South Asian Journal of Research in Microbiology

Volume 18, Issue 10, Page 53-62, 2024; Article [Link].123572

ISSN: 2582-1989

Isolation and Characterization of

Terrestrial Cyanobacterium Producing
Commercially Important UV-B
Absorbing Compound
Mamadou Chetima Maina Boukar a,b*,
Moussa Diagara Saley c, Maman Moustapha Rabiou d,
Mai Moussa Chetima Bagana a and Kai Wang b
a Université de Diffa, Faculté des Sciences Agronomiques et Ecologiques, Département Biodiversité,
BP: 78 Diffa, Niger.
b School of Life Sciences, Hubei Key Laboratory of Genetic Regulation and Integrative Biology,

Central China Normal University, Wuhan, Hubei 430079, P. R. China.

c Université Abdou Moumouni de Niamey, Faculté des Sciences et Techniques,

BP : 10662 Niamey, Niger.

d Université Dan Dicko Dankoulodo de Maradi, Faculté des Sciences et Techniques, Département de

Biologie. Maradi, Niger.

Authors’ contributions

This work was carried out in collaboration among all authors. All authors read and approved the final
manuscript.

Article Information

DOI: [Link]

Open Peer Review History:

This journal follows the Advanced Open Peer Review policy. Identity of the Reviewers, Editor(s) and additional Reviewers,
peer review comments, different versions of the manuscript, comments of the editors, etc are available here:
[Link]

Received: 21/07/2024
Accepted: 23/09/2024
Original Research Article
Published: 03/10/2024

_____________________________________________________________________________________________________

*Corresponding author: Email: mainamenes@[Link];

Cite as: Boukar, Mamadou Chetima Maina, Moussa Diagara Saley, Maman Moustapha Rabiou, Mai Moussa Chetima Bagana,
and Kai Wang. 2024. “Isolation and Characterization of Terrestrial Cyanobacterium Producing Commercially Important UV-B
Absorbing Compound”. South Asian Journal of Research in Microbiology 18 (10):53-62.
[Link]
 Boukar et al.; S. Asian J. Res. Microbiol., vol. 18, no. 10, pp. 53-62, 2024; Article [Link].123572

ABSTRACT

Mycosporine-like amino acids (MAAs) constitute an important class of small water-soluble ultraviolet
radiation (UV)-absorbing compounds to counteract UV damages in algae and other organisms, and
have potential applications in sun care products as the active ingredients. In this study, one
filamentous cyanobacterium strain was isolated from the soil in southeast of Niger (Diffa), which
received strong UV radiation in summer. The 16S rDNA phylogenetic analysis classified the new
isolate as Leptolyngbyasp.CN1. MAA production was low in Leptolyngbya sp.CN1 under white light
condition but was significantly enhanced by prolonged UV-B treatments. Liquid chromatography
revealed one dominant type of MAAs in Leptolyngbya sp.CN1, and this kind of MAA was
characterized as shinorine based on special characteristics of in line absorption spectrum and mass
spectrum. The shinorine content was as high as 940 [Link]-1 dry weight after 4 days of UV-B
treatment. The present investigation indicates considerable shinorine is induced to protect
Leptolyngbya sp.CN1 from UV-B radiation, and also provide an avenue to explore the source of
various MAAs from the biotechnology perspective.

Keywords: Cyanobacteria; Leptolyngbya; mycosporine-like amino acids; shinorine; ultraviolet B.

1. INTRODUCTION photosynthesis. The obligate requirement of

sunlight for photosynthesis inevitably exposes
Mycosporine-like amino acids (MAAs) are low cyanobacteria to UV radiation. Since
molecular weight (ranging from 188 to 756), approximate 2.6-3.5 billion years ago before the
water-soluble, colorless secondary metabolites present ozone shield, cyanobacteria have
found in a wide variety of organisms, such as evolved sophisticated ways to synthesis diverse
fungi, cyanobacteria, algae, and corals [1,2,3,4]. MAAs to cope with UV radiation for their
More than 40 kinds of MAAs have been reported ubiquitous adaptation on the earth [14]. Studies
[5]. In general, they structurally compose a have showed that many taxonomically different
substituted cyclohexenone or an imino cyanobacteria from marine and terrestrial
cyclohexene ring [6,7,8]. The different substituent environments can produce and accumulate
of amino acids or its imino alcohol is conjugated MAAs [8,14]. The abundance and composition of
with a cyclohexenone or an imino cyclohexene MAAs varied among cyanobacterium species
ring to form diverse MAAs, and also determine and were also affected by the environmental
the differences of their absorbance spectra [5,9]. factors such as light fluctuations and nutrient
These special structures confer MAAs to limitations [2,5]. In this study, we try to isolate a
efficiently absorb UV radiation with the maximum cyanobacterium strain for novel MAA production
wavelength between 312 and 360 nm and high from terrestrial soil in southeast of Niger (Diffa),
molar absorptivity from 2.81×104 to 5.00×104 M- which received strong UV radiation and periodic
1·cm -1[8]. MAAs attenuate the harmful UV desiccation in most of the time during all the year.
radiation by converting it into heat to dissipate
the energy into environments without generate 2. MATERIALS AND METHODS
ROS [10,11]. Studies have also suggested other
functions of MAA, such as scavenging oxygen 2.1 Sample Collection and Isolation
radicals as antioxidant molecules, managing salt
stress as osmotic solutes, etc. [12]. In recent The soil was collected in southeastern Niger
years, MAAs have attracted considerable (Diffa), considered to have a desert climate
attention as the promising additives for where the average air temperature is 34 oC, with
application in pharmaceutical and cosmetic rainfall 141 mm in August. The soil was
industries [5]. Indeed, the formulation containing transferred to flasks and immersed in BG11
shinorine as an active ingredient has been liquid medium for cyanobacterial enrichment
developed in two market sunscreen products under 30 μmol photons m-2s-1 at 25°C. The
(Helioguard 365 and Helionori) [13]. Thus, it is upper solution turned slightly green after three
highly significant to explore the new source of weeks and some aliquots were then transferred
MAA from natural organisms. to new flasks with fresh BG11 liquid medium.
Cyanobacteria are the oldest photoautotrophic After growth for 20 days, the culture was serially
prokaryotes that can perform plant-like oxygenic diluted by the gradients of 10-1, 10-2, 10-3, 10-4and

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10-5 and spread on BG11 plates containing 1% 2.3 Induction and Detection of MAAs
agar. The single green clones were picked up
and cultivated in new flasks containing liquid After the culture growth for nearly three weeks
BG11 media for next classification. The under white light of 30 μmol photons m -2s-1at 25
morphology of cyanobacterium culture was 0C, the culture was divided into several open

observed using a laser scanning confocal petri dishes to induce MAA production under 0.1
microscopy (TCS SP5 Leica). W.m-2 UV-B treatments for 6, 24, and 48 hours.
The cyanobacterium cells were harvested by
2.2 Preparation of Partial gene DNA, 16S centrifugation at 6000 rpm for 5 min. The pellets
rDNA amplification and phylogenetic were mixed with methanol at 4oC overnight to
analysis extract MAAs. After the mixture was centrifuged
at 6000 rpm for 10 min, the MAAs in supernatant
Cells (1 mL) were harvested by Centrifugation at were detected by spectroscopic analysis
12000 rpm for 2 min. the supernatant was between 300-800 nm using a UV/Vis
removed and the cell pellet was rinsed twice by spectrophotometer.
pure water and resuspended in 100 μl water. The
cells were incubated at 100oC water bath for up 3 2.4 Characterization of MAAs
min. Thereafter cell debris were removed by
centrifugation at 12000 rpm for 2 min. The cyanobacterium cells were harvested for
MAA extraction by methanol as above. The
Rinsed cells pellet was resuspended in 250 μl methanolic extracts were dried in a vacuum
Tris-EDTA buffer (pH= 8.0) containing 20 mg/ml), concentrator (Labconco, UK) and water was
and incubated at 370C for 20 min. Proteinase K added to resolve the MAA samples. Equal
(20 mg/ml) and SDS were added to the cell volume of chloroform was used to remove
mixture to final concentrations of 50-100 μg/ml pigments in the MAA solution and MAAs were
and 2% (w/v) respectively. This mixture was characterized by liquid chromatography- mass
incubated at 60 oC for about 50 min. spectrometry (LC-MS) analysis on the machine
Subsequently, RNAse A (20mg/ml) was added to of Agilent technologies 6540 UHD Accurate-
a final concentration about 10 μg/ml and Mass Q-TOF. The samples of 50 μL solution
incubated at 65oC for 40 min. when samples were injected into a reversed-phase HPLC
cooled to room temperature Promega protein system coupled with in-line absorption spectral
precipitation solution was added and incubated scans and equipped with column inertsil ODS-SP
on ice for 5 min. Precipitated protein was (5 μm, 4.6 mm X 250 mm GL Sciences Inc
removed by centrifugation at 12000 rpm for 3 min, Japan). The MAAs were detected at 330 nm after
and the clear aqueous supernatant was mixed separation by 1 [Link]-1 of binary gradient
with equal volume of prechilled 100% elution of mobile A (methanol) and mobile B
isopropanol (HPLC grade). This mixture was kept (water) (0-7min, 1%-20% mobile A; 7-9 min,
at 4oC. The precipitated DNA pellets were 20%-50% mobile A; 9-17min, 50%-80% mobile A;
washed in cold 70% (v/v) ethanol twice and air 17-22 min, 80% mobile A). The electrospray
dried at room temperature for 5-10 min until the interface (ESI) source and positive mode was
pellets became transparent. Isolated DNA were used for mass spectrometer. MAAs could be
resuspended in water and kept at 20oC. The characterized from the features of in-line spectra
partial gene of 16S rRNA was amplified by PCR and mass spectra. The concentration
using the genomic DNA and the primers of of MAAs was determined by the value of
16S_27F, 5’-AGAGTTTGATCCTGGCTCAG-3’ absorption spectra maximum at 334 nm, the
and 16S_1494R, 5’- extinction coefficient (M-1Cm-1 ) and Molecular
TACGGCTACCTTGTTACGAC-3’. The PCR Weight.
condition was set as the initial denaturation at
95oC for 5 min, 35 cycles of denaturation for 1 3. RESULTS
min, annealing at 55oC for 1 min, extension at
72oC for 2 min, and final extension at 72oC for 10 3.1 Classification of the Isolated
min. The PCR products were extracted after gel Cyanobacterium
electrophoresis and sequenced. The sequence
was subjected to BLAST analysis and further one filamentous cyanobacterium strain was
used to construct phylogenetic tree by using finally isolated. The filaments show straight or
MEGA (version 6.0) software for cyanobacterium slightly waved or arcuate without branches and
classification.

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sheaths. The cells in the filaments are cylindrical Leptolyngbya sp.CN1. In consistence with the
and blunt at both ends with the size of 2.3-7.6 classification, Leptolyngbya sp.CN1 showed 98%
μm in length and 2.7-4.4 μm in width (Fig.1). The and 97% identity of their 16s rDNA sequence
constrictions were observed at the crosswalls with Leptolyngbya sp. JSC-1 and Leptolyngbya
between adjacent cells. Based on the 16S rDNA antartica [Link].1, respectively. However, the
phylogenetic tree, the isolated strain was similarities of the 16S rDNA sequences between
classified into the clade of Leptolyngbya genus Leptolyngbya sp.CN1 strain and the other related
(Fig.2). Thus, this strain can be named as strains are less than 95% (Table 1).

100 Anabaena_variabilis_ATCC_29413_
69 Nostoc_sp._PCC_7120
99 Nostoc_punctiforme_PCC_73102_
Nodularia_sp._BCNOD9427
59
100 Nodularia_sp._PCC_9350_
Chroococcidiopsis sp. A789-2
96
99 Chroococcidiopsis sp. CCMEE 29
Chroococcidiopsis sp. PCC 8201
71 100 Chroococcidiopsis_thermalis_PCC_7203_

94 Chroococcidiopsis sp. CCMP2733

Chroococcidiopsis sp. PCC 6712

99 Cyanothece_sp._PCC_8802_
Microcystis_aeruginosa_strain_PCC_7806_
52
45
88 Cyanothece_sp._PCC_7424_
100 Cyanothece_sp._PCC_7822_

92 Leptolyngbya sp. 1T12c

100 Leptolyngbya_sp.JSC-1_
Leptolyngbya sp. Nb3F1

57 Leptolyngbya sp. CN1

100 Leptolyngbya_antarctica_ANT.LAC.1_
97
Leptolyngbya_PCC7104_
86 Leptolyngbya_sp._HBC1_
95 Leptolyngbya_PCC7375_
Cyanothece_sp._PCC_7425_
Pseudanabaena_sp._PCC_7367_
Pseudanabaena_PCC7403
93
95 Pseudanabaena_PCC6903
100 Pseudanabaena_PCC7408

Fig. 1. Maximum-likelihood phylogeny of cyanobacteria based on 16S rDNA gene sequences

Fig. 2. Cell morphology of Leptolyngbya sp. CN1 under white field of confocal microscopy, the
scale bar presents 20 μm

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Table 1. The 16S rDNA comparisons between Leptolyngbya sp. CN1 and other cyanobacteria

Sequence Identity Matrix 1 2 3 4 5 6 7 8 9 10

1 Leptolyngbya _sp._CN1 ID
2 Leptolyngbya _sp._JSC-1 0.98 ID
3 Leptolyngbya _antartica_ANT.LAC.1 0.97 0.97 ID
4 Leptolyngbya _sp._PCC7104 0.94 0.93 0.92 ID
5 Leptolyngbya_laminosa_ETS-08 0.93 0.92 0.93 0.91 ID
6 Leptolyngbya_frigida_ANT.L53B.2 0.93 0.92 0.93 0.91 0.93 ID
7 Leptolyngbya_sp._Doroninskoye 0.94 0.93 0.93 0.92 0.92 0.92 ID
8 Leptolyngbya_sp._LEGE_06070 0.94 0.93 0.93 0.92 0.92 0.92 1.00 ID
9 Leptolyngbya_valderiana_SABC022801 0.94 0.93 0.93 0.92 0.92 0.92 1.00 1.00 ID
10 Leptolyngbya_ sp_HBC1 0.93 0.92 0.92 0.92 0.90 0.92 0.92 0.92 0.92 ID

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3.2 Induction of MAAs in Leptolyngbya characterized by the technology of LC-MS. The

sp.CN1 HPLC profile at detecting wavelength of 330 nm
showed an obvious peak at 2.6 min, possibly
Chlorophyll a (Chl a) contributed to absorbance suggesting one type of MAA production by UV-B
peak at 665 nm and carotenoids gave rise to the induction (Fig. 4A). The mass spectrum of the
absorbance in the range of 400 nm to 600 nm. compound corresponding to this peak showed a
The strong absorbance from 300 nm to 400 nm prominent ion peak of protonated fragment [M+H]
indicated MAA production by UV-B treatments at m/z 333.1269 suggesting the molecular weight
(Fig.3). The quite low peak at 334 nm suggested of 332 (Fig.4B). Besides, this compound also
MAA was produced in Leptolyngbya sp.CN1. demonstrated in-line absorbance spectrum
MAA production was positively related to centered at 334 nm (Fig.4C). The results of
prolonged UV-B treatments, suggesting molecular weight and profile of absorbance
protective roles of MAAs in Leptolyngbya spectrum were consistent with the characteristics
sp.CN1from UV-B radiation (Fig.3). of previously recognized MAA shinorine. These
results also indicated shinorine was the dominant
3.3 Identification of MAAs in type or likely the only one type of MAAs in
Leptolyngbya sp. CN1 Leptolyngbya sp.CN1.

MAAs are well-known for their strong absorbance The shinorine content reached up to 940 µ[Link]⁻¹
in UV regions. In consistence, the extracted MAA dry weight after 4 days of UV-B treatment. There
solution from UV-B treated Leptolyngbya sp.CN1 were no significant changes in shinorine
showed maximal absorbance at 334 nm. The production in Leptolyngbya sp. CN1at the
extracted MAAs were then separated and subsequent time points (Fig. 5).

0h
6h
24h
16 48h

12
Absorbance

300 400 500 600 700 800

Wavelength (nm)

Fig. 3. Absorption spectra of methanol extract from Leptolyngbya sp. CN1 treated by 0.1 W.m-2
UV-B for different hours

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Fig. 4. Characterization of MAA in Leptolyngbya sp. CN1, HPLC profile (A), LC-MS analysis (B)
and in line absorption spectrum (C) for methanol extract of Leptolyngbya sp. CN1 with 0.1
W.m-2 UV-B treatments for 7 days

1600

c c c

1200
MAAs (ug/mg)

b
800
b
b

400

a
0
0H 6H 12H 24H 48H 72H 96H
Time

Fig. 5. Concentration of MAAs in Leptolyngbya sp. CN1 exposed to 15 μmol photons m-2 s-1
photosynthetically active radiation and 0.1 W m-2 UV-B radiation for up to 96 H. Different letters
on the error bars indicate significant differences (Tukey’s HSD, p ≤ 0.05). Data are presented as
the mean ± standard deviation (n = 3). [15]

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4. DISCUSSION the precursor for various MAA production [29]. In

the pentose pathway Desmethyl-4-Deoxygadusol
MAAs are well-known as UV-protective Synthase DDGS and O-Methyltransferase O-MT
compounds and play an essential role in catalyze Sedoheptulose-7-Phosphate SH7P to
photoprotection of cells under UV radiation form 4-DG, which was used as the substrate with
conditions.[16]. Their strong UV absorption and glycine to produce mycosporine-glycine [28].
high molar coextinction efficiency suggested a Shinorine was then yielded through condensing
promising application in cosmetic industries to serine with mycosporine-glycine by non-
reduce the harmful effects of UV radiation on ribosomal peptide synthase (NRPS) or D-ala D-
human skin cells. Cyanobacteria are considered ala ligase [3, 28, 30, 31].
a rich source for the production of novel MAAs
because of their unexpected diversity and 5. CONCLUSION
ubiquitous distribution on the earth [14, 17].
Although more than 40 kinds of MAAs have been Leptolyngbya sp.CN1 was identified as a
reported, scientists have explored novel MAAs in organism that produces a considerable
various cyanobacteria from different abundance of shinorine to protect against UV-B
environments [3,18,19,20,21]. radiation. Present study shown that Leptolyngbya
sp.CN1 may be useful as a producer of UV
In the present study, we isolated a filamentous absorbing compound MAA. It will be the next
cyanobacterium strain, Leptolyngbya sp. CN1, exciting research to elucidate the genetic bases
from soil in the southeast of Niger and and biosynthetic pathway for shinorine in
characterized the production of the mycosporine- Leptolyngbya sp.CN1 in the future.
like amino acid (MAA) shinorine in Leptolyngbya
DISCLAIMER (ARTIFICIAL INTELLIGENCE)
sp. CN1. Leptolyngbya sp. CN1 taxonomically
belongs to the order Oscillatoriales. To our Author(s) hereby declare that NO generative AI
knowledge, only a few cyanobacterial strains in technologies such as Large Language Models
the Oscillatoriales order have been reported to (ChatGPT, COPILOT, etc) and text-to-image
produce MAAs, including Arthrospira sp. generators have been used during writing or
CU2556[22, 23], Lyngbya sp. CU2555 [24], editing of manuscripts.
Microcoleus chthonoplastes [25], Oscillatoria
spongelidae [26], Trichodesmium spp. [27]. MAA COMPETING INTERESTS
production varied widely among genus, species,
and even strains. Some Microcoleus isolates Authors have declared that no competing
produced one type MAA shinorine while interests exist.
Microcoleus chthonoplastes and Microcoleus
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