60% reduced oxygen demand, 80% reduced sludge Carbon concentrating pretreatment, suppression of Cao et al. (2017)
source production, 24 Wh/p/day, compared to a 44 Wh/p/ NOB especially under low temperatures (15–10 °C),
day consumption in conventional treatment intensification of anammox biofilm activity, reactor
design, final polishing
Simultaneous nitrification and 82% nitrogen removal Requirement of external Saving cost for anoxic tank, applicable only for low Reactor design, oxygen availability for nitrification, Guo et al. (2005)
denitrification (SND) carbon source C/N ratio (< 5) wastewaters effective carbon source utilization for denitrification
Shortcut nitrification and Nitrite denitrification rate is 1.5 40% lower demand of 25% reduced oxygen demand in aerobic phase with DO, SRT, pH, temperature, substrate concentration Peng and Zhu (2006)
denitrification to 2 times higher than nitrate electron donors in anoxic 60% saving energy, applicable for high ammonium and load, operational and aeration pattern, inhibitor
denitrification rate phase concentrations or low C/N ratios wastewaters
Nitritation/anammox 81% nitrogen removal No need of external carbon 60% reduced oxygen demand, energy recovery by Poor effluent water quality, need of post- Du et al. (2015); Ma

4
source methane production, minimal surplus sludge denitrification process et al. (2016); Li et al.
production, consumption of inorganic carbon CO2, no (2016a)
nitrous oxide emission, decrease in energy
consumption from 2.66 to 1.50 kWh per kg N
removed for reject water treatment
Simultaneous partial nitrification, 99% nitrogen removal Low concentrations of Simultaneous removal of inorganic nitrogen and Intermittent aeration, pH, DO Zhang et al. (2017)
anammox, and denitrification organic matter organic carbon, applicable for wastewater with
(SNAD) complex composition and high ammonia
concentration and low C/N ratio
Denitrifying ammonium oxidation 94% nitrogen removal, 80% reduced demand of 100% reduced aeration demand, 64.8% reduced Co-existence of partial-denitrification and anammox Du et al. (2017)
(DEAMOX) simultaneous nitrate and organic carbon sludge production, low nitrogen contained bacteria
ammonium removal wastewater, low/high-strength nitrate and
ammonium containing wastewater, reduced
greenhouse gas (CO2 and N2O) emission
Partial-denitrification/anammox More than 90% nitrogen 79% reduced demand of 45% reduced oxygen demand, reduced biomass Avoiding high organic matter in the effluent of Ma et al. (2016), Cao
removal organic carbon production, applicable for high-strength wastewater partial denitrification reactor et al. (2016)
Denitrification by bioelectrochemical 100% nitrate removal Required carbon source 100% reduced oxygen demand, producing power and Generation of high concentrations of ammonium in Naga Samrat et al.
systems and buffering agent current densities of 2.1 W/m3 and 26.6 A/m3 anode and cathode (2018)

COD- chemical oxygen demand; DO- dissolved oxygen concentration; SRT- sludge retention time; Wh/p/day- watt hours per person per day.
Biotechnology Advances 43 (2020) 107570
 Table 2
Comparison of nitrogen removal efficiencies between different anammox methods.
Optimization method Reactor type Operation technique Wastewater Total nitrogen Temperature References
S. Rahimi, et al.

removal

Combined anammox Sequencing batch reactors (SBR) Anammox-partial denitrification Synthetic wastewater 94.06% 30 °C Du et al. (2015)
system 20–26 °C
SBR Anammox-denitrification Synthetic wastewater 97.47% 30 °C Du et al. (2014)
Plug-flow granular sludge-based pilot-scale One-stage partial nitritation-anammox A-stage of the WWTP of Dokhaven, Rotterdam 46% 19 °C Lotti et al. (2015)
reactor
Upflow anaerobic sludge blanket reactor Anammox-partial denitrification Synthetic wastewater, domestic wastewater 97.8% 28 °C Cao et al. (2016)
(UASB) +SBR
Upflow reactor Synergy of sludge fermentation, denitrification and Pre-treated domestic wastewater and 0.065 g N L−1 16–29 °C Wang et al. (2016a)
anammox processes synthetic wastewater d−1
Anaerobic upflow reactor Granular bed anammox Synthetic medium 60% 37 °C Cho et al. (2010)
Combining high rate anammox reactor SBA-anammox process Pharmaceutical wastewater 9.4 g N L−1 d−1 35 °C Tang et al. (2011)
with sequential biocatalyst addition (SBA)
Membrane biofilm reactor (MBfR) Synergy of anammox and denitrifying anaerobic Synthetic wastewater 0.25 g N L−1 d−1 NA Shi et al. (2013)
methane oxidation (DAMO) microorganisms
SBR Simultaneous partial nitrification, anammox and Synthetic wastewater 85-87% 35 °C Lan et al. (2011)
denitrification (SNAD)
Lab-scale upflow membrane-aerated Granular nitritation-anammox Synthetic wastewater 81% 25 °C Li et al. (2016a)
biofilm reactor (UMABR)
Full-scale SBR Decentralized full-scale system Municipal wastewater 50% NA Fernandes et al. (2013)
Lab-scale sequencing batch biofilm reactors Intelligent control system (ICS) and timer control Synthetic wastewater 87.8% 25 °C Jin et al. (2012)
(SBBR) system (TCS)
Lab-scale A2N-SBR Anaerobic-anoxic/nitrification Domestic wastewater 83% 22–25 °C Wang et al. (2009)
UASB Anaerobic digester seedling sludge Inorganic medium 42 g N L−1 d−1 30-35 °C Hu et al. (2010)
Low temperature Aerobic/anoxic sequence batch reactor SBR Removal of carbon and nutrients Synthetic wastewater 71.15% 20 °C Mansouri et al. (2014)

5
UASB Effect of seasonal temperatures on anammox Synthetic wastewater 3.77 g N L−1 d−1 2.5–15.8 °C seasonal Guo et al. (2015)
variations
Continuous reactor Gel carrier with entrapped anammox bacteria at Synthetic water 0.36 g N L−1 d−1 6.3 °C Isaka et al. (2008)
lower temperature
Gas-lift reactor Cold-adapted anammox species Synthetic medium 0.02 g N L−1 d−1 10 °C Hendrickx et al. (2014)
SBR Direct treatment of municipal wastewater using Synthetic media and municipal wastewater 0.046 g N L−1 12.5 °C Laureni et al. (2015)
anammox from Dübendorf Switzerland d−1
SBR Optimization of the nitrogen sludge loading rate Synthetic sewage 0.029 g N L−1 13.2 °C Sánchez Guillén et al.
(NSLR) d−1 (2016)
Granular SBR Completely autotrophic nitrogen removal over Supernatant of an anaerobic sludge digester of 0.2 g N L−1 d−1 15 °C Vázquez-Padín et al.
nitrite (CANON) process the WWTP of Lugo Spain (2011)
Membrane bioreactor (MBR) Anammox at lower temperatures Synthetic nutrient medium 1.1 g N L−1 d−1 15 °C Awata et al. (2015)
Upflow anaerobic biofilter (AF) Anammox for treating low-strength wastewater Synthetic wastewater 1.965 g N L−1 15.3 °C Taotao et al. (2015)
d−1
UASB High anammox activity and abundance Low strength wastewater 2.28 g N L−1 d−1 16 °C Ma et al. (2013)
SBR Anammox at lower temperatures Synthetic autotrophic medium 0.325 g N L−1 18 °C Dosta et al. (2008)
d−1
Upflow anammox sludge bed (UAnSB) Anammox process at low temperature Nitrite-amended pre-treated real urban 82 ± 4% 11 °C Reino et al. (2018)
reactor wastewater
Up-flow column reactor (UCR) Porous polyester nonwoven fabric Synthetic inorganic medium 0.18 g N L−1 d−1 18 °C Osaka et al. (2012)
Gas-lift Direct anaerobic treatment of municipal Synthetic influent 0.29 g N L−1 d−1 20 °C Hendrickx et al. (2012)
wastewaters
(continued on next page)
Biotechnology Advances 43 (2020) 107570
 Table 2 (continued)

Optimization method Reactor type Operation technique Wastewater Total nitrogen Temperature References
removal
S. Rahimi, et al.

Anaerobic biological filtrated (ABF) reactor Porous polyester nonwoven fabric carriers as a Synthetic water 8.1 g N L−1 d−1 20–22 °C Isaka et al. (2007b)
fixed bed for anammox bacteria
Continuous reactor Gel carrier with entrapped anammox bacteria Synthetic water 2.8 g N L−1 d−1 22 °C Isaka et al. (2008)
UCR Gas–solid separator Synthetic inorganic wastewater 17.5 g N L−1 d−1 23 ± 2 °C Yang et al. (2011)
Single reactor high activity ammonia Two-unit SHARON reactor coupled to anammox Supernatant of an anaerobic sludge digester of 0.08 g N L−1 d−1 20 °C Vázquez-Padín et al.
removal over nitrite (SHARON), SBR SBR the WWTP of Lugo Spain (2011)
Moving bed biofilm reactor (MBBR) Partial nitritation-anammox Synthetic wastewater 0.007 g N L−1 10 °C Gilbert et al. (2015)
d−1
MBBR Partial nitritation-anammox Synthetic influent 0.015 g N L−1 10 °C Gilbert et al. (2014)
d−1
SBR Combination of aerobic ammonium-oxidizing Synthetic pre-treated municipal wastewater 0.025 g N L−1 12 °C Hu et al. (2013)
bacteria (AOB) and anammox d−1
OLAND rotating biological contactor (RBC) Oxygen-limited autotrophic nitrification/ Synthetic wastewater 0.5 g N L−1 d−1 15 °C De Clippeleir et al.
denitrification (OLAND) (2013)
−1
MBBR Partial nitritation-anammox Municipal wastewater 0.030 g N L 15 °C Laureni et al. (2016)
d−1
MBBR Integrated fixed-film activated sludge (IFAS) mode Mainstream wastewater 0.010 g N L−1 16 ± 1 °C Trojanowicz et al.
d−1 (2016)
RBC Anammox process accompanied with autotrophic Municipal landfill leachate and artificial 0.5 g N L−1 d−1 17 °C Cema et al. (2007)
nitrification and heterotrophic denitrification NaNO2 and NH4Cl solutions
Air-lift sequencing batch reactor (SBAR) Granular sludge-anammox based single stage Synthetic medium 85-75 % 10-20 °C Lotti et al. (2014)
Immobilization Continuous stirred tank reactor (CSTR) Polyvinyl alcohol (PVA)- immobilized system Synthetic and partially nitrified swine 0.5 g N L−1 d−1 33 °C Magrí et al. (2012)
wastewater
CSTR PVA, sodium alginate (SA)-immobilized system Synthetic wastewater and modified reject 8.2 g N L−1 d−1 33 °C Quan et al. (2011)
water

6
CSTR Polyethylene glycol (PEG)-immobilized system Digester liquor of biogas plant 4 g N L−1 d−1 30 °C Furukawa et al. (2009)
CSTR PEG-immobilized system Digester supernatant 3.8 g N L−1 d−1 30 °C Isaka et al. (2011)
CSTR PEG-immobilized system Ammonia-rich wastewater 6 g N L−1 d−1 36 °C Isaka et al. (2008)
CSTR PEG-immobilized system Synthetic water 3.7 g N L−1 d−1 36 °C Isaka et al. (2007a)
CSTR PEG-immobilized system Digester supernatant for sludge 3.8 g N L−1 d−1 30 °C Kimura et al. (2013)
CSTR PVA-immobilized system Synthetic wastewater 4.4 g N L−1 d−1 30 °C Ge et al. (2009)
CSTR PVA, SA-immobilized system Synthetic wastewater 1.69 g N L−1 d−1 33-35 °C Qiao et al. (2013)
SBR PVA, SA-immobilized system Synthetic medium 0.58 g N L−1 d−1 35 °C Zhu et al. (2014)
Up-flow glass column reactors (UFCR) PVA, SA-immobilized system Culture medium 10.8 g N L−1 d−1 37 °C Ali et al. (2015)
Lab-scale MBR Bacillus methylotrophicus L7 Artificial wastewater 53% 25–30 °C Yao et al. (2013)
Pilot-scale SBR Activated sludge + A. tumefaciens LAD9, C. Municipal wastewater 80.5% NA Chen et al. (2015)
testosteroni GAD3 and A. xylosoxidans GAD4
Biotechnology Advances 43 (2020) 107570
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Fig. 3. Strategies for partial nitritation and anammox by ammonium oxidizing bacteria (AOB) and suppression of nitrite oxidizing bacteria (NOB). Schematic
structure of partial nitritation/anammox (B), simultaneous partial nitrification, anammox and denitrification (SNAD) (C) and partial denitrification/anammox (D)
reactors.

removal of nitrogen and phosphorus in partial nitrification systems has AOB/NOB species was found as the dominant in some of these systems,
not been achieved and needs to be further investigated. while different species existed in other systems. Furthermore, nitrifying
granules with high sedimentation property maintain β-proteobacterial
3.1.1. Microorganisms involved in nitrification ammonia oxidizing bacteria and the Nitrospira-like nitrite-oxidizing
Nitrification, a two-step process of ammonia oxidation via nitrite to bacteria as the dominant bacteria in a reaction tank. As high-rate ni-
nitrate, is catalysed by chemolithoautotrophic microorganisms oxi- trification of 1.5 kgN m−3 day−1 is achieved using real electronics
dizing either ammonia or nitrite. Two phylogenetically unrelated industry wastewater, which is 2.5–5 times faster than traditional acti-
groups of AOB and NOB are Gram-negative autotrophic bacteria re- vated sludge methods (Hasebe et al., 2017).
sponsible for aerobic nitrification. They obtain energy and carbon from
ammonia oxidation and CO2, respectively and they use oxygen as the 3.1.2. Reactor technologies in nitrification
terminal electron acceptor (Shoda, 2017). AOB have multi-layered cell 3.1.2.1. Partial nitritation and anammox. 200,000 m3/day step-feed
wall morphology and are motile by means of flagella. Five recognized activated sludge process of the Changi WRP, Singapore, and the
genera of AOB include β-subclass of proteobacteria such as Ni- deammonification process in Strass WWTP, Austria, are two examples
trosomonas, Nitrosospira, Nitrosovibrio and Nitrosolobus, and only Ni- full-scale application of partial nitritation and anammox suspended
trosococcus from the γ-subclass proteobacteria (Ge et al., 2015). A total sludge processes (Cao et al., 2013a; Cao et al., 2016; Wett et al., 2013).
25 AOB species have been collected from various environments, certain Partial nitritation and anammox can be operated in a single-stage
of which can grow under both aerobic and anaerobic conditions (Ge process in one reactor which is cost-effective with less emission of
et al., 2015). Interestingly, nitrification products of AOB species vary greenhouse gas N2O compared with two-stage process in two reactors
based on the availability of DO. For example, Nitrosomonas eutropha (Fig. 3B) (Ge et al., 2015; Kampschreur et al., 2009). In spite of
aerobic oxidation product at the DO higher than 0.8 mg L−1 is only remarkable progress in feasibility of mainstream partial nitritation and
nitrite while some other products such as nitrogen gas, nitrite and nitric anammox process at low temperatures (Lotti et al., 2014), “warm
oxides are produced at DO below 0.8 mg L−1 (Ge et al., 2015). NOB are anammox” operating between 20-30 °C is still promising compared
more widespread than AOB and they are classified into four phylo- with the cold anammox (Sánchez Guillén et al., 2015; Li et al., 2016a).
genetically distinct groups (Ge et al., 2015). Genera of Nitrococcus and Suppression of NOB bacteria can be achieved in partial nitritation and
Nitrobacter belong to the α- and γ-subclass, respectively. Meanwhile, anammox by controlling competition of AOB and NOB for oxygen in
the Nitrospira genus with the first-deciphered complete genome of oxygen-limited condition (Pérez et al., 2014).
Candidatus Nitrospira defluvii, is classified in the δ-subclass (Ge et al., AOB bacteria are the main producer of N2O during nitrification.
2015). Recent characterization of a complete nitrifying bacterium Ni- However, there is no contribution by anammox to N2O formation. The
trospira, that carries out a process called Comammox, fundamentally aeration pattern was found to be the principal factor influencing the
changed the picture of microbial nitrification (Daims et al., 2015). emission and formation of N2O in reactors (Ma et al., 2017; Ni et al.,
Pathways for ammonia and nitrite oxidation are concomitantly ex- 2013; Castro-Barros et al., 2015). Periodic aeration with increasing
pressed in this organism during growth, leading to ammonia oxidation cycle frequency, transient aeration patterns from low (or anoxic) to
to nitrate. high aeration, and continuous aeration are some of the effective aera-
Overall, among AOB and NOB microorganisms previously detected tion patterns for reducing N2O production in reactor setups (Ni et al.,
as the main nitrifiers in activated sludge and engineered system sam- 2013; Castro-Barros et al., 2015).
ples, Nitrosomonas sp. was present in all the systems described, as well
as the NOB Nitrospira (Ferrera and Sánchez, 2016). However, a single 3.1.2.2. NOB suppression in biofilm reactors. The membrane-biofilm

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S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

reactor (MBfR), also known as the membrane-aerated biofilm reactor et al., 2002). This effect of alcohols is due to formation of smaller size of
(MABR), is an attractive nitrogen removal technology in wastewater biofilms with higher density of bacteria, causing higher denitrification
treatment based on gas-transferring membranes. Gaseous substrates rate versus nitrate reduction rate. These carbon sources are more ap-
acting as the electron donor or acceptor (such as oxygen, hydrogen, and propriate for the biological denitrification of water contaminated with
methane) are diffused through the hydrophobic and gas-permeable nitrate and containing DO. Other challenges with denitrification in-
membranes to a biofilm which is forming on the membrane surface clude slow reaction rate due to high start-up time and HRT, need for pH
(Nerenberg, 2016). adjustment and drop of productivity at cold temperatures (Rezvani
Layered biofilm structure and oxygen-controlled system in MABRs et al., 2019). Some of these problems such as the slow reaction rate may
repress NOB activity, while providing favorable growth conditions for be circumvented by increasing nitrate loading up to 130 mg L-1, how-
AOB and/or anammox bacteria. Therefore, MABR setup can be parti- ever, nitrate loading above this value adversely affects nitrate removal
cularly beneficial for allowing other bacteria to out-compete NOB. This (Rezvani et al., 2019). One known exception is Thiobacillus denitrificans-
setup is much more efficient in this respect compared to e.g. adjustment dominated biofilms, which completely remove nitrate even at a nitrate
of DO in liquid phase of suspended sludge systems (Picioreanu et al., loading rate of 600 mg L-1 h-1 and an HRT of 10 min (Zou et al., 2016).
2016). In aerobic conditions, AOB bacteria grow in the outer surface of While biological denitrification effectively converts nitrate to nitrogen
biofilms, NOB can be found several μm deeper, and anaerobic ammonia gas, it is not amenable to nitrogen recovery, which can be considered as
oxidation bacteria (AnAOB) are found in the anoxic interior. This ar- a drawback of this process.
rangement requires substrate diffusion among these different layers for
the full conversion (ammonium oxidation using nitrite, as electron ac- 3.2.1. Microorganisms involved in denitrification
ceptor, to produce nitrogen gas) (Cao et al., 2017). Another approach Both autotrophic and heterotrophic bacteria can reduce nitrate. A
for suppression of NOB in MBBR consists of supplying a small amount of limited number of autotrophic denitrifiers have been discovered.
oxygen (Gilbert et al., 2015). Furthermore, biofilm thickness is a critical Compared to the heterotrophic denitrifiers, they exhibit slow growth
property influencing the community structure and function. Aerobic with low biomass production and inefficient assimilation (Rezvani
nitrifiers were abundant in 50 μm biofilms whereas anaerobic ammo- et al., 2019). Autotrophic denitrifiers oxidize inorganic matters and the
nium oxidizers abundantly localized in 400 μm biofilms. Nitrifying released electrons are delivered to the nitrate as the terminal electron
biofilms differing in thickness are composed of different nitrogen- acceptor. There are two types of autotrophic denitrification: hydrogen-
transforming bacteria and vary in their nitrogen transformation rates based (Micrococcus denitrificans and Paracoccus denitrificans) and sulfur-
(Suarez et al., 2018; Suarez et al., 2019). based autotrophic denitrification (Thiobacillus denitrificans and T. thio-
parus), oxidizing H2 and sulfur compounds (such as elemental sulfur or
3.2. Denitrification thiosulfate), as the electron donors, respectively (Rezvani et al., 2019;
Zou et al., 2016). Di Capua et al. (2019) investigated twelve electron
Denitrification is the process of complete removal of nitrate to donors for autotrophic denitrification including hydrogen gas, chemi-
harmless nitrogen gas as the end product, with relatively low genera- cally synthesized and biogenic elemental sulfur, sulfide, thiosulfate,
tion of waste brine (Rezvani et al., 2019) (Fig. 2A). Denitrification sulfite, pyrite, thiocyanate, zero-valent iron, ferrous iron, arsenite and
treats various contaminants at the same time, leading to a reduced manganese. Denitrification kinetics was found to be strongly affected
waste disposal cost. For denitrification, several primary factors are es- by the type of electron donor. Regardless of safety issues, fast kinetics,
sential: requirement for strict anoxic conditions, carbon sources, and low biomass yield, ecosustainability and reasonable cost of H2, make it
post-treatment. Additional organic carbon sources work as the electron the most promising electron donor. Meanwhile, reduced inorganic
donor and are required for cell growth and heterotrophic denitrification sulfur compounds are alternative to H2, limiting effluent sulfate con-
(Modin et al., 2007; Miao and Liu, 2018). Glucose, alcohols such as centration and treating a wide range of nitrate-contaminated waters.
methanol and ethanol, succinate and acetate are the most common Tian et al. (2020) recently confirmed exclusive autotrophic iron-de-
carbon sources supplemented to the denitrification systems (Ji et al., pendent denitrification seeded with activated sludge. A novel sulfur-
2015; Miao and Liu, 2018). Due to the high biodegradability a wide based denitrification process coupled with iron(II) carbonate ore
range of biopolymers including poly(ε-caprolactone) (PCL), poly(buty- (SICAD system) synergistically enhanced denitrification rate (up to
lene succinate) (PBS); polyhydroxyalkanoates (PHAs), poly (l-lactic 720.35 g N/m3 d) with reduced accumulation of intermediates (NO2–
acid) (PLLA), polyvinyl alcohol (PVA), poly3-hydroxybutyrate-co-3- and N2O) and production of sulfate (Zhu et al., 2019). Sulfur oxidizing
hydroxyvalerate (PHBV)/PLA, starch/PCL, and starch/PVA are ex- bacteria including Acidithiobacillus thiooxidans and Thiobacillus deni-
amined for nitrate removal (Xu et al., 2018). It was also found that the trificans use iron sulfides as the efficient electron donors for autotrophic
aerobic methane oxidation by methanotrophic bacteria can serve or- denitrification treating nitrate in wastewater (Yang et al., 2017). OH−
ganic compounds acting as the electron donors for heterotrophic de- ions generated by dissolved S2− hydrolysis buffer H+ ions produced by
nitrification (Modin et al., 2008; Modin et al., 2010). autotrophic denitrification of iron sulphides, thereby eliminating the
In spite of several advantages offered by denitrification, these sub- need for alkaline reagents for neutralization. Sulfur autotrophic deni-
strates result in turbidity as the consequence of excessive biomass and trification also leads to SO42− accumulation. This issue is less serious in
remnant carbon source, thereby necessitating further treatment. iron sulfide autotrophic denitrification, probably due to the incomplete
There are several issues impeding large scale application of biode- S2− oxidation to SO4 2−.
nitrification. There is a risk of gaseous nitrous oxide production, which In wastewater treatment systems, Thiobacillus sp. comprises the
is a greenhouse effect-causing gas, more potent than the CO2 (Wang and majority of autotrophic denitrifiers (Miao and Liu, 2018). Interestingly,
Wang, 2013). The requirement for continuous carbon source supply is a cooperation of predominated hydrogenotrophic and heterotrophic de-
considerable burden, combined with the need for precise dosing to nitrifiers demonstrated a shift from autotrophic to heterotrophic deni-
avoid deterioration of effluent water quality by excessive biomass of trification in H2-based hollow-fiber membrane biofilm reactor (HF-
bacterial cells and remnant carbon source (Boley et al., 2000). Fur- MBfR) (Park et al., 2016).
thermore, presence of oxygen during denitrification negatively affects Faster denitrification reactions performed by heterotrophs require
nitrogen removal efficiency and increases nitrite concentration in smaller reactor volumes, thereby reducing the cost. Pseudomonas and
treated water. This negative effect of oxygen varies according to the Bacillus are the most common heterotrophic denitrifiers (Rezvani et al.,
type of electron donor used as the carbon source. For example, deni- 2019). Heterotrophic bacteria utilize carbon from the complex organic
trification is less affected by DO when using alcohols, such as ethanol compounds, prefer low to zero DO, and use nitrate as the terminal
and methanol, compared with sucrose as the carbon source (Gómez electron acceptor. Under both aerobic and anoxic environments, nitrate

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S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

can be removed by heterotrophic bacteria from wastewater. Under and SA–A was collected from an anaerobic sludge fermentation cou-
anoxic conditions, nitrate is used as the terminal electron acceptor for pling a anoxic denitrification reactor with a carbon source produced by
cell respiration instead of oxygen. Thus, nitrate gets reduced simulta- sludge fermentation. In denitrification process, SA and SA–A–O sludges
neously with oxidation of organic matters. Some bacteria, such as showed the transient accumulation of nitrite, however SA–A showed
Thiosphaera pantotropha, Alcaligenes faecalis, and Bacillus sp. possess the high nitrite accumulation with a nitrate-to-nitrite transformation ratio
capacity of aerobic denitrification, in addition to heterotrophic ni- (NTR) of 80% before the nitrate reduced completely. Therefore, it can
trification (Chen et al., 2015). DO concentration, carbon to nitrogen be assumed that the denitrifiers, reducing nitrate only to nitrite, are
ratio (C/N) as well as temperature and pH are known to influence dominated microorganism communities (Cao et al., 2013b). Further-
aerobic denitrification rates (Ji et al., 2015). There are several ad- more, nitrite accumulation due to inconsistent nitrite reductase and
vantages of aerobic denitrification using these organisms, such as high nitrate reductase activities is also induced in several conditions in-
growth rates, aerobic removal of ammonium and nitrate by simulta- cluding carbon-limited condition, type of carbon sources such as glu-
neous nitrification and denitrification, minimized acclimation pro- cose, pH and nitrate concentration, oxygen concentration and toxic
blems, and reduced requirement for buffering (alkalinity produced by compounds such as pesticide (Gong et al., 2013; Yang et al., 2012; Ge
denitrification partially compensates the alkalinity required for ni- et al., 2012; Glass and Silverstein, 1998; Cao et al., 2013c; Sáez et al.,
trification) (Chen et al., 2015). The nitrate and oxygen co-respiration in 2003).
these conditions are believed to result from microbial adaption to harsh Bioaugmentation is a biological approach of adding specific mi-
environment with high dosage of nitrate to degrade the toxic nitrogen croorganisms into a microbial community to enhance the capacity of
(Ji et al., 2015). microbial community for degradation of specific contaminants.
In wastewater treatment systems, members of the genera Thauera, Altogether, bioaugmentation with the strains that possess complete
Paracoccus, Hyphomicrobium, Comamonas, Azoarcus, Denitratisoma, denitrification capacity would be beneficial to achieve a complete de-
Dechloromonas, and family Comamonadaceae are the major denitrifiers nitrification system for wastewater treatment.
contributing into the nitrogen removal (Jiang et al., 2012; Baumann
et al., 1996; Carvalho et al., 2007; Cowan et al., 2005; Neef et al., 1996; 3.2.2. Reactor technologies in denitrification
Martineau et al., 2013; Gumaelius et al., 2001; Khan et al., 2002). In- 3.2.2.1. Simultaneous nitrification and denitrification (SND). SND
terestingly, microbial species composition in wastewater affects nitrite particularly for treating wastewaters with low C/N ratio (< 5) is the
accumulation in denitrification process. It can be due to the differential occurrence of both nitrification and denitrification simultaneously in
pattern of denitrification pathway in various bacteria. The denitrifying the same reactor and saving cost for anoxic tank (Guo et al., 2005). SND
bacteria contributing in nitrate removal are shown in Fig. 4, which are can be operated through the physical and biological mechanisms.
functioning in nitrite accumulation and or complete denitrification. Physical mechanism is based on gradient of DO due to limitation of
Three different patterns of denitrification process are found in waste- oxygen diffusion through the flocs or biofilms. The nitrifiers and
water treatment plants including i) reducing nitrate only to nitrite, ii) denitrifiers localize in higher (more than 1–2 mg L-1) and lower
reducing both nitrate and nitrite with no nitrite accumulation which the concentration of DO (less than 0.5 mg L-1), respectively (Zhu et al.,
rate of reducing nitrite is higher than that of nitrate in these bacteria, 2008). However, the biological mechanism of SND is based on the
iii) reducing nitrate and nitrite, along with a transient nitrite accumu- activity of heterotrophic nitrifiers and aerobic denitrifiers with the
lation which rate of nitrite reducing is lower than that of nitrate in these capacity of denitrification even at oxygen-saturated condition (Chen
bacteria (Ma et al., 2016; Martienssen and Schops, 1997). To demon- et al., 2015).
strate the effect of denitrifying community composition on nitrite ac-
cumulation, Cao et al. (2013a) investigated three different seeding 3.2.2.2. Shortcut nitrification and denitrification. Shortcut nitrification
sludges (SA, SA–A–O, SA–A). SA was collected from the anoxic zone in and denitrification also called as partial nitrification-denitrification, is
lab-scale anoxic and aerobic reactor treating domestic wastewater with feasible technology for treatment of wastewaters with high ammonium
a long SRT; SA–A–O was collected from an anaerobic/anoxic and concentrations or low C/N ratios. In this case, nitrite is produced by
aerobic reactor with high denitrifying phosphorus removal efficiencies; nitrification as an intermediate product instead of nitrate and
subsequently reduced to N2 by nitrite denitrification (Zhu et al.,
2008). There are several advantages by shortcut nitrification and
denitrification compared with the conventional nitrification and
denitrification via nitrate; i) 25% lower consumption of oxygen in
aerobic phase with 60% saving energy within whole process, ii) 40%
lower demand of electron donors in anoxic phase, iii) nitrite
denitrification rate is 1.5 to 2 times higher than nitrate denitrification
rate (Peng and Zhu, 2006).

3.2.3. Synthetic biology in denitrification

Quorum sensing (QS) including rhl and las -two acyl homoserine
lactone (AHL)-mediated QS systems- and Pseudomonas quinolone signal
(PQS) systems, is a cell–cell communication mechanism of Pseudomonas
playing crucial role in wastewater treatment (Kalia et al., 2018; Yong
et al., 2015). The denitrification activity of Pseudomonas aeruginosa
PAO1 was positively affected by QS mutants (Δ(Acyl-homoserine-lactone
synthase I)rhlI and ΔrhlR), indicating involvement of QS in denitrifica-
tion process (Yoon et al., 2002; Toyofuku et al., 2007). Regulatory
mechanism of denitrification by QS systems proposed that the deni-
trification processes can be improved by engineering of QS systems.
Furthermore, regulatory role of PQS signalling molecule in deni-
trification suggests potential regulation of denitrification process by
Fig. 4. Nitrite accumulation and complete denitrification by denitrifying bac- manipulation of PQS signalling molecule biosynthesis in various deni-
teria. trifying bacteria and microbial consortia (Toyofuku et al., 2008).

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3.3. Anammox denitrifying bacteria are able to compete with anammox bacteria re-
sulting in lower ammonium removal efficiency. In addition, certain
Anaerobic digestion, transforming organic materials into mostly organic compounds, such as methanol, inactivate anammox activity
CO2 and methane (CH4) is one of the technologies for commercial completely or partially (Ali and Okabe, 2015). Low concentrations of
production of energy from waste (Appels et al., 2008). The transfor- organic matter do not significantly affect anammox activity, so nitrogen
mation of organic matter into biogas (60–70 vol% of CH4) by anaerobic removal in the presence of low concentrations of organic matter can be
digestion reduces final sludge solids, destroys most of the sludge pa- promoted via heterotrophic denitrification. This process is called si-
thogens and decreases odour problems associated with the residual multaneous nitrification, anammox and denitrification (SNAD)
putrescible matter (Appels et al., 2008). Hydrolysis, acidogenesis, (Fig. 5A) (Lan et al., 2011), and can be used for treatment of main-
acetogenesis and methanogenesis are the subsequent steps in anaerobic stream wastewater. Optimal temperature for anammox process is 37 °C
digestion of organic materials. Organic matter as the main energy re- (Fig. 5B, Table 2), however, at 45 °C anammox irreversibly loses ac-
source is used by the anaerobic methanogenic bacteria during metha- tivity due to the biomass lysis. Anammox bacteria can adapt to lower
nogenesis step of anaerobic digestion process. However, it is also used temperatures and they are able to grow and maintain their activity at
by the heterotrophic denitrifiers present in wastewater microbial 10-20 °C in wastewater. Anammox activity can be detected at tem-
community thereby lowering energy production by methanogenic peratures as low as 4 °C in laboratory conditions (Oshiki et al., 2011). It
bacteria. However, nitrogen removal by autotrophic microorganisms was shown when temperature decreased to 15 °C, the maximum reactor
would be preferable, since it leaves the organic matter for methano- capacity and system stability negatively affected due to nitrite accu-
genic bacteria during wastewater treatment. Autotrophic denitrification mulation. However, anammox was adapted to low temperature and no
(Ma et al., 2016), photoautotrophic systems (Ma et al., 2016) and changes in sludge physical properties and/or bacterial populations were
anammox processes (Kartal et al., 2010) are the autotrophic nitrogen found during the operation (Dosta et al., 2008). In contradiction with
removal approaches. Among them, anammox process seems to be the previous finding, prolonged cultivation of anammox bacteria at 20 °C
most promising for energy-neutral or energy-generating sewage treat- results in deterioration of biomass-specific activity due to the required
ment (Kartal et al., 2010). In the anammox process, nitrite and am- long SRT in the system. The SRT controls the bacteria concentration
monium are utilized to form nitrogen gas through NO and N2H4 in- within the treatment and higher SRT can contribute to a higher bac-
termediates (Fig. 2B). In 2002, the first full-scale anammox reactor was terial concentration in the reactor. Long SRT causes non-active and non-
set up for treatment of reject water at Dokhaven, Rotterdam, Nether- anammox bacterial cells such as heterotrophs growing on minimal or-
lands. In 2015, there were reportedly 114 full-scale anammox in- ganic carbon present in the influent and becoming dominant in the
stallations around the world with a capacity to treat 134 tons of N per reactor, thereby decreasing the biomass-specific activity (Hoekstra
day (Ali and Okabe, 2015). Along with increasing number of installa- et al., 2018).
tions, capacity volume of the anammox plants is also increasing. These Average NH4+ and NO3− concentrations of 100 and 50 mg L−1 are
full-scale treatment plants are mainly treating reject water streams, found in the effluent of full-scale anammox installations, respectively
however, in terms of nitrogen loading rates, their main targets are (Ali and Okabe, 2015). Hence, the effluent water quality needs to be
glutamate and amino acids industries and slaughterhouses (Ali and improved to meet the effluent discharge standard by further post-
Okabe, 2015). treatment (increasing the cost and energy consumption).
Anammox bacteria oxidize ammonium using nitrite as the electron
acceptor. Nitrite can be obtained from nitritation (oxidizing ammonium 3.3.1. Microorganisms involved in anammox
to nitrite) and partial denitrification (reducing nitrate to nitrite) (Ali Anammox is a recently discovered process in the nitrogen cycle. The
and Okabe, 2015). Thus, nitritation/anammox and partial denitrifica- representative anammox bacteria are Candidatus “Brocadia anammox-
tion/anammox can remove biological nitrogen from wastewater idans” and Candidatus “Kuenenia stuttgartiensis” (Shoda, 2017). Ana-
(Table 2). Since both anammox and nitritation are autotrophic pro- mmox bacteria belonging to phylum Planctomycetes (Strous et al.,
cesses, they are advantageous compared with nitrification/denitrifica- 1999) and are ubiquitously found in anoxic environments such as
tion, since they do not utilize the carbon sources present in the was- marine, freshwater and terrestrial ecosystems, where the nitrogen loss
tewater. By comparison, nitrification/denitrification can use up to mainly occurs due to anammox processes (Ali and Okabe, 2015). About
100% of organic matter present in treated wastewater. With nitritation/ nineteen species and broadly six genera of anammox bacteria have been
anammox, methane can be produced using organic matter, thereby characterized. No pure culture was found for anammox species, how-
enhancing energy recovery from wastewater (Kartal et al., 2010). ever, some of the anammox cultures have been enriched as the mono-
Furthermore, energy consumption can be reduced due to about 60% species in laboratory conditions (Oshiki et al., 2011).
less oxygen demand in nitritation/anammox processes, and only ap-
proximately 50% of the ammonium must be oxidized to nitrite instead 3.3.2. Reactor technologies in anammox
of nitrate. In addition, surplus sludge production is minimal with ni- 3.3.2.1. Simultaneous partial nitrification, anammox, and denitrification
tritation/anammox, due to lower cell production but higher rate of (SNAD). As there is no demand of organic carbon for the anaerobic
nitrogen removal (Du et al., 2015; Kartal et al., 2010). The chemoau- conversion of ammonia to N2 by anammox, it is an attractive
totrophic anammox utilizes inorganic carbon source of CO2 as it can technology for the treatment of nitrogen rich wastewaters. However,
positively affect the anammox growth and activity. Therefore, nitrita- combination of partial nitrification with anammox through the
tion/anammox processes could also decrease the emission of green- SHARON (single reactor high activity ammonia removal over nitrite)-
house gases due to consumption of inorganic carbon CO2 as well as anammox (two-reactor system) and CANON (completely autotrophic
lower N2O emission (Du et al., 2015). nitrogen removal over nitrite in single reactor system) produces the
Besides the above-mentioned advantages of anammox process, there electron acceptor nitrite required for anammox process. However, these
is one crucial shortcoming: usually excessive amounts of nitrate are two processes are not able to eliminate organic carbon along with
introduced into the effluent. Consequently, a post-denitrification pro- ammonium. Furthermore, nitrate production in the system making the
cess is required to meet the discharge standard, which is in demand of necessity of further treatment. Therefore, SNAD process (simultaneous
external carbon source (Modin et al., 2007) (Fig. 5A). This comes at a partial nitrification, anammox, and denitrification) has been developed
cost: energy consumption, surplus activated sludge and CO2 emission. for simultaneous removal of inorganic nitrogen and organic carbon. It
High C/N ratio, low temperature, and poor effluent water quality conducts three chemical reactions by three bacterial communities
are the main challenges for application of anammox process in treating aerobic AOB, anammox, and denitrifying bacteria in a single reactor
mainstream wastewater. When organic matter is present, heterotrophic under oxygen limiting conditions (Fig. 3C) (Chen et al., 2009) (Fig. 5A).

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Fig. 5. Anammox process with the need of post denitrification treatment leading SNAD (simultaneous nitrification, anammox and denitrification) process (A). In
SNAD process, ammonia is partially oxidized to form nitrite, and then anammox and denitrification together remove ammonia and nitrate, respectively. Comparison
of the nitrogen removal efficiencies at various temperatures (B), the graph was drawn based on the data shown in Table 2.

Nitrate production in mainstream anammox process and variation the conventional biological nutrient removal such as i) 100% reduced
in nitrite to ammonium ratio result in poor quality of anammox effluent demand of aeration, ii) simultaneous nitrate and ammonium removal
with total nitrogen concentration of above 10 mg N L−1 (Xie et al., with 80% reduced demand of organic carbon, iii) 64.8% reduced sludge
2018). The counter-diffusion delivery in MABR allows a higher effi- production, iv) low nitrogen contained wastewater, low/high-strength
ciency of gas transfer and substrate consumption compared to the nitrate and ammonium containing wastewater, and v) significant
conventional methods (Xie et al., 2018). The gaseous methane delivery reduction in greenhouse gas (CO2 and N2O) emission (Cao et al.,
through the membrane causes growth of denitrifying anaerobic me- 2019a).
thane oxidation (DAMO) organisms along with anammox bacteria.
Thus, nitrate produced by anammox reaction is consumed by DAMO 3.3.3. Synthetic biology in anammox
organisms. If the feed has non-optimal nitrite to ammonium ratio for AHLs-regulated metabolic pathways and AHLs-mediated QS me-
the anammox reaction, the additional nitrite is also removed by DAMO chanism in wastewater treatment were explored in anammox consortia
organisms. Therefore, combination of anammox and denitrifying (Sun et al., 2018; Tang et al., 2018). Anammox fed with influent
anaerobic methane oxidation (DAMO) has been established in MBfR to comprising high ammonium concentration enriched more QS organ-
improve the mainstream anammox process. High nitrogen removal rate isms producing more AHLs, which likely benefited anammox activity.
and satisfactory effluent quality are achieved by this method in main- Furthermore, more hydrophobic amino acid and protein were produced
stream wastewater treatment (Xie et al., 2018). in extracellular polymeric substances (EPS). Thus, active QS and EPS
synthesis in anammox might cause high nitrogen removal capacity and
3.3.2.2. Denitrifying ammonium oxidation (DEAMOX). DEAMOX is the dense biofilm (Sun et al., 2018). AHLs-mediated regulation of anammox
novel process of anammox coupling with partial denitrification (nitrate activity, growth rate, and EPS production implied that genetically en-
generates nitrite) simultaneously treats ammonia and nitrate containing gineered bacteria carrying signal gene for AHLs synthesis could im-
wastewaters. It obtains a stable performance (total nitrogen removal of prove nitrogen removal rate or biomass aggregation and thereby
93.6%) despite the seasonal changes of temperature (29.2 °C–12.7 °C). overcoming limitations of long start-up required for wastewater treat-
It is due to enhanced anammox activity by high accumulation of nitrite ment in anammox reactor (Tang et al., 2018).
through the partial-denitrification process (Du et al., 2017).
Interestingly, the partial-denitrification process creates broader range 3.4. Nitrogen removal from industrial wastewater
of capacity for application of anammox technology (Fig. 3D). This
economically recommended technology has advantages compared to Industrial wastewaters containing over 500 mg L-1 ammonium are

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S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

produced from oil refining, organic chemicals, glass manufacturing, evolution (ALE) can be used to facilitate NPs removal, thereby cir-
feed production, chemical fertilizer, iron alloy, meat processing, animal cumventing the necessity of ecological safety evaluation for introduc-
husbandry, pharmaceutical industry, and other industries (Tabassum tion of GMM into contaminated sites (Elena and Lenski, 2003;
et al., 2018). Industrial wastewater treatment was developed using Chaudhary and Kim, 2019). Pseudomonas sp. strain WBC-3 is an ex-
various anammox processes, as one-stage nitritation/anammox system ample of NP-degrading bacteria that evolved to utilize 2-chloro-4-ni-
is feasible to treat numerous types of ammonium-enriched industrial trophenol (2C4NP) as a growth substrate in an ALE experiment. The key
wastewaters (Zhang et al., 2015; Miao et al., 2014; Wang et al., 2016b; mutation obtained by ALE was detected in a transcriptional regulator
Shen et al., 2012; de Graaff et al., 2011; Tang et al., 2011; Molinuevo PnpR, which activated expression of pnpA and pnpB operons. These
et al., 2009; Daverey et al., 2013). Complex components (heavy metals, genes encode enzymes for the initial reactions in NP and 2C4NP cata-
antibiotics and salinity) present in ammonium-enriched industrial bolism. In the mutated ALE strain, they were strongly expressed in the
wastewaters affect anammox activity, autotrophic nitrogen removal absence of inducer and even higher induction was obtained by inducer
performance, microbial community structure transformation, and supplementation (Deng et al., 2019). Similarly, Acidovorax sp. strain
system stability (Li et al., 2018). Therefore, studying impact of these JS42 was able to grow either on 3-nitrotoluene (3NT) or on 4-ni-
components on anammox is of practical significance to provide insights trotoluene (4NT) after and ALE experiement, due to variations in 2-
on anammox technology for treatment of different industrial waste- nitrotoluenene 2,3-dioxygenase (2NTDO) and evolved activities of
waters. 2NTDO against 3NT and 4NT (Mahan et al., 2015). Therefore, the ALE-
High concentration of nitrate is also discharged from certain in- based approaches can be suggested to optimize the capacity for bio-
dustries including stainless steel pickling rinse wastewater (450 mg L-1), degradation of toxic nitro group-containing components.
fertilizer industry (950 mg L-1), liquid-liquid extraction process of ur-
anium nitrate raffinate (up to 77,000 mg L-1) (Fernández-Nava et al., 3.5. Bioelectrochemical systems
2008; Zala et al., 2004; Biradar et al., 2008). Partial denitrification
coupled with anammox process (PD-A) is a new approach for nitrate- Specific interests are found in bioelectrochemical reactors for ni-
enriched industrial wastewater treatment (Cao and Zhou, 2019). Toxic trogen removal from wastewaters, along with energy and/or chemicals
substances including metals, fluoride, sulfate, chloride, toxic organics production. Significant progress has been made to improve bioelec-
present in nitrate-enriched industrial wastewaters could affect nitrate trochemical system technology for large-scale treatment of various
and nitrite reductase activities, nitrite production for anammox process wastewaters (Fig. 6B, Table 3). Bioelectrochemical systems utilize
and likely anammox activity (Jin et al., 2012). Granular sludge with electrochemically active microorganisms (bioanode/biocathode) with
compact physicochemical structure as well as protection mechanisms extracellular electron transfer capacity. Electrons driven by oxidation of
offered by EPS enhance tolerance of microorganisms to toxic com- pollutants are transferred into the anode, resulting in pollutants re-
pounds (Cao and Zhou, 2019). Furthermore, granules are able to absorb moval such as organic matter decomposition. According to the type of
toxic substances. Therefore, granule-based systems should be favoured cathodic reaction, there are two types of bioelectrochemical systems:
to mitigate negative effects of toxic components in nitrate-enriched microbial fuel cells (MFCs), which generated electrical power because
industrial wastewater. the anodic oxidation is coupled to a cathode reducing an electron ac-
ceptor with high reduction potential (such as O2, Fe3+, and Cu2+) and
3.4.1. Removal of nitro group-containing chemicals from industrial microbial electrolysis cells (MEC), which require electrical power be-
wastewater cause the anodic oxidation is coupled to a cathode operated at low
Industrial wastewater also contains toxic nitro group-containing potential, for example for the reduction of protons to hydrogen gas
chemicals such as nitrophenols (NPs) composed of benzene rings and (Rodríguez Arredondo et al., 2015).
nitro (-NO2) and hydroxyl (-OH) groups. NPs are widely used as a raw
material and intermediate in production of pharmaceuticals, pigments, 3.5.1. Denitrification by bioelectrochemical systems
wood, preservatives, dyes, pesticides, explosives and rubbers, while Biological nitrogen removal using bioelectrochemical systems is
listed as a priority pollutant (Park and Bae, 2018; Keith and Telliard, based on denitrification at the cathode (Rodríguez Arredondo et al.,
1979). Common methods for NPs wastewater treatment are adsorption, 2015; Wu and Modin, 2013). Denitrification can be performed in the
extraction and oxidation. These are complicated and costly processes cathode compartment of BES either by the production of H2, which is
and generate secondary pollution. However, NPs can be consumed as consumed by denitrifying autotrophs (Fig. 6A) or by denitrifiers di-
the sole carbon sources by some bacteria, which is a basis for an ef- rectly accepting electrons from the cathode surface. An MFC func-
fective technology of their removal from the environment (Arora et al., tioning with acetate as electron donor at the anode and nitrate as
2014; Xiong et al., 2019). Microbial degradation of NPs is considered to electron acceptor at the cathode was demonstrated by Clauwaert et al.
be efficient when the concentration of NPs is under 200 mg L-1. Re- (2007). Another study showed that denitrification is enhanced with a
cently, Mei et al. (2019) constructed an integrated membrane-aerated constant electric field in a continuous stirred tank reactor (CSTR), when
bioreactor system with anoxic and aerated zones. Using this reactor, the cathode potential is maintained constant around the standard po-
efficient simultaneous removal of NPs (95.86%) and nitrogen (94.81%) tential value of the nitrate/nitrite redox couple (Parvanova-Mancheva
was demonstrated on influent water with NPs concentration of 500 mg and Beschkov, 2009). The denitrification rate is influenced by applied
L-1. The presence of different types of NP molecules in aqueous solution potential and current. When DO level is low, the positive effect of
limits bacterial remediation (Xiong et al., 2019). current on nitrate removal is elevated (Sakakibara and Kuroda, 1993;
Tanaka and Kuroda, 2000).
3.4.2. Synthetic biology in removal of nitro group-containing chemicals There are several advantages offered by bioelectrochemical
from industrial wastewater methods of wastewater treatment, including removal of specific con-
Genetically modified microorganisms (GMM) show potential for taminants, reduced environmental footprint, stable operation at or-
degrading pollutants in wastewater, but bio-environmental concerns dinary environmental temperatures, processing speed, and cost-effec-
restrict their applications. For example, Bacillus cereus strain isolated tiveness due to cheap and self-propagating microorganisms. This type
from pulp and paper wastewater effluent showed higher degradation of of treatment also uses wastewater as a renewable source of energy
NPs when it expressed a heterologous vgb gene encoding hemoglobin- (Kato, 2015; Rajmohan et al., 2016). Furthermore, bioelectrochemical
like protein, Vitreoscilla Hemoglobin b (VHb) from Vitrocilla stercoraria systems can easily be coupled with other techniques or may be used for
(Vélez-Lee et al., 2016). As an alternative to such targeted genetic en- post-treatment of effluents of other techniques. For example, the anodic
gineering, genetic mutations obtained during adaptive laboratory oxidation of organic matter produces electricity, while denitrification

12
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Fig. 6. Bioelectrochemical system for biological nitrogen removal from wastewater (A). Comparison of the nitrogen removal efficiencies of different bioelec-
trochemical setups (B), the graph was drawn based on the data shown in Table 3. ⁎Measurement is based on net cathodic compartment (NCC), ⁎⁎Total compartment
volume (TCV), ⁎⁎⁎Net cathode volume (NCV).

occurs at the cathode. In addition, an external nitrification reactor en- denitrifying biofilms in anaerobic denitrification and under low DO
ables the removal of ammonium from wastewater (Virdis et al., 2008). condition. Increasing DO results in a change of the predominant
Even simultaneous nitrification and denitrification can be achieved by phylum to Proteobacteria, predominantly α, β, and γ, classes (Zhao
optimizing the oxygen supply in the aerated cathode chamber of an et al., 2017). Several proteobacteria such as Geobacter, Shewanella,
MFC (Virdis et al., 2010). Furthermore, a tubular dual-cathode MFC Acidithiobacillus, as well as Bacteroidetes, Chloroflexi, and Gram-positive
with an anoxic inner cathode for denitrification and an aerobic outer bacteria Firmicutes, and Archaea have extracellular electron transfer
cathode for the nitrification process was designed using both anion and ability which can support applications in bioelectrochemical systems
cation exchange membranes (Zhang and He, 2012). Interestingly an for wastewater treatment (Kato, 2015). Enrichment of the electro-
algal biofilm (AB) integrated with an MFC was established as an algae chemically active bacterial community on the electrode can be posi-
biofilm microbial fuel cell (ABMFC). It was shown to facilitate nitrogen tively affected by the electrode pre-treatment, optimization of poten-
and phosphorous removal much better than an AB and MFC alone. In tial, current, external resistance, chemical additions, bioaugmentation
case of bioenergy generation, ABMFC produced 18% higher power and temperatures (Butti et al., 2016). Our understanding of the mi-
density than the MFC alone (Yang et al., 2018). Another example of crobial extracellular electron transfer is not complete, and further stu-
combining MFCs with other technology comes from the cheese industry dies are needed to provide engineering strategies for improving bioe-
wastewater treatment. This type of wastewater is treated with a lectrochemical reactors.
membrane bioelectrochemical reactor coupled with an MFC, in which
contaminants such as COD, suspended solids and nitrite are removed by 3.5.3. Synthetic biology in bioelectrochemical systems
MFC. Since ratio of energy recovery and consumption is more than one Phenazines, heterocyclic nitrogen-containing and redox active sec-
thereby energy gets recovered. Moreover, a high-quality effluent is ondary metabolites, are produced by Pseudomonas (Mavrodi et al.,
obtained by post-treatment in multiple bioelectrochemical reactors (Li 2006). Regardless of whether phenazines are produced by Pseudomonas
et al., 2014). or by chemical synthesis, they play a crucial role as electron shuttles for
extracellular electron transfer between bacteria and electrodes and
3.5.2. Microorganisms involved in bioelectrochemical systems thereby enable efficient electricity production in MFC (Jayapriya and
Denitrification by autotropic microorganisms requires CO2 as the Ramamurthy, 2012; Pham et al., 2008; Rabaey et al., 2005). Phenazine
inorganic carbon source and hydrogen as the electron donor (Ghafari biosynthesis by Pseudomonas species is regulated by QS systems (Yong
et al., 2008). However, faster denitrification reaction rate by hetero- et al., 2011). Engineered QS systems in P. aeruginosa (overexpressing
trophs requires smaller reactor volumes, thereby reducing the cost and rhlI and rhlR genes) resulted in higher phenazine biosynthesis, efficient
time. Firmicutes (Bacilli) are the dominant component of cathodic extracellular electron transfer and thereby enhanced electricity

13
 Table 3
Bioelechtochemical systems performance for removal and recovery of nitrogen.
Reactor type System Type of wastewater Removal mechanism Removal efficiency/ Current density A m−2 References
S. Rahimi, et al.

rate

Single-chamber MFC Air-cathode Swine wastewater Ammonia removal 60% NA Kim et al. (2008)
Dual-chamber MFC Anode with ferricyanide catholyte Swine wastewater Ammonia removal 69% NA Kim et al. (2008)
Dual-chamber MFC Gas diffusion cathode Urine Ammonia removal 3.3 g N m−2 d−1 0.5 A m−2 Kuntke et al.
(2012)
Dual-chamber MFC Urine Ammonia removal 9.57 g N m−2 d−1 2.6 A m−2 Kuntke (2013)
Three compartment H2 recycling electrochemical system Synthetic urine Ammonia removal 335 gN m−2 d−1 50 A m−2 Kuntke et al.
electrochemical system (HRES) (2017)
Dual-chamber MEC Batch cathode Urine Ammonia removal 162.18 g N m−2 d−1 14.7 A m−2 Kuntke et al.
(2014)
Dual-chamber MFC Tubular reactor with an internal Synthetic Nitrate reduction 146 g N m−3 NCC d−1 35 A m−3 Clauwaert et al.
cathode (2007)
Dual-chamber MFC Carbon and nitrogen removal Synthetic Carbon removal, 67.4% TN, 410 g NO3- 133 A m−3 INCLUDEPICTURE "https:// Virdis et al.
nitrification, m−3 NCC d−1 www.rsc.org/images/entities/char_2009.gif" \* (2008)
denitrification MERGEFORMATINET NCC
Dual-chamber MFC In situ nitrification Synthetic Simultaneous nitrification 94.1% TN, 104 g N 39.7 A m−3 TCV Virdis et al.
and denitrification m−3 TCV d−1 (2010)
Dual-cathode MFC Tubular dual-cathode MFC Synthetic Nitrification and 67–90% TN, 140 g TN 43 Am-3 Zhang and He
denitrification m−3 d−1 (2012)
Single-chamber MFC Diethylamine-functionalized Synthetic Simultaneous nitrification 96.8% 3.6 A m−2 Yan et al. (2012)
polymer (DEA) as the Pt catalyst and denitrification
binder
Dual-chamber MFC/MEC Anion exchange membrane (AEM) Synthetic Ammonia removal 2.94 g N m−2 d−1 3.6 A m−2 Haddadi et al.
(2013)
Dual-chamber MFC/MEC Cation exchange membrane Synthetic Ammonia removal 8.5 g N m−2 d−1 3.6 A m−2 Haddadi et al.

14
(2013)
Dual-chamber MFC/MEC Cation exchange membrane Synthetic Urea removal 37.8 g N m−2 d−1 5 A m−2 Haddadi et al.
(2013)
Biofilm-electrode reactor Synthetic Nitrate removal 0.17 mg NO3-N cm-2 NA Park et al. (2005)
biofilm surface area d-
1

Integrated SNAD-MFC Short-cut nitrification and University of Connecticut Ammonia removal 99.9%, 12.5 g N m-3 0.158 mA/cm2 Li et al. (2016b)
autotrophic denitrification (SNAD)- Wastewater Treatment Facility
MFC UConn-WTF
Flat-panel air-cathode MFC FA- Two separator electrode assembly Domestic wastewater Organic and nitrogen 620 g N m−3 d−1 401 ± 13 A m−3 Park et al. (2017)
MFC (SEA) compounds removal
MFC Aerobic nitrification in the cathode, Recirculating aquaculture Nitrate, ammonia removal 51 g N m−3 NCC d−1 74.00 A m−3 Zou et al. (2018)
heterotrophic denitrification in the system (RAS) water
anode
Upward plug-flow baffled-reactor Autotrophic cathodic denitrifying Synthetic Nitrate removal 148.3 ± 1.4 g N m−3 76.5 ± 0.5 A m−3 NCV Al-Mamun et al.
MFC NCV d−1 (2017)
−3
Dual-chamber MFC Seawater bacteria Synthetic Nitrate removal 100% 26.6 A m Naga Samrat et al.
(2018)
MFC and electric membrane Proton exchange membrane (PEM)- Synthetic Phosphorus, ammonia > 93% 0.0137 A m−2 Gao et al. (2017)
bioreactor (EMBR) free MFC removal
Dual-chamber MFC Single MFC reactor with zero alkaline Tannery wastewater Carbon and nitrogen 97.9% 0.83 A m−2 Wu et al. (2018)
consumption removal
−3 −1 −3
MFC and MEC Continuous-flow membraneless MFC Synthetic, municipal wastewater Carbon and nitrogen 0.38 g N m d 0.34 A m Hussain et al.
and MEC systems removal (2016)
Dual-chamber MFC Anion exchange membrane AEM Synthetic Nitrate removal 48 g NO3- m−3 d−1 23.7 A m−3 Lee et al. (2018)
Algae biofilm microbial fuel cell Integrating an algal biofilm (AB) Domestic wastewater Carbon and nitrogen 96% 0.17 A m−2 Yang et al. (2018)
(ABMFC) with a MFC removal

NCC: net cathodic compartment; TN: total nitrogen. d TCV: total compartment volume; NCV: net cathode volume.
Biotechnology Advances 43 (2020) 107570
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

production in MFCs. These results imply that engineering the QS system cation exchange membranes, which significantly affects the perfor-
is a promising strategy for improving the efficiency of bioelec- mance of bioelectrochemical reactors (Prosnansky et al., 2002; Sleutels
trochemical systems. et al., 2017).
Performance of bioelectrochemical reactors has significantly im-
4. Nitrogen recovery proved recently, as the current density of 400 A m-3 has been achieved
in flat-panel air-cathode MFC (FA-MFC) with a promise for energy
Nitrogen is one of the key nutrients for survival of living organisms. sustainable wastewater treatment (Park et al., 2017). To achieve
It is an important constituent of several biomolecules such as proteins practical application of bioelectrochemical systems, it is expected that
and DNA. Large proportion of nitrogen exist in N2 gas form in the at- the full-scale bioelectrochemical reactors should exhibit a volumetric
mosphere. However, it cannot be utilized by most of living organisms current density of 1000 A m-3 reactor volume (Rozendal et al., 2008).
except some bacteria. Instead, it should be converted to reactive forms The challenge is still scaling-up of bioelectrochemical reactor volume
such as nitrate, nitrite, ammonium, and ammonia to be used as a nu- from lab scale reactors to larger volume with less internal resistance.
trient by living organisms. To supply food to a growing human popu-
lation, large amounts artificial fertilizers are applied to agricultural 4.2. Nitrogen recovery by microalgae and cyanobacteria
land. The nitrogen content of artificial fertilizers is obtained by con-
verting N2 using the Haber-Bosch process, which is very energy-in- Unicellular species of microscopic photosynthetic microorganisms,
tensive. The fixation of N2 and application of fertilizers have led to an microalgae and cyanobacteria, are present in freshwater and marine
excess of reactor nitrogen in the environment, which has caused pol- systems. Their cells can exist individually or in chains or groups and are
lution. Recovery of reactive nitrogen from wastewater for use in food characterized by relatively fast growth and adaptability to harsh con-
production could thus contribute both to lower energy consumption ditions. Microalgae and cyanobacteria have been recently considered as
and less pollution (Matassa et al., 2015). Two biological techniques that an alternative system for biological wastewater treatment with several
potentially could be used for nitrogen recovery include bioelec- applications (Delgadillo-Mirquez et al., 2016; Sood et al., 2015). In
trochemical systems and photosynthetic microorganisms. Bioelec- wastewater treatment, they photosynthetically generate O2, which is
trochemical systems have a wide range of applications including ni- consumed by bacterial populations to decompose organic wastes to
trogen removal and recovery from wastewaters while producing simple inorganic nutrients. Furthermore, microalgae and cyanobacteria
electricity. Photosynthetic microorganisms include eukaryotic micro- remove inorganic nutrients in tertiary treatment before discharge to
algae and prokaryotic cyanobacteria, which can assimilate nitrogen and receiving waters (Taziki et al., 2015; Pouliot et al., 1989). Large
phosphorus present in wastewaters and recycle them in the form of amounts of nitrogen and phosphorus are required for fast growth of
microalgal biomass for producing fertilizers. Nitrogen can be alter- microalgae and cyanobacteria, which can be effectively provided by
natively removed or recovered by chemical methods, such as stripping uptake of nitrogen and phosphorus from wastewaters. Their potential
process and struvite precipitation. Table 4 presents nitrogen recovery for nitrogen recovery is the specific advantage of these microorganisms.
efficiency, chemical input, economic evaluation and main technical Nitrate and ammonia assimilated by microalgae and cyanobacteria are
parameters of different nitrogen recovery processes. converted to biomass rather than being released to the atmosphere as
the N2 gas by the dissimilatory nitrate reduction (Taziki et al., 2015).
4.1. Ammonia/ammonium recovery by bioelectrochemical systems The nitrogen removal capacity of microalgae and cyanobacteria relies
on ammonification and assimilatory reduction of nitrite to ammonium
Biological nitrogen recovery using bioelectrochemical systems is (Fig. 2B). Nitrogen is fixed by cyanobacteria converting atmospheric
based on ammonia/ammonium recovery (Rodríguez Arredondo et al., molecular nitrogen into ammonia through the following reaction;
2015; Wu and Modin, 2013). In the first mechanism, the biological N2+8H++8e−+16ATP→2NH3+H2+16ADP+16Pi. Later, it can be
oxidation of organic matter in wastewater at the anodic compartment incorporated into the amino acids and proteins or excreted to the en-
contributes to energy recovery. At the same time, the ammonia/am- vironment (Barsanti and Gualtieri, 2006).
monium in the wastewater is transported through the cation ion ex- NH4+, NO3−, and NO2− are fixed nitrogen forms which can be
change membrane to the cathode compartment with elevated pH assimilated and transported into the microalgae. NO3− is the most
catholyte, leading to ammonia recovery by stripping (Fig. 6A). The oxidized and stable inorganic form of nitrogen in aquatic environments.
electric field induces the ammonia/ammonium migration across the ion It needs to be reduced into NH4+ before assimilation. It goes into a two-
exchange membrane. This process ultimately allows for chemical re- step process catalysed by the cytosolic nitrate reductase and chlor-
covery of ammonia/ammonium from wastewater in a bioelec- oplastic nitrite reductase through the following reactions, NO3−+2H+
trochemical system. Ammonium recovery is also performed from urine +2e−→NO2−+H2O, NO2−+8H++6e−→NH4++2H2O (Barsanti
with a pre-treatment step for phosphate recovery via struvite pre- and Gualtieri, 2006) (Fig. 7A). NH4+ (resulting from NO3− and NO2−
cipitation (Rodríguez Arredondo et al., 2015). Ammonium was re- reduction) is incorporated into the amino acids via glutamate dehy-
covered from urine at rate of 9.7 gN m−2 d−1 with an energy yield of drogenase (at high levels of ammonium concentrations) or glutamine
−10 kJ gN−1 at a current density of 2.6 A m−2 (Kuntke, 2013). synthetase/glutamate synthase cycle (at low levels of ammonium con-
Bioelectrochemical systems can also support ammonium oxidation centrations) (Barsanti and Gualtieri, 2006; Taziki et al., 2015).
at the cathode. Modin et al. (2011) also utilized the alkalinity produced Higher production of biomass and absence of structural carbon such
in the cathodic compartment of an MFC to support nitrification of reject as cellulose in cyanobacteria and microalgae (C/N 5-20) make them
water. Yan et al. (2012) used a cathode pre-enriched with a nitrifying more efficient in water reclamation and nitrogen recovery compared
biofilm in a single-chamber MFC. The nitrifiers scavenged oxygen and with complex plants (C/N ratio 18-120) (Taziki et al., 2015). Phylo-
oxidized ammonium at the gas-diffusion electrode. genetic position of nitrate reductase and nitrite reductase in microalgae
In spite of many advantages of reactors, there are several issues with in comparison with other organisms was demonstrated in phylogenetic
this technology. Electrolytes in bioelectrochemical systems have large trees constructed via the Neighbour-Joining method and established the
number of cations and anions other than H+ and OH−. The transport of reliability of each node through bootstrap methods, using MEGA 4
these cations and anions through the ion exchange membranes de- (Fig. 7B, C). Furthermore, the chloroplast localization of nitrate re-
termines the pH gradient between the anode and cathode as well as the ductases and nitrite reductases was investigated using Target P and
membrane potential. Although transport of NH4+ is beneficial for N Chloro P and shown by green arrow in Fig. 7B and C. As it was shown,
recovery in some systems, pH gradients as well as concentration gra- nitrate reductase in some but not all of higher plants is located in
dients of other cations than H+ are responsible for potential loss in chloroplast while this enzyme is localized in chloroplast of microalgae

15
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Chlorella sorokiniana and Dunaliella salina. Immuno-specific electron

microscopy observation has indicated that the nitrate reductase is lo-

environmental factors (pH, temperature, light, O2, and CO2)

wastewater characteristics (nutrients and toxic compounds),
Requires vast land area for installing ponds, optimization of
control, resistance for electron transfer, large-scale reactor,
Biocatalyst microorganism, electrode materials, reaction calized in pyrenoids of Monoraphidium braunii, Chlamydomonas re-

long-term durability, cost of electrode materials, cost of

inhardii, Chlorella fusca, Dunaliella salina, and Scenedesmus obliquus
(Lopez-Ruiz et al., 1985). Pyrenoids are sub-cellular micro-compart-
ments in microalgal chloroplasts, with a possible role in photosynthesis.
Both photosynthesis-derived nicotinamide adenine dinucleotide

pH, temperature and mass transfer area

(NADH) and nicotinamide adenine dinucleotide phosphate (NADPH)
can be used as the electron donors for nitrate reduction in Chlorella sp.
fabrication and cost of operation

Therefore, it can be hypothesized that the energy-intensive process of

Molar ratio of Mg:NH4:P, pH
nitrate reduction may be the reason for the chloroplast localization of
Main technical parameters

nitrate reductase in microalgae (Taziki et al., 2015).

Nitrogen and phosphorus taken up by microalgal biomass can be
used for producing fertilizers, bioenergy, food, animal feed and phar-
maceuticals. Wastewater treatment by algae also includes assimilation
of organic pollutants into cellular constituents such as lipids and car-
bohydrates. Furthermore, it is more environmentally friendly compared
to the conventional wastewater treatments with introduction of acti-
vated sludge, a biological floc. Biological treatments using microalgae
Reduced COD consumption to 0.57 kg by MFC for 1
kg N recovery compared to 2.86 kg COD for 1 kg N

and cyanobacteria can offer a solution for the limitations of the current
Expensive due to required chemicals, dewatering
compared to 500 Wh per m3 by activated sludge
process, reduced greenhouse gas (CO2) emission

chemicals and reconditioning of the ammonium

tertiary treatment methods. Secondary and tertiary treatments use more

Expensive due to the complex process, cost of
Reduced energy demand to 1.5-8 Wh per m3

than half of the energy cost devoted to the municipal wastewater

treatment. This cost is mostly related to the oxygen transfer into the
sulfate solution to a fertilizer product

secondary treatment and chemical demands in the tertiary treatment.

Chlorella sp. is frequently investigated for its nitrogen removal ca-
removal, no aeration demand

and drying of the precipitate

pacity in combination with other microalgae or bacteria (Table 5). Both

Nitrogen recovery efficiency, chemical input, economic evaluation, main technical parameters of different nitrogen recovery process.

native and non-native consortia can be used for wastewater treatment.

The nitrogen removal efficiencies shown in Table 5 represent the
Economic evaluation

combined effects of such consortia. Few reports exist on the individual

capacity of microalgal species for nitrogen recovery, namely it was
found that Dunaliella tertiolecta, Neochloris oleobundans, and Chlorella
vulgais could individually uptake 155, 150, and 103 mg L-1 d-1, re-
spectively (Li et al., 2008; Hulatt et al., 2012).
No demand for additional substances to
adjust pH for ammonia stripping at the

4.2.1. Microalgae growth

Required additional magnesium salts
Additional substances to adjust pH

Microalgae are cultivated through the suspended- and immobilized-cell

systems for wastewater treatment purposes (Table 5). Nutrients supply in-
cluding inorganic carbon as well as nitrogen (NO3−, NH4+, and urea) and
phosphorus are required for the photosynthesis and production of proteins
cathodic compartment

and nucleic acids during microalgal growth (Grobbelaar, 2004). Microalgal

No chemical input

biomass production but not nitrogen and phosphorus removal is critically

Chemical input

and phosphate

affected by nitrogen to phosphorus molar ratio (N/P) in wastewater. The

ratio lower than 5 and higher than 30 causes nitrogen and phosphorus
deficiency for microalgal growth, respectively (Choi and Lee, 2015). Dif-
ferent wastewaters, including the piggery industry and domestic waste-
waters, as well as dairy manure and municipal sewage anaerobically-di-
Energy recovery by biological oxidation

gested wastewaters with the appropriate N/P molar ratios (9, 11, 14 and 15,
phosphorous and COD removal from
of wastewater organic matter at the

Only NH4+recovered, no impact on

respectively) are suitable for microalgal growth (Gonçalves et al., 2017).

Nitrogen and phosphorus recovery

Interestingly, the nitrogen fixation capacity of cyanobacteria make them

NH4+and phosphorus recovery

able to survive at low concentration of nitrogen (Sood et al., 2015).

anodic compartment

4.2.2. Factors affecting nitrogen removal by microalgae and cyanobacteria

Recovery efficiency

For an optimal growth and nitrogen removal by microalgae, several

principle parameters should be carefully controlled. The solubility of
wastewater

CO2, required for microalgae photosynthesis, is negatively affected by

the medium pH and temperature. NH4+ volatilization also occurs at
increased pH and temperature, which adversely affects NH4+ removal
COD- chemical oxygen demand.

process by microalgae (Gonçalves et al., 2017). CO2 enrichment and

buffering can prevent the harmful effect of pH increase on growth and
Chemical stripping process

nitrogen removal (Taziki et al., 2015). The microalgae optimal growth

recovery by MFCs
Ammonia/ammonium
Operation technique

is influenced by temperature. Optimal temperature for microalgae

cyanobacteria

Chemical struvite
precipitation

growth differs among various species from below 10 °C to moderate

Microalgae and

temperatures (10–20 °C) and even some of them above 30 °C. Although,
increasing temperature usually increase metabolic activity when mi-
Table 4

croalgal growth is reduced at lower temperatures (Xin et al., 2011;

Robarts and Zohary, 1987).

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S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

Fig. 7. Biological nitrogen removal mechanism by microalgae (A). Phylogenetic tree of nitrate reductase (B) and nitrite reductase (C) proteins in microalgae in
comparison with other organisms. Microorganisms used for wastewater treatments are marked with red circle.

In terms of nitrogen recovery, a temperature-dependent specific 4.2.3. Mixed heterotrophic bacteria-microalgae culture
affinity is found for nitrate in microalgae (Q10 ≈ 3, Q10 is the pro- An interesting potential for nitrogen recovery is found in poly-
portional change with 10°C increase in temperature), with no clear cultures of microalgae or microalgae and bacteria. These polycultures
temperature-dependence for ammonium assimilation. Temperature- have a broad range of metabolic activities which allow them to adapt to
dependent nitrogen preference shows reduced affinity of microalgae for various conditions. These valuable consortia can grow in different en-
nitrate utilization at reduced temperatures whereas ammonium uptake vironments with various nutrient loads. The cooperative metabolic in-
and affinity is not affected suggesting ammonium as the more essential teractions of microorganisms in consortium can lead to nutrient re-
nutrient for microalgae (Reay et al., 1999). moval from wastewater (Renuka et al., 2013). In such a beneficial
The capacity of cyanobacteria for nutrient removal is also influ- consortium, the oxygen generated by microalgae photosynthesis is used
enced by environmental factors such as light, temperature, pH, etc by heterotrophic aerobic bacteria to biodegrade organic pollutants from
(Sood et al., 2015). However, a cyanobacteria Phormidium strain iso- wastewater. Heterotrophic bacteria discharge CO2, which can be used
lated from polar environment and Phormidium bohneri can efficiently by microalgae in the presence of light. Autotrophic, heterotrophic,
remove nutrients at temperatures below 10 °C and high temperatures mixotrophic, and photoheterotrophic are different metabolic types of
around 30 °C, respectively (Tang et al., 1997; Talbot and De la Noüe, microalgae, which can be shifted in response to changes in environ-
1993). These strains are sedimented for easy harvesting and they can be mental conditions (Delgadillo-Mirquez et al., 2016). Under certain
suggested as the suitable strains for wastewater treatment at low and conditions, they may also compete with heterotrophic bacteria. High
high temperatures, respectively. rate algal pond (HRAP) technology is used for mixed bacteria-micro-
Light, both in quality (wavelength) and quantity can affect the algae culture to treat municipal, industrial and agricultural waste-
microalgae growth and nitrogen removal efficiency. For example, red waters. HRAP is essentially a shallow race-track reactor (0.3-0.4 m
light is suggested as the optimum wavelength for C. vulgaris reproduc- depth), equipped with mechanical mixing for the simultaneous growth
tion and wastewater total nitrogen removal efficiency. Whereas the of algae and bacteria. HRAP is fed with the primary/secondary waste-
stimulation of nitrate uptake and activation of nitrate reductase require water, which is mixed with the algal and bacterial culture inside the
blue light (Azuara and Aparicio, 1984; Calero et al., 1980; Yan et al., bioreactor. In this system, the removal of pollutants is caused by algal
2013). Wastewater treatment at dark condition is the best in terms of assimilation, bacterial biological processes (nitrification/denitrifica-
economy and efficiency. Thus, wastewater treatment using combined tion) and stripping phenomena such as ammonia volatilization and
culture of Rhodobacter sphaeroides and Chlorella sorokiniana is suggested phosphorus precipitation (facilitated by high pH levels induced by
to efficiently remove nutrients under aerobic dark heterotrophic con- photosynthetic microalgal growth). Microalgal-bacterial consortia are
dition (Ogbonna et al., 2000). more beneficial than only microalgal consortia, as the microalgal-bac-
terial consortia can replace both secondary and tertiary treatment of

17
 Table 5
Application of microalgal and microalgal-bacterial consortia in nitrogen removal from different wastewaters and respective removal efficiencies.
Microorganisms Wastewater Operation technique Nitrogen removal References
S. Rahimi, et al.

rate %

Centrate wastewater native algal-bacterial consortium Centrates wastewater, primary-treated Immobilized system with higher nutrient removal rates 60 Posadas et al. (2013)
domestic wastewater 70
Centrate wastewater native algal-bacterial consortium Synthetic domestic wastewater Closed suspended system and mixotrophic metabolism 99.8 Alcántara et al. (2015b)
Chlorella sorokiniana and activated sludge native bacteria Potato-processing wastewater Open suspended system and biogas production ≥ 95 Hernández et al. (2013)
Chlorella sorokiniana and activated sludge native bacteria Primary-treated piggery wastewater Open suspended system and biogas production 82.7 Hernández et al. (2013)
Chlorella sorokiniana and activated sludge native bacteria Primary-treated piggery wastewater Immobilized system biofilm reactor with simultaneous 94–100 De Godos et al. (2009)
denitrification/nitrification
Chlorella sp., Pediastrum sp., Phormidium sp., Scenedesmus sp. and Primary-treated municipal wastewater Closed suspended system with microalgal bacterial flocs MaB-flocs 61.2 Van Den Hende et al.
activated sludge native bacteria (2011)
Chlorella spp. and Azospirillum brasilense Municipal wastewater Co-immobilized system using alginate beads 15 NO3-N De-Bashan et al. (2004)
100 NH4-N
Chlorella vulgaris and Azospirillum brasilense Synthetic wastewater Co-immobilized system using alginate beads 93 De-Bashan et al. (2002)
91
100
Chlorella vulgaris and Bacillus licheniformis Synthetic medium Closed suspended system with pH control 78 Liang et al. (2013)
Chlorella vulgaris and activated sludge native bacteria Synthetic wastewater Closed suspended system considering food to microorganisms ratio F/ 33.43–65.96 Medina and Neis (2007)
M and hydraulic retention time HRT
Chlorella vulgaris and primary-treated municipal wastewater native Primary-treated municipal wastewater Closed suspended system 30.9–100 He et al. (2013)
bacteria
Microalgal consortium from a high rate algal pond treating diluted Synthetic wastewater Anoxic–aerobic closed suspended system with nitrous oxide emission 75–96 Alcántara et al. (2015a)
vinasse and activated sludge native bacteria
Microalgal consortium from a high rate algal pond treating domestic Domestic wastewater Open suspended system with and without CO2 addition 91.8–96.9 Park and Craggs (2011)
wastewater and activated sludge native bacteria
Municipal wastewater native microalgae and activated sludge native Primary-treated municipal wastewater Open suspended system and effect of sludge inoculation ratios 93.7–95.8 Su et al. (2012b)

18
bacteria
Piggery wastewater native algal-bacterial consortium Fresh piggery wastewater Open suspended system 58.2–94.8 González-Fernández et al.
(2011)
Primary-treated wastewater native algal-bacterial consortium Primary-treated municipal wastewater Closed suspended system 100 Su et al. (2011)
Scenedesmus sp. and anaerobic sludge native bacteria Starch wastewater Closed suspended system 88.7 Ren et al. (2015)
Microalgal consortium composed by Ulothrix zonata, Ulothrix aequalis, Digested dairy manure wastewater Immobilized system biofilm reactor and dry matter/crude protein 62 Wilkie and Mulbry (2002)
Rhizoclonium hieroglyphicum and Oedogonium sp. yields
Chlamydomonas reinhardtii, Scenedesmus rubescens and Chlorella vulgaris Primary-treated municipal wastewater Closed suspended system considering biotic and abiotic factors 41.2–100 TN Su et al. (2012a)
Chlorella sp. and Scenedesmus sp. Primary-treated municipal wastewater Closed suspended system under the climatic conditions specific to 88.6–96.4 Koreiviene et al. (2014)
at different concentrations Lithuania
Chlorella sp., Scenedesmus spp. and Chlorella zofingiensis Dairy wastewater Closed suspended system for biodiesel production 87.0–91.0 Qin et al. (2016)
Chlorella vulgaris and Planktothrix isothrix Municipal wastewater Closed suspended system and co-culture effect 43.9–81.5 Silva-Benavides and
Torzillo (2012)
Microalgal consortium composed by the families Chlorophyta, Primary-treated municipal wastewater Closed suspended system 100 Samorì et al. (2013)
Cyanobacteria, Euglenozoa and Ochrophyta
Carpet mill industry wastewater native microalgal consortium Carpet mill industry wastewater Closed suspended system for biodiesel production 99.7–99.8 Chinnasamy et al. (2010)
Phormidium sp., Limnothrix sp., Anabaena sp., Westiellopsis sp., Primary-treated sewage water Closed suspended system with native filamentous microalgal strains, 83.3 Renuka et al. (2013)
Fischerella sp. and Spirogyra sp. native unicellular microalgal strains, selected microalgae from 100
germplasm
Rhodobacter sphaeroides and Chlorella sorokiniana Synthetic high strength organic Closed suspended system 100 Ogbonna et al. (2000)
wastewater 100
Synechocystis salina and Chlorella vulgaris Synthetic medium Closed suspended system with polyculture 84.5 Gonçalves et al. (2016)
Chlorella vulgaris Treated sewage Algal biofilm airlift photobioreactor ABA-PBR with solid carriers 61.6 Tao et al. (2017)
Betaproteobacteria, Gammaproteobacteria, Flavobacterium, Chlorophyta, Synthetic domestic wastewater Photobioreactor with algal–bacterial granules 59.8-70.5 TN Zhang et al. (2018)
Trebouxiophyceae, Bacillariophyceae, Cyanobacteria 99% NH4-N
Chlorella vulgaris-Bacillus licheniformis Synthetic wastewater Algae-bacteria symbiotic system 88.95 TN Ji et al. (2018)
Microcystis aeruginosa-Bacillus licheniformis 21.56 TN

TN - total nitrogen mg N L− 1.
Biotechnology Advances 43 (2020) 107570
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

wastewater whilst microalgal consortia can be only applied in tertiary 4.3.2. Struvite precipitation
treatment of wastewater (Gonçalves et al., 2017). HRAP with algae- Struvite precipitation is considered as the one of the preferred
dominated consortium shows high removal efficiency for COD, total chemical technologies in NH4+ and phosphorus removal from waste-
nitrogen and phosphorus from untreated municipal wastewater (Kim water, with significant potential for nitrogen recovery (Cao et al.,
et al., 2014). Furthermore, a hydrodynamic model of HRAP with a ratio 2019b; Huang et al., 2016; Song et al., 2018). It is a highly effective,
length/width (L/W) higher than 10 shows better performance with simple and environmentally friendly method, with nitrogen recoverable
respect to the velocity uniformity and reduced shear stresses as the fertilizer (Barbosa et al., 2016). Struvite is a valuable fertilizer in
(Hadiyanto et al., 2013). However, increasing depth significantly in- the form of white crystalline solid which is poorly soluble in water. It is
creases overall areal productivity (Sutherland et al., 2014). formed through the following simplified reaction; Mg2+ + NH4+ +
Despite their utility, the HRAP systems present some hurdles. In PO43− + 6H2O → MgNH4PO46H2O. This reaction can be mainly af-
these systems, there is lack of balance in oxygen consumption and fected by two factors including molar ratio of Mg:NH4:P and pH (op-
production by bacteria and algae, caused by difficulties in light pene- timum pH 9.0–10.0) (Cao et al., 2019b). Struvite precipitation with an
tration and mixing. However, closed photobioreactors (PBRs) and Mg:NH4:PO4 ratio of 1:1:1 could remove 95% of NH4+ from anaero-
closed tanks have been proposed to overcome the obstacles of light bically treated effluents in 30 s (Escudero et al., 2015). At higher pH,
penetration, mixing and presence of predators (He et al., 2013; the solubility of struvite reduces resulting in struvite crystals formation.
Alcántara et al., 2015a). The demand of an additional step to harvest Several studies investigated struvite formation and phosphorus and
microalgae biomass from treated effluent is another issue with HRAPs, ammonium recovery from urine, livestock manure, anaerobically-
which is addressed by immobilized growth system. There are several treated effluents, industrial wastewater and landfill leachate (Etter
immobilization techniques to decrease time and costs for harvesting et al., 2011; Huang et al., 2011; Song et al., 2011; Crutchik and Garrido,
microalgae as following; i) a centrate (the liquid removed from thick- 2011; Di Iaconi et al., 2010). One considerable difficulty with struvite
ened sludge) microalgal-bacterial consortium in biofilm reactor precipitation is the large amount of ammonium and phosphorus found
(Posadas et al., 2013; De Godos et al., 2009), ii) growth immobilization in anaerobically-treated effluents from livestock manures. These re-
in solid carriers such as beads (De-Bashan et al., 2004), iii) usage of quire large amounts of magnesium salts for effective struvite pre-
microorganisms with flocculation characteristics as artificial consortia cipitation. Unfortunately, due to high cost of the reagents and necessity
(Van Den Hende et al., 2011). To further improve the capacity of these of pH control, very few industrial-scale struvite crystallization plants
systems in nutrient removal, some studies investigated the complex are in operation (Escudero et al., 2015). However, magnesium oxide
interactions between physico-chemical factors such as light, photo- (MgO) is recently suggested as a proper Mg source for struvite crys-
period, temperature, nutrients concentration, pH, microalgal: bacterial tallization. It is cheap, existing in large quantities, and also it has high
ratio and biological factors (Gonçalves et al., 2017). Examples of re- alkalinity and adsorption capacity for removal of organic and polymeric
levant biological factors include pathogens, viral attack, protozoa pre- substance, such as polysaccharide, polyphenols, and organic acid (Cao
dation and competition with bacteria over the available nutrients et al., 2019b; Chimenos et al., 2003; Cai et al., 2017). Furthermore,
(Gonçalves et al., 2017). Large seasonal variations in photoperiod and combining ammonia stripping with struvite precipitation could feasibly
temperature affect wastewater treatment efficiency and biomass pro- remove ammonia nitrogen, phosphate, and COD from digested swine
ductivity in HRAP (Delgadillo-Mirquez et al., 2016). The photoperiod wastewater with high efficiency, low cost, and environmental friend-
duration has been shown to affect algal-bacterial population dynamics liness (Cao et al., 2019b). Furthermore, no pH adjustment is needed
in a photo-bioreactor for municipal wastewater treatment (Lee et al., using Na3PO4·12H2O as the PO43− source which is an effective reagent
2015). for ammonium removal and struvite precipitation due to reaching to
high pH in the medium.

4.3. Nitrogen recovery by chemical processes 5. Perspectives

4.3.1. Stripping process Partial nitritation and anammox for mainstream wastewater treat-
The stripping technology is a chemical ammonium removal process ment is an attractive concept because it would reduce energy require-
promoting conversion of NH4+ to NH3 by forcing air or other gas into ments for aeration and allow a larger fraction of organic matter to be
the wastewater to get NH3 into the gas phase. The ammonia stripping valorized as biogas. However, the concept is challenging because of the
process includes four major steps including: i) NH4+ conversion to low growth rate of anammox bacteria at low temperatures, full-scale
ammonia gas (NH3), ii) NH3 diffusion to the air-water interface, iii) NH3 operation is remaining a challenge under winter conditions. The long-
release to the air at the interface, and iv) NH3 diffuses from the air- term stability of the process has also been pointed out as an aspect
water interface into the air above. The process is affected by pH, tem- requiring further research. Stable nitrite production plays a key role for
perature and mass transfer area. In common applications, NH4+ in long-term operation of coupled partial nitritation and anammox.
wastewater can be released from the aqueous phase by air, steam or Therefore, effective strategies such as organic carbon and reaction time,
biogas (Limoli et al., 2016). etc should be further investigated to maintain nitrite production for
Both continuous and batch mode can be used for operation of different wastewater compositions and operational conditions.
strippers. To avoid NH3 emission into the air causing the greenhouse Another concern with anammox processes is the nitrate present in
effect, NH3 is typically absorbed by phosphorus acid (Shen et al., 2017). effluent. Both the anammox bacteria themselves and failure to suppress
Sulfuric acid is also used for the absorption of the stripped ammonia as NOB activity will lead to nitrate production, which means the effluent
ammonium sulphate. According to the initial ammonia concentration in may require further treatment. This challenge could be addressed by a
wastewater, it is introduced at stoichiometric concentration. The most SNAD process simultaneously accomplishing partial nitrification, ana-
common use for nitrogen recovered in this process is the conversion to mmox, and denitrification. However, these conditions present serious
fertilizer with 40%–60% ammonium sulfate solution and low organic difficulties for conventional nitrification and denitrification methods.
contamination. This can be produced directly from the ammonia To address the issue with toxic substances present in nitrate-en-
stripping process effluent after pH neutralization (Laureni et al., 2013). riched industrial wastewaters, it is required to perform a comprehen-
Thus, the ammonia stripping process can be suggested as a beneficial sive analysis of chemical composition and then adapt the treatment
technology to support agriculture in areas where this is required. process accordingly. Granules or biofilms based systems are promising
However, only NH4+ can be removed by this method, with no impact approaches when it comes to mitigating negative effects of toxic com-
on phosphorous and COD removal from wastewater (Cao et al., 2019b). ponents in nitrate-enriched industrial wastewater.

19
S. Rahimi, et al. Biotechnology Advances 43 (2020) 107570

In case of nitrogen recovery, bioelectrochemical systems can make a Acknowledgment

shortcut in ammonium removal from wastewater through the direct
recovery in the form of ammonia rather than reduction to nitrogen gas. This study was supported by a grant from the Carl Tryggers
Nitrogen recovery by bioelectrochemical systems is advantageous, as Foundation [CTS17:312] and ÅForsk grant [19-508].
there is no demand for additional substances to increase pH for am-
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