Rhizopoda Advanced article

O Roger Anderson, Columbia University, Palisades, New York, USA Article Contents
. Introduction
. Overall Taxonomic Scheme

. Major Taxonomic Groups

. Reproduction

. Phylogenetic Evolutionary Considerations

. Foraminifera

Online posting date: 15th June 2011

Rhizopoda are a broad group of protozoan amoeboid groups, although it is increasingly recognised that pseu-
organisms placed in the kingdom Protista. They include dopodial morphology is probably not a conservative fea-
the naked and testate amoebae, some members of the ture and may have arisen in different evolutionary lineages
slime moulds and foraminifera. The latter are almost by convergent adaptation. For example, molecular genetic
evidence indicates that the radiolaria may be more closely
exclusively marine organisms, either benthic or plank-
related to some Rhizopoda than previously thought, and
tonic. Locomotion is by extension of pseudopodia of var-
they are placed together with some of the members of
ied morphology that are specific to the taxonomic group. Rhizopoda in the newer higher order group ‘Rhizaria’ (e.g.
Pseudopodial morphology includes broad and fan-shaped Adl et al., 2005). Among some groups, such as the testate
anterior extensions, finger-like tubular extensions, or a amoebae and foraminifera (also included in the Rhizaria),
web-like network, the latter are called rhizopods. The the cell is enclosed by a species-specific shell or test that
shape of the pseudopodia, and the morphology of the is secreted by the organism. The shape of the test, and
enclosing shell or test, when present, are major defining its chemical composition, are important taxonomic
taxonomic characteristics. The Rhizopoda are important characteristics used in many established classification
aquatic and terrestrial protozoa at the base of food webs systems. See also: Amoeba; Foraminifera; Heliozoa; Pro-
and thus provide a major link in the transfer of energy to tist Systematics; Protozoan Organelles of Locomotion;
Radiolaria
higher order consumers. Some are capable of preying on
Members of the Rhizopoda are widely distributed
fungi (e.g. large mycophagous amoebae) or other protists
globally in terrestrial and aquatic habitats. There is
and in some cases small invertebrates (e.g. foraminifera). increasing evidence that many species of this group serve an
important role in ecosystem dynamics, especially as
important food sources at the base of food webs. During
feeding on smaller protists and bacteria, they also release
Introduction particulate bound nutrients making them available to other
organisms. This occurs partially during engulfment and
The Rhizopoda are an eclectic group of amoeboid organ- degradation of the food, and subsequently in expelled
isms that move by cytoplasmic extensions from the cell waste matter. For example, terrestrial amoebae are
surface known as pseudopodia. Pseudopodia vary in size increasingly recognised as numerically important micro-
and shape (Anderson, 1988a; Sleigh, 1989). Slender elongate biota inhabiting the rhizosphere (zone immediately adja-
forms are known as filopodia, whereas those that are more cent to the roots) where they can increase soil fertility by
blunt and lobose (finger-shaped) are lobopodia as observed remineralisation of major inorganic nutrients required by
in the familiar Amoeba proteus. In some species, the plants. The foraminifera, characterised by calcareous,
pseudopodia form an interconnected, web-like network porous shells, are significant members of marine eco-
known as rhizopodia (e.g. planktonic foraminifera, Figure 6). systems. The benthic species found in the sediments or
However, none of these have stiffened internal arrays of attached to surfaces of plants in salt marshes are abundant
microtubules as are found in the ray-like axopodia char- members of coastal communities. Their shells accumulate
acteristic of the heliozoa and radiolaria. The form of the in the sediments and over time form a fossil record that can
pseudopodia has been used in defining various taxonomic be used to interpret the climatic and ecological conditions
in that region. Planktonic foraminifera with spiral calcitic
eLS subject area: Microbiology shells occur widely in the open ocean. Their shells also
accumulate in the marine sediments and are used exten-
How to cite: sively by micropalaeontologists to reconstruct palaeocli-
Anderson, O Roger (June 2011) Rhizopoda. In: eLS. John Wiley & Sons, mates and the palaeoecology of oceans. The succession of
Ltd: Chichester.
different shells of species with increasing depth in the
DOI: 10.1002/9780470015902.a0001986.pub2
sediments forms an excellent microfossil record that can be

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 Rhizopoda

used in conjunction with other evidence to deduce the The third major subphylum, Sarcodina, are the ‘amoeboid
evolutionary pathways of the foraminifera. See also: organisms’ including the major group Rhizopoda.
Marine Communities; Palaeoclimatology; Palaeoecology; Based on modern evidence, including electron micro-
Protozoan Diversity and Biogeography; Rhizosphere; scopic fine structural features and molecular genetic data,
Soils and Decompositiont recent changes have been recommended for the higher
order classification categories (e.g. Adl et al., 2005). Other
sources offer perspectives on interim categorisation
Overall Taxonomic Scheme schemes that help us put the emerging evidence into at least
a reasonable approximation to a more natural system (e.g.
A variety of classification schemes exist for the Rhizopoda, Cavalier-Smith, 1998; Lee et al., 2000; Smirnov et al.,
and increasing evidence from molecular genetic analyses 2005). Taxonomy, as with other fields of scientific inquiry,
has led to some major revisions in our thinking about is a dynamic and evolving science. We are currently in an
how to classify the Rhizopoda. In the system of Levine exciting time of gathering new and substantial evidence on
et al. (1980), they included the Rhizopoda in a Superclass the natural affinities of protists based on molecular evi-
(Rhizopodea) within a subphylum Sarcodina that in- dence combined with established techniques of light and
cluded all pseudopod-bearing protozoa. This system in electron microscopy. Therefore, current taxonomic
general is also used by the Zoological Record (ZR), a schemes can only be considered as works in progress, but
standard taxonomic reference source. The ZR hierarchical they promise to bring much clearer resolution to solving the
taxonomic scheme is as follows: See also: Protozoan natural phylogenetic relationships among living organ-
Taxonomy and Systematics isms. A perspective, published by the International Society

Sarcomastigophora (phylum): amoeboid and flagellated protozoa.

Sarcodina (subphylum): amoeboid protozoa.
Rhizopoda (superclass): pseudopod-bearing protozoa.
Lobosea (class): lobate-pseudopod-bearing protozoa.
Gymnamoebia (subclass): naked amoebae, lacking a test.
Amoebida (order): typically uninucleate and possessing mitochondria.
Pelobiontida (order): one or two nuclei, living in anaerobic environments.
Schizopyrenida (order): heterolobsean amoebae with eruptive locomotion.
Testacealobosia (subclass): amoebae enclosed in a test.
Arcellinida (order): with lobose pseudopodia.
Himatismenida (order): with external scale-covered flexible test.
Trichosida (order): with external, flexible, spicule-containing test.
Acarpomyxea (class): much-branched forms, plasmodial or uninucleate.
Acrasea (class): slime moulds with limax-shaped amoeboid stages.
Eumycetozoea (class): true slime moulds with plasmodial stages.
Protosteliia (subclass): with long-stalked, single spore-containing sporecase.
Dictyosteliia (subclass): amoebae fuse into a motile slug that makes sporocarps.
Myxogastria (subclass): plasmodial, producing stalked fruiting bodies with spores.
Plasmodiophorea (class): minute plasmodial intracellular parasites.
Filosea (class): amoeboid protists with slender, long-tapered filopodia.
Aconchulinida (order): siliceous, scale-bearing testate amoebae.
Gromiida (order): with chitinous test varying from ovoidal to spherical.
Granuloreticulosea (class): amoeboid protists with granular, reticulate rhizopods.
Athalamida (order): lacking a test.
Foraminiferida (order): with calcareous, typically multichambered, porous test.
Monothalamida (order): single enclosing chamber or test and oral aperture.
Xenophyophorea (class): very large plasmodial-like, multinucleated marine protists.

The Sarcomastigophora includes the subphylum Mas- of Protistologists (Adl et al., 2005), illustrates current
tigophora, encompassing the photosynthetic and non- thought on the higher level relationships of some Rhizo-
photosynthetic flagellates, and the subphylum Opalinata, a poda and their relatives. Two major groups are included
group of flagellated protists commonly found in the intes- here: Amoebozoa (Shadwick et al., 2009) and Rhizaria (e.g.
tines of aquatic vertebrates such as fishes and amphibians. Nikolaev et al., 2004; Pawlowski and Burki, 2009).

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AMOEBOZOA
Tubulinea Smirnov et al., 2005
Naked or testate amoeboid organisms, tubular, sub-
cylindrical pseudopodia, or transforming from flat-
tened and expanded to subcylindrical; monoaxial flow
of cytoplasm in entire cell or within each pseudo-
podium; without centrosomes.
Flabellinea Smirnov et al., 2005
Flattened locomotive amoebae, without tubular sub-
cylindrical pseudopodia; motile form is constant, not
altered; polyaxial cytoplasmic flow, or without pro-
nounced axis; without centrosomes.
Acanthamoebidae Sawyer and Griffin, 1975
Subpseudopodia prominent, flexible, and tapering to a
fine or blunt tip; uninucleate; nonadhesive posterior
uroid; glycocalyx extremely thin; cysts of most species
double-walled, with operculate pores; centriole-like
body present.
Entamoebida Cavalier-Smith, 1993
Pseudopodia clear, eruptive arising from hyaline ecto-
plasm and a granular or clear endoplasm; mitosis closed
with endonuclear centrosome and spindle; mito-
chondria, peroxisomes and hydrogenosomes absent;
reduced Golgi dictyosome.
Figure 1 A lobose gymnamoeba (Chaos carolinense). With permission
RHIZARIA from Lee et al. (1985).
Silicofilosea Adl et al., 2005 [Imbricatea Cavalier-Smith
and Chao, 2003]
Testate amoebae with filose pseudopodia; internally
secreted siliceous surface scales; mitochondria with
tubular cristae.
Foraminifera d’Orbigny, 1826
Calcareous, porous-shelled protists with granular,
reticulated pseudopodia.
Radiolaria Müller, 1858, emend. Adl et al., 2005
Siliceous skeletal protists with stiffened axopodia.

Major Taxonomic Groups

Lobose amoebae
This includes the so-called naked amoebae (Figure 1) Figure 2 A lobose testate amoeba (Phryganella nidulus) showing the
(gymnamoebae) without a shell, but often with a thin granular test enclosing the cell and emerging finger-shaped pseudopodia.
With permission from Lee et al. (1985).
organic surface coat or layer of scales, and the testate
amoebae with lobose pseudopodia (Figure 2), enclosed
within an organic or mineralised shell (Page, 1988). The limax amoebae with a tubular or worm-like shape. The
naked amoebae are characterised by the familiar A. proteus form of locomotion and rate of movement are often of
often used in the classroom to exemplify the amoebae taxonomic importance. Some of the limax amoebae move
broadly. However, A. proteus is not so commonly by a rather steady forward creeping motion including the
encountered in samples from the natural environment. In genus Hartmannella and Saccamoeba. The amoebae with
general, the naked amoebae inhabit the surfaces of par- eruptive locomotion (e.g. Naegleria and Vahlkampfia) are
ticles in soils and sediments or of suspended flocculent characterised by genera that produce flagellated stages in
matter in the water column. They all move by pseudopodial their life cycle. They are classified in the Heterolobosea and
formation. Some have rather blunt pseudopodia (e.g. current evidence indicates that they are not amoebae, but
Amoeba and Mayorella), whereas others have long, tapered flagellates with an amoeboid life stage. Therefore, they
pseudopodia as in Vexillifera. Other major groups are have been moved into their own taxonomic group separate
either discoid or fan-shaped (e.g. Vannella) and some are from the Rhizopoda. However, mention will be made of

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them when it contributes to clarifying some taxonomic or

evolutionary relationships.
Naked amoebae are typically abundant protists in
aquatic and terrestrial environments where they are sig-
nificant members of the microbial community, preying on
bacteria, small algae, or other microbes. Hence, they are
important links in the food web transferring energy and
matter to higher level consumers. They also contribute to
the fertility of soils by releasing nutrients during predation
on prey organisms. They are one of the important members
of the so-called microbial loop, whereby prey-contained
nutrients, including mineral and organic nutrients, are
released during predation and assimilated by primary
producers. The nutrients support photosynthesis and
growth of primary producers, thus increasing the available
sources of organic nutrients to sustain microbial food
webs, and completing the loop. At least one amoeba
(Mayorella viridis) is a host for symbiotic green algae. With
proper illumination, the amoeba can be maintained in
culture with only a mineral medium (Page, 1988, p. 79). The
photosynthetic symbionts provide sufficient nutrition to
sustain growth and reproduction of the amoeba. See also:
Amoeba
The testate amoebae with lobose pseudopodia are
included in the Testacealobosia (Ogden and Hedley, 1980).
All possess some form of external test or shell whose shape Figure 3 Euglyphid testate amoeba (Euglypha ciliata) with filose
and chemical composition are important taxonomic char- pseudopodia emerging from a spinose test composed of imbricated
acteristics. In some species such as Arcella, the test is siliceous scales. With permission from Lee et al. (1985).

composed of numerous organic subunits secreted by the

amoeba and organised into a somewhat flattened discoid surrounded by specialised, toothed scales. Other genera
shell. The ventral aperture is rounded. In other genera, the dwelling in beach sands, such as Microamphora, Amphor-
organic test is augmented by mineral matter, either secreted ellopsis, Chardezia and Psammonobioticus, have elaborate
from the cytoplasm of the organism or gathered as mineral tests whose terminal apertures bear outwardly flared rims.
particles from the environment and organised in species- This may help secure them in the sand.
specific patterns on the surface of the test. For example,
some species of Difflugia, with globose to elongated shells,
selectively gather mineral particles from the environment Acarpomyxea, Acrasea, Eumycetozoea and
by collecting them with their pseudopodia. The gathered Plasmodiophorea (‘slime moulds’ and
particles are brought to the test by pseudopodial streaming related genera)
and cemented into place on the surface. Netzelia, however,
secretes siliceous particles within vacuoles in the cyto- The Acarpomyxea are a heterogeneous group of much-
plasm, expels them on the cell surface, and cements them branched plasmodial forms that are multinucleate, or
together to form a protective test (e.g. Anderson, 1988b). A uninucleate, and dwell in freshwater, marine or terrestrial
terminal, rounded to stellate aperture permits extension of habitats (Margulis et al., 1990). A prominent example is
pseudopodia for locomotion and feeding. Other genera, Stereomyxa ramosa (Figure 4), a uninucleate, cruciform cell
such as Quadrulella, secrete small quadrangular, siliceous with much-branched peripheral pseudopodia arising from
plates that form the vase-shaped test. Lesquereusia secretes the cell body that is covered with debris collected from the
vermiform or sigmoidal rodlets of silica that are arranged environment. Their position is uncertain, but they are
decoratively on the surface of the organic test. sometimes grouped near the Acrasea and Eumycetozoea,
two classes that encompass the so-called slime moulds
Filose amoebae included in the Amoebozoa of some modern classifications
(e.g. Shadwick et al., 2009). The Acrasea are cellular slime
Testate amoebae with thin, filose pseudopodia (Figure 3) are moulds (feeding stage is a limax-shaped amoeba known as
placed in the class Filosea (Ogden and Hedley, 1980). myxamoebae). They are probably a polyphyletic group
Euglypha, for example, has a vase-shaped test covered with characterised by amoeboid stages that aggregate to form
imbricated (shingle-like) thin, oval, siliceous often spiny spore-containing sporocarps. Sporocarps are multicellular
plates secreted by the organism. The hyaline, finely tapered aerial stalked structures also known as fruiting bodies.
pseudopodia emerge from a terminal ovate aperture Taxonomic characteristics of the Acrasea include pattern

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germination produces a biflagellated zoospore that dis-

perses and infects the host tissue, completing the life cycle.
See also: Slime Moulds

Granuloreticulate Rhizopods (foraminifera

and related organisms)
These are organisms with anastomosing or net-like
pseudopodia (Figure 5) with small intracellular granules
moving along the pseudopodia, hence the class name
‘Granuloreticulosea’ (Lee et al., 1985; Lee and Anderson,
1991). There are three main groups: (1) Athalamida,
without a test, (2) Foraminiferida, enclosed within single to
multichambered tests, often composed of calcium car-
bonate and (3) Monothalamida, with single-chambered,
organic or calcareous tests, commonly with attached deb-
ris, and lacking alternation of generations. The Athala-
mida include Arachnula, with branched, not anastomosed,
pseudopodia, and Biomyxa and Gymnophrys, with bran-
ched, anastomosing pseudopodia. The foraminifera are a
large and elegant group of marine Rhizopoda. Some form
organic tests either unadorned or coated with mineral
grains gathered from the environment. Others have elab-
orate multichambered, uniserial or biserial conical shells
formed of calcite. Others have flattened or conical spiral
Figure 4 Stereomyxa ramosa, a species in the class Acarpomyxea showing shells of varied design. Members of the suborder Miliolina
the branching plasmodium and bifurcated terminal pseudopodia. With have tests resembling fired porcelain, including the genera
permission from Lee et al. (1985).
Spiroloculina and Quinqueloculina. Others in the suborder
Rotalina have glassy shells including the genera Ammonia,
Elphidium and Heterostegina. The benthic species are
of sporogenesis, type of sporocarp, presence or absence of typically nonspinose, whereas some planktonic (floating)
mastigote (flagellated) cells, and the type of mitochondrial species bear long spines anchored in the surface of the shells
cristae. The cristae are the internal membranes (whether (Hemleben et al., 1989). The spines of planktonic species
tubular or plate-like) of the mitochondrion. Acrasis rosea (e.g. Figure 6) support external cytoplasm and provide
exemplifies the Acrasids. It is characterised by a pink to anchorage when capturing large prey such as copepods,
orange tint of the cytoplasm of amoeboid stages and the crustacean larvae, and other invertebrate prey. Spinose
delicate pink, branched, arborescent sporocarps produced species include Globigerina, Orbulina, with a porous
by the aggregated amoebae at maturation. The Eumyce- spherical final chamber at maturity, and Hastigerina, one
tozoea, also known as the ‘true slime moulds’, encompass
spore-forming slime moulds that have uninucleate to
multinucleate amoeboid stages that sporulate either by: (1)
differentiation of single amoeboid cells into simple stalked
sporocarps (Protosteliia), (2) aggregation of individual
amoebae to form multicellular pseudoplasmodia that
produce stalked multispored sporocarps (Dictyosteliia), or
(3) development of many spored sporangia from a multi-
nucleate, often sexually derived, diploid plasmodium usu-
ally of relatively large, sometimes several centimetres, size
(Myxogastria). The slime moulds are commonly found in
moist terrestrial environments where the grazing amoebae
consume bacteria, yeasts, spores of moulds and other small
microbiota. The beautiful, golden-yellow, large plas-
modium of Physarum polycephalum is often used in the
classroom to illustrate the morphology and life habits of
the Myxogastria. The Plasmodiophorea are all obligate,
Figure 5 A general diagram of a benthic foraminifer showing the
spore-forming, parasites living within the cells of plants, multichambered spiral shell with a small initial chamber (proloculus) at the
typically seed plants. Small plasmodia form within the host centre and peripheral halo of granular rhizopodia. With permission from
cells and give rise to resting spores. Each spore upon Lee et al. (1985).

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 Rhizopoda

Figure 6 A living planktonic foraminifer showing the translucent calcitic shell and radiating spines covered by, and supporting, a network of rhizopodia
bearing yellow-green algal symbionts.

of the largest planktonic foraminifera with diameters in the calcareous shell. The shells sink to the ocean floor and
millimetre range. Nonspinose planktonic foraminifera are become buried, some converted to calcareous rocks by
widely distributed with some species preferring warmer geological processes, and thus help to sequester the
and others colder water masses. They include the genera atmospheric CO2 and reduce the concentrations of this
Globoquadrina, Globorotalia and Pulleniatina. Some ben- greenhouse gas. However, the large amounts of anthro-
thic and planktonic foraminifera contain algal symbionts, pogenic CO2 being released into the atmosphere form
which supply photosynthetically derived organic nutrients carbonic acid when absorbed by the seawater and threaten
to the host. Among the benthic species, alternating gener- to lower the pH of the ocean seawater to such an extent that
ations consist of a gamont phase that produces gametes the planktonic foraminiferans are unable to secrete their
and an agamont phase that reproduces asexually. There are calcareous shells. See also: Foraminifera
many variations on the following plan, which is offered as a
general example. The multiple gametes released from a Class Xenophyophorea
gamont fuse in pairs to form a zygote that gives rise to an
agamont phase. After repeated asexual division, the aga- The Xenophyophorea are large (multimillimetre to centi-
monts eventually undergo multiple fission of the cytoplasm metre size) sediment-dwelling Rhizopoda found in the deep
to produce numerous individuals of the gamont phase, thus sea (Lee et al., 1985). They are cosmopolitan in distri-
completing the life cycle. Foraminifera are abundant and bution. Xenophyophores are plasmodial and enclosed by a
widely distributed. For example, the pink sand along the branching tube system made of a transparent, cement-like
coasts of Bermuda is composed of the pigmented shells of organic material. The tests of xenophyophores consist of
dead foraminifera. The massive carbonate rocks used by aggregates of foreign matter including foram shells,
the Egyptians to build the pyramids contain fossil remains radiolarian skeletons, sponge spicules and mineral grains
of exceptionally large calcareous foraminifera. Sediments cemented together within an organic matrix. The test of
from productive salt marshes worldwide are likely to con- most species is lumpy in appearance and ranges in size from
tain the elegant shells of benthic foraminifera. Open ocean a few millimetres to several centimetres. They are often
planktonic foraminifera are a major sink (second to coc- overlooked in sediment samples since their tests may
colithophore flagellates) for atmospheric carbon dioxide resemble masses of detrital matter. Care is needed in col-
(CO2) that is absorbed in the seawater and accumulated lecting the sediment to preserve these delicate organisms.
by the foraminiferan as calcium carbonate to build its They have been overlooked in the past as nonliving debris

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 Rhizopoda

or have been so badly destroyed during collection of the which in some species are flagellated, or in others
sediment that they were undetectable. amoeboid. The gametes fuse to form a diploid zygote that
secretes a new shell and enlarges to form a parent organism
thus completing the life cycle. In multichambered spiral-
Reproduction shelled species, the first formed chamber or proloculus is
small and rounded (Figure 5) followed by secretion of
Asexual and sexual reproduction occur among species in successively larger chambers during maturation. See also:
the Rhizopoda. The naked amoebae reproduce asexually Binary Fission in Bacteria; Protozoan Asexuality;
by binary fission. The cell rounds up or becomes discoid Protozoan Sexuality
and divides mitotically to yield typically two identical
daughter cells. The two cells are connected at first by a
cytoplasmic bridge, but soon separate, assume the char-
acteristic species shape and migrate away from each other.
Phylogenetic Evolutionary
Sexual reproduction has not been convincingly observed. Considerations
Testate amoebae reproduce asexually by binary fission.
However, the process is somewhat more complex than in Given the breadth of different groups of protists included
the naked amoebae (gymnamoebae) since a new shell must in the Rhizopoda, it is difficult at present to make broad
be produced to enclose the daughter cell. The parent cell generalisations about their phylogenetic relationships and
produces a bulge of cytoplasm that is extruded from its evolutionary history. It is generally recognised that the
aperture. This bulge forms a mould-like surface whereupon Rhizopoda are not monophyletic and include highly
a new shell is deposited, the two shells being connected at diverse groups that have evolved along many different
their apertures. The cytoplasmic bulge is withdrawn into lines (Cavalier-Smith and Chao, 1996; Hinkle and Sogin,
the parent shell in some species before mitosis but not in 1993; Brown and De Jonckheere, 1994). The presence of
others. Subsequently, the nucleus divides mitotically. an amoeboid habit undoubtedly represents convergent
Eventually, the cell undergoes binary fission by migration evolution and is no longer considered to be a conservative
of one nucleus and a portion of the cytoplasm into the new feature. However, current evidence indicates that the
shell. This is followed by separation of the two daughter amoeboid protists evolved from ancestral flagellates.
cells. Thus, two identical daughter cells with the charac- These flagellates initially comprised two groups the uni-
teristic species-specific shell shape are produced during konts (with a single flagellum) and the bikonts (with two
each division cycle. The slime moulds reproduce asexually flagella). Amoeboid protists appear to have arisen from
and sexually at different stages in their life cycle and there is the unikonts – their flagellated stages, when present, bear
a great deal of diversity among various taxonomic groups. one flagellum (e.g. Minge et al., 2009), whereas members
For example, P. polycephalum produces haploid spores in of the Rhizaria may have branched from the bikonts
sporangia that develop from the multinucleated amoeboid (Burki and Pawlowski, 2006). However, there are alter-
plasmodium during one phase of the life cycle. These are native hypotheses for the origin of the eukaryotes indi-
released and scattered by the wind. They settle on moist cating that a first evolutionary split may lie between
substrata and give rise to flagellated haploid swarmers photosynthetic and nonphotosynthetic forms (e.g.
that act as gametes. Fusion of two swarmers produces Rogozin et al., 2009). The Evidence for phylogenetic
a diploid multinucleated amoeboid plasmodium that can relationships among protozoa in general is derived from
reproduce asexually by fragmentation. Alternatively, three sources: (1) microfossils for species that produce
during unfavourable growth conditions, the plasmodium mineralised tests or skeletons, (2) electron microscopic,
produces a sclerotium (dehydrated, crust-like resting stage) fine structural evidence of cytoplasmic organisation in
that can fragment. Each fragment, containing cysts, pro- living species and (3) molecular genetic analyses to
duces a new plasmodium when environmental conditions determine likely phylogenetic affinities based on protein,
are favourable for resumption of growth (e.g. Anderson, deoxyribonucleic acid (DNA) or ribonucleic acid (RNA)
1992). The plasmodium eventually produces sporangia analyses (Patterson, 1994). Foraminifera and testate
with haploid spores, thus completing the life cycle. The amoebae have excellent microfossil records. The naked
foraminifera have some of the most elaborate reproductive amoebae and most ‘slime moulds’, however, leave no
cycles among the rhizopoda. There is considerable vari- trace in the fossil record and therefore evidence for their
ability in life cycles among the species but a general phylogenetic relationships comes from fine structural and
description follows. During one phase of growth, the par- molecular genetic analyses (e.g. Fiore-Donno et al.,
ent cell reproduces asexually by multiple fission. That is, 2010). Although it is not possible to set forth a grand
the nucleus undergoes multiple divisions followed by scheme for the evolution of the Rhizopoda, there is some
fragmentation of the cytoplasm into many individual evidence for evolutionary and phylogenetic relationships
nucleated cell masses, each of which produces a new shell within subgroups. Evidence is presented for the amoebae
characteristic of the species (for example, Figure 5). In some and foraminifera, which have been the subject of more
species, this is followed by a sexual reproductive phase. intensive investigation. See also: Protozoan Evolution
Each parent foraminiferan produces haploid gametes, and Phylogeny

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Naked and testate amoebae amoebae analysed (Cavalier-Smith and Chao, 1996).
Although much additional research remains to be done,
There is increasing evidence that many of the classical there is strong evidence that the euglyphid testate amoebae,
taxonomic subgroups of the amoebae are artificial and that at least, evolved from a sarcomonad flagellate ancestor by
polyphyletic pathways are more common than previously the loss of flagella and that they are possibly closely related
assumed in some classification schemes, although experts to the amoeboflagellate chlorarachnean algae. Moreover,
in amoeba taxonomy have cautioned for some time that certain members of the sarcomonads such as the thauma-
naked amoebae are probably polyphyletic, based on fine tomonad flagellates are coated with siliceous scales
structural evidence and more refined light microscopic secreted from within the cell. They feed by branched
observations (e.g. Page, 1988). For example, molecular pseudopodia emanating from a ventral groove and exhibit
genetic analyses have confirmed that the subclass Gymno- extensive amoeboid stages. The euglyphid testate amoebae
amoebia is probably polyphyletic since the discoidal are also covered by overlapping siliceous scales and feed by
species Vannella anglica, for example, does not occur on the extruding filose pseudopodia through the terminal aper-
same branch of a taxonomic tree as two other widely ture of the shell. This further augments the conclusion that
occurring species in this subclass (Acanthamoeba castellanii the euglyphid testate amoebae may have arisen from a
and Hartmannella vermiformis) (Sims et al., 1999). Fur- thaumatomonad flagellate ancestor.
thermore, small-subunit ribosomal RNA analyses (SS-
rRNA) indicate that Acanthamoeba, Dictyostelium and
Naegleria are sufficiently divergent that there is no evidence Foraminifera
that they are monophyletic (Baverstock et al., 1989). Even
among the heterolobosean limax amoebae with eruptive Molecular genetic analyses of some benthic foraminifera
locomotion placed in the family Vahlkampfiidae in current indicate that they may be among the earliest known
taxonomic schemes, there is increasing evidence that they eukaryotes possessing mitochondria with tubular cristae
are polyphyletic. This family is characterised by members and may have emerged much earlier than other amoeboid
with flagellated stages (with the exception of those in the protists including the vahlkampfiids and some mycetozoan
genus Vahlkampfia) and presumably may have been among slime moulds such as Physarum (Pawlowski et al., 1996).
the earliest amoeboid protists derived from a flagellated Based on microfossil sedimentary analyses, it is generally
ancestor. Paratetrimitus, Tetramitus and Vahlkampfia assumed that the calcareous shelled species evolved from
appear to be closer relatives of each other than any of the nonshelled species that build tests of agglutinated particles
three are to Naegleria, a widely studied genus occurring in gathered from the environment. The oldest fossil evidence
soils and including a human pathogen (Naegleria fowleri). of foraminifera with agglutinated walls date from the early
The depth of the evolutionary split in the branching path- Cambrian, about 560 Ma, and may have evolved from
way between Naegleria and the other three vahlkampfiids is earlier ancestors with simple organic tests as occur in living
sufficiently large to suggest a relatively ancient divergence. genera such as Allogromia (Tappan and Loeblich, 1988).
This line may have diverged as early as the divergence of Fossil evidence for evolutionary relationships is based on
plants and animals at about one billion years ago (Hinkle changes in morphology from more simple to more complex
and Sogin, 1993). shells, growth patterns as observed in fossil shells and living
The genus Entamoeba, which includes the human intes- representatives of major groups, apertural (major pore)
tinal pathogen Entamoeba histolytica, has no mitochondria characters of the shell, and pattern of occurrence over
and forms multinuclear cysts in contrast to the others in geological time as evidenced in sedimentary layers. It
this subclass that have uninuclear cysts. However, appears that two lines of evolution diverged from the
molecular genetic analyses of species within the genus Allogromiina with simple organic shells. One line diverged
Entamoeba support a monophyletic relationship of this toward the agglutinated (granular) walled species, which
group, and it is included in the Amoebozoa in some modern also contain a certain amount of calcite deposition. This
classifications (Adl et al., 2005). Entamoeba species pro- line eventually could have given rise to the more advanced
ducing cysts that have the same number of nuclei appear to forms with aragonite and calcite walls. The other major line
form monophyletic groups. The most basal or earliest that diverged from Allogromiina may have been by way of
evolved Entamoeba species are those that produce cysts the Fusulinina with microgranular calcitic walls. This
with eight nuclei. The most derived (evolutionary group may have given rise to several branches of evo-
advanced) are those with four-nucleated cysts (Silberman lutionary development including the Miliolina, which form
et al., 1999). See also: Entamoeba and Entamoeba shells with small calcite crystals that are arranged to give a
histolytica; Protozoan Cysts and Spores porcellaneous appearance in reflected light. Although the
Molecular genetic analyses of testate amoebae further fossil evidence suggests that the calcitic species emerged
indicate the polyphyletic quality of the amoeboid organ- from groups with organic walls, molecular evidence points
isms. For example, gene sequence analyses show that the to a possible early emergence of some calcareous wall
testate amoebae Euglypha rotunda and Paulinella chroma- producing genera and this line of inquiry may be very
tophora with filose pseudopodia share a monophyletic productive in resolving the various lines of evolutionary
origin and are not closely related to any of the lobose descent among the highly diverse species of foraminifera.

8 eLS & 2011, John Wiley & Sons, Ltd. www.els.net

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