Hindawi Publishing Corporation
Archaea
Volume 2012, Article ID 596846, 11 pages
doi:10.1155/2012/596846
Review Article
Archaea in Symbioses
Christoph Wrede,1, 2 Anne Dreier,1, 3 Sebastian Kokoschka,1 and Michael Hoppert1, 3
1 Institute of Microbiology and Genetics, Georg-August-Universita¨t Go¨ttingen, Grisebachstraße 8, 37077 Go¨ttingen, Germany
2Hannover Medical School, Institute of Functional and Applied Anatomy, Carl-Neuberg-Straße 1, 30625 Hannover, Germany
3Courant Centre Geobiology, Georg-August-Universita¨t Go¨ttingen, Goldschmidtstraße 3, 37077 Go¨ttingen, Germany
Correspondence should be addressed to Anne Dreier, anne.dreier@gmx.de
Received 5 September 2012; Accepted 19 November 2012
Academic Editor: Martin Kru¨ger
Copyright © 2012 Christoph Wrede et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
During the last few years, the analysis of microbial diversity in various habitats greatly increased our knowledge on the kingdom
Archaea. At the same time, we became aware of the multiple ways in which Archaea may interact with each other and with
organisms of other kingdoms. The large group of euryarchaeal methanogens and their methane oxidizing relatives, in particular,
take part in essential steps of the global methane cycle. Both of these processes, which are in reverse to each other, are partially
conducted in a symbiotic interaction with different partners, either ciliates and xylophagous animals or sulfate reducing bacteria.
Other symbiotic interactions are mostly of unknown ecological significance but depend on highly specific mechanisms. This paper
will give an overview on interactions between Archaea and other organisms and will point out the ecological relevance of these
symbiotic processes, as long as these have been already recognized.
1. Introduction
Symbiotic interactions between various groups of prokary-
otes as well as between prokaryotes and eukaryotic organisms
were one essential driving force of evolution, including
the development of differentiated tissues in multicellular
organisms [1]. Apart from the essential key events of
endosymbiosis, leading to mitochondria and chloroplasts, a
multitude of symbiotic interactions at various levels is an
ongoing process [2]. Interestingly, most of these interactions
are contributed by Bacteria, frequently by Proteobacteria [3].
Regarding parasitic or pathogenic interactions in particular,
the outer envelope of the bacterial cell mediates highly
specific contact to its host. Surface structures like pili,
lipopolysaccharides, and outer membrane proteins may
rapidly adapt to modified host tissue structures, mainly
with respect to deleterious host-pathogen interactions [4].
How about Archaea? Up to now, no clearly identifiable
pathogenic interactions between an Archaeon and its host
have been detected, though some archaeal commensals may
be indirectly involved in bacterial infections [5]. On the other
hand, mutualistic symbioses have been well described, some
of them with high relevance to global environmental cycles
[6]. Here we will present a short overview on interaction
mechanisms known so far and relevant symbioses between
Archaea and other organisms. We use the term symbiosis
here in a broader sense (see Table 1); in most if not all cases
the benefit of both interaction partners could not be proven,
though none of these interactions appeared to be detrimental
for one of the partners [7].
2. Mechanisms for Interaction with Host Cells
Apart from vertically transmitted endosymbionts, any
interaction between host and symbiont depends on the
surface-surface recognition. A variety of proteinaceous and
polysaccharide-based surface structures are known to be
involved. Surface layers are common in all Archaean groups
known so far. Though their function in adhesion is up to
now poorly understood, it may be expected that in particular
the glycosylated surface layers are involved in adhesion. In
fact, like in Bacteria, extracellular polysaccharides are known
as adhesive matrix for biofilm formation [8]. As it has been
described for Bacteria, filamentous protein appendages are
important for adhesion of Archaean cells. Some of them
appear to be unique for particular phylotypes, like the hami,
2 Archaea
Table 1: Some examples for symbioses between Archaea and other organisms (red Archaea, green Bacteria, blue-unicellular Eukarya, and
metazoans).
Symbiotic partners Examples Interaction Key features
Archaeon-Archaeon
Ignicoccus hospi-
talis/Nanaoarchaeum
equitans
Cell-cell contact
Transfer of essential biological
macromolecules from host to
symbiont
Archaea-Bacteria
SM1/Thiothrix Cell appendages Sulfur redox cycling?
ANME-Archaea/sulfate
reducing Bacteria
Cell-cell contact/ no
direct contact
Anaerobic methane oxidation
coupled to sulfate reduction
Archaea-unicellular
Eukarya
Methanogenic
Archaea/Ciliates,
Archamoebae
Endosymbiotic
Methanogen/hydrogenosome
association, transfer of
hydrogen, and/or C1/C2
compounds
Archaea-metazoans
Porifera-associated
Thaumarchaeota
Tissue associated
Ammonia oxidation
Diverse associations
between insect and
vertebrate guts
Gut microbial
communities
Methanogens as a terminal part
of the anaerobic food chain
highly complex proteinaceous appendages appearing like
hooks. These structures are supposedly involved in the
formation of a tight biofilm consisting of the euryarchaeon
SM1 and a filamentous Thiothrix-related sulfur-oxidizing
proteobacterium [9, 10] and seem to be unrelated to any
other known surface appendage. Remarkably, the filamen-
tous protein assembly ends up in a terminal hook. In
addition, short prickles branch from the main filament.
Though it is not known in which way interaction at the
molecular level may work, a tight binding of the cells to each
other and to various surfaces was shown. The filaments and
an exopolysaccharide supposedly excreted by the Archaeon
provide the matrix for the formation of a tight consortium
between the Archaeon and the sulfur oxidizer. The shape
of the consortia may vary but exhibit sort of a “string of
pearl” appearance. Each pearl is in the millimeter order
of magnitude and is colonized by cells of the anaerobic
SM1 Archaeon in the core and a shell of the aerobic sulfur
oxidizer. SM1-related sequences have been detected in low
saline sulfidic water worldwide, thus a certain ecological
significance is likely. The tight association is beneficial
for both symbiotic partners when the Archaeon uses the
sulfate generated by the sulfur oxidizes for dissimilatory
sulfate reduction. The Thiothrix “shell” will provide anoxic
conditions inside the consortium [11].
In this context another apparently unique surface struc-
ture should be mentioned. Though not involved in sym-
biotic interaction, hollow tubes (cannulae) composed of
glycoproteins interconnect the cells of the hyperthermophilic
Pyrodictium occultum [12]. Another uncommon structure
has been described recently by cryoelectron microscopy of
a microbial biofilm [13]. Cells of a member of the archaeal
group Thermoplasmatales form protuberances penetrating
cells of the ultrasmall archaeal Richmond mine acidophilic
organism (ARMAN).
In addition to these unique structures, interaction is fre-
quently brought about by appendages that are also common
to Bacteria. Several pilus types involved in recognition of
and attachment to surfaces have been detected in Bacteria
so far [4]. Yet, by far most of the archaeal pili have
similarities to just the bacterial type IV pilin. Intriguingly,
the archaeal flagellin is homologous to the bacterial pilin
protein. The archaeal rotating flagellum is homologous to
the bacterial type IV pilus secretion apparatus. Consequently,
no homologies between the bacterial flagellar genes and
archaeal sequences could be detected up to now [14, 15].
Also the genes of the machinery for pilus assembly have
been detected in the archaeal genomes. The involvement
of the appendages in attachment may differ in various
groups. The flagella of Pyrococcus furiosus are probably
motility organelles, but are also important for biofilm
formation and surface attachment [16]. Flagella and pili
are also necessary for the aggregate formation and surface
adherence of Sulfolobus solfataricus [17]. As in bacteria, the
pili are responsible for primary adhesion on surfaces and
initiate biofilm formation. The environmental conditions
for biofilm formation have been extensively studied for
several Sulfolobus strains. Basically, temperature, pH, and
iron concentrations, which are also relevant in the natural
(hot spring) habitat, strongly influence biofilm development.
In particular, pH and iron concentration may synergistically
act on biofilm development, but in different ways in various
Sulfolobus strains [18]. In an artificial archaeal biofilm
formed by Pyrococcus furiosus and Methanopyrus kandleri,
Archaea 3
the latter adheres to the surface (mica, glass, and others),
whereas Pyrococcus adheres to Methanopyrus via flagella
and/or direct contact between cells [19]. Haloferax volcanii
uses nonmotile pili for surface attachment [20].
Pili are also involved in interactions between the Archaea
and eukaryote hosts. Methanobrevibacter’s polar pilus-like
fibers are responsible for the attachment of cells to the
hindgut epithelium cuticle of the termite Reticulitermes
flavipes [21].
Generally, a dual nature of cellular appendages (motility
and attachment) is not uncommon and has been also repeat-
edly described for Bacteria [22, 23]. This feature is also true
among Archaea, as the mentioned examples may illustrate.
However, some types of cellular appendages have not been
detected in Archaea. The type III secretion system (TTSS),
in particular, is the essential export mechanism for bacterial
flagellins and is also an important pathogenicity factor.
Specific bacterial proteins are delivered to a eukaryote host
after recognition by the TTSS via a hollow channel. This very
specific interaction to eukaryotes may have been developed
at a time in evolution, when specific signaling between
pathogens and multicellular eukaryotes was evolutionary
useful [24].
3. Archaeon-Archaeon Interaction
The symbiosis between the host Ignicoccus hospitalis and
Nanoarchaeum equitans is well described at the struc-
tural level. Ignicoccus, (Desulfurococcales, Crenarchaeota)
is an anaerobic, hyperthermophilic obligate chemolithoau-
totrophic hydrogen oxidizing Archaeon. Interestingly, cells
belonging to the genus Ignicoccus are surrounded by a dual
membrane, which appears to be a similarity to most Bacteria.
However, the archaeal “outer membrane” is distinct from
the composition of the known bacterial outer membranes.
Most interestingly, the outer membrane of Ignicoccus hosts
the H2: sulfur oxidoreductase and ATPase protein complexes,
that is, membrane energization takes place at this membrane
and not at the inner (normally referred to as cytoplasmic)
membrane as it is common in all Bacteria with a double
membrane cell envelope [25]. Typical porins, homologous
to those in bacterial outer membranes, are missing, which
also implies that the Ignicoccus outer membrane is not
homologous to the outer membrane of Bacteria. Instead,
in Ignicoccus hospitalis, a unique pore-forming complex
(Ihomp1) consists of nine monomers of a small unique
alpha-helical protein [26]; other membrane proteins appear
to be involved in the Ignicoccus/Nanoarchaeum symbiosis as
well [27]. The symbiont Nanoarchaeum equitans depends
obligately on the Ignicoccus host. TheNanoarchaeum cells are
directly attached to the outer membrane of Ignicoccus. The
extremely reduced genome (490Kbp) lacks genes for essen-
tial biosynthetic pathways, such as lipid, amino acid, and
nucleotide biosynthesis. Thus biological macromolecules
must be provided by the Ignicoccus host; even transfer of ATP
from host to symbiont has been discussed [28].
The relationship between Ignicoccus and Nanoarchaeum
does not appear to be a true mutualistic symbiosis: though
the growth parameters of either infected or uninfected
Igni-coccus cultures (containing infected cells of different
degrees and uninfected cells) are the same, attached Nanoar-
chaeum cells significantly reduce the ability of Ignicoccus to
reproduce [29].
Up to now, direct interactions between two archaeal
partners appear to be extremely rare. Other species of the
genus Ignicoccus are free living and could not be infected
with theNanoarchaeum equitans symbiont [29]. Though it is
unlikely that interactions within the kingdom of Archaea are
an exception, it has to be taken into account that interactions
between largely unculturable organisms are difficult to
detect. In an artificial binary biofilm between Pyrococcus
furiosus and Methanopyrus kandleri hydrogen produced by
Pyrococcus is utilized by Methanopyrus, which implies that
mutualistic benefits may lead to stable aggregations between
Archaea [18]. Upcoming in situ techniques may uncover
interactions between Archaea in the near future [13].
4. Archaea-Bacteria Interactions
Under anaerobic conditions, organic compounds are
degraded by the anaerobic food chain whereby the product
of one group serves as a substrate for the next group within
this chain. Methanogenic Archaea terminate the chain by
degrading C1 and C2 substrates to methane and carbon
dioxide.
The conversion of higher organic acids to acetate and
hydrogen is endergonic, unless the hydrogen partial pressure
is kept low. This may be achieved by the activity of
hydrogenotrophic methanogens. This necessary coupling of
hydrogen formation and uptake by syntrophic microbial
consortia is termed “interspecies hydrogen transfer.” A
well-known consortium, “Methanobacillus omelianskii,” was
isolated several times from anaerobic sediments and sewage
sludge and was regarded as a pure culture of an anaerobe
converting ethanol to acetate and methane [30]. In fact,
the culture consisted of a methanogenic archaeon and a
Gram-negative Bacterium [31, 32]. Since then a multitude
of syntrophic associations have been described, for example,
with the fermentativeAcetobacterium or Syntrophobacter [33,
34], withDesulfovibrio under low sulfate concentrations [35],
but also under thermophilic conditions with Thermoanaer-
obacter, Desulfotomaculum, and Pelotomaculum [36–38] and
with hydrogenotrophic methanogens as syntrophic partners.
These examples show the diversity of interactions with
respect to organisms and metabolic properties. Though
stable aggregates and specific interactions between the
syntrophic partners have been observed [39], syntrophy in
interspecies hydrogen transfer is generally highly variable
and may depend on the availability of substrates [40].
An important process of methane oxidation in anoxic
sediments is conducted by consortia of Euryarchaeota and
sulfate reducing Bacteria (SRB). The anaerobic oxidation
of methane (AOM) has been first postulated by Reeburgh
[41]. Up to 90% of methane produced in marine sediments
is anaerobically oxidized [42], which makes AOM to an
essential process in global methane turnover. However,
quantitative modeling based on existing data of the few
sampling sites at the ocean floor is still difficult and
4 Archaea
the contribution of the process to global methane cycling
is still a matter of debate [43]. In ocean systems, methane
is either generated by methanogenesis in sediments, or abi-
otically by serpentinization, and may derive from methane
hydrates and fossil reservoirs. In cases of high methane fluxes
from large reservoirs, the AOM is usually associated with
the precipitation of carbonates and sulfides. This has been
particularly observed at sites of intense methane seepage,
such as marine mud volcanoes and cold methane seeps;
also fossil seeps were identified [44–46]. These precipitates
are mostly found in sediments as carbonate-cemented plates
or large tabular constructions, but also as grapestone-like
concretions or even as giant columnar structures, up to
several tens of meters in height, buried in the sediment [47–
49]. Under anaerobic conditions, below the chemocline of
anoxic ocean basins, these precipitates may form tower-like
constructions in the water column, reaching several meters
in height [50–52]. In most cases, tube-like or columnar
towers exhibit cavities that are perfused by methane and
seawater. The inner faces of these concretions are covered
by remarkably complex biofilms [53–55], dominated by
various representatives of the ANME Archaea (ANME:
anaerobic methanotroph). The three known ANME groups
are not monophyletic. ANME-1 are distantly related to
Methanomicrobiales [56], while ANME-2 and ANME-3 are
distantly related to Methanosarcinales [57, 58]. A fourth
group has been described as ANME-2d or GoM Arc I;
this group is not monophyletic with the other ANME-2
subgroups [59–61]. AOM metabolism for this novel group
has not yet been proven [42]. ANME-1 and ANME-2 are the
most diverse groups detected in a multitude of habitats and
appear to be most relevant for AOM in anoxic environments.
ANME-1 cells exhibit a cylinder-shaped morphology with
an external sheath and were found only in loose association
with SRB of the Desulfococcus/Desulfosarcina (DSS) group
[53]. ANME-2 cells are coccoid and are frequently detected
in consortia with SRB [55, 62]. In ANME-2a/SRB-aggregates,
both cell types appear to be randomly intermixed, while
ANME-2c/SRB aggregates reveal a shell-like structure with
SRB at the outer shell of the aggregate. ANME-2 are usually
associated with SRB of the DSS group [63, 64], but also
associations with alpha-Proteobacteria, beta-Proteobacteria,
or Desulfobulbus-related SRB and ANME-2 cells without
contact to other bacteria were reported [65–71].
There is up to now no indication that the metabolism
of the SRB in AOM is distinct from free-living sulfate
reducing bacteria. The metabolic pathway of the ANME
archaea is clearly related to methanogenesis. Intriguingly,
ANME Archaea use this pathway in the reverse direction,
while reducing equivalents are transferred to SRB [42, 72].
Until now, it seems that AOM with ANME Archaea is
feasible just in syntrophy with sulfate reduction. A recently
discovered thermophilic ANME group closely affiliated to
ANME1 (ANME 1c), though may conduct AOM in contact
to hydrothermal vent systems without SRB and with Fe3+ as
putative electron acceptor. However, conclusive evidence is
still missing in this case [73].
The methyl-coenzyme M reductase (MCR) catalyses
in methanogenic archaea the terminal step of methane
formation. In reversal, MCR is needed in a reversed
methanogenic pathway for the initial step of AOM; also most
of the other enzyme steps of methanogenesis operate in the
reverse direction [74–76]. However, direct evidence for the
reverse operation of this pathway is still lacking.
Intermediates for a necessary transfer of reducing equiv-
alents between the syntrophic partners are still unknown.
In vitro feeding studies excluded hydrogen, formate, acetate,
methanol, and even more uncommon compounds like
methylsulfides or humic acids [77–81]. The energy yield of
AOM is still extremely low, compared with other anaerobic
processes [82].
Recent findings indicate that the ANME Archaea are
capable of both methane oxidation and sulfate reduction
with elemental sulfur as an intermediate [83]. The reduced
product HS2
−may be the disproportionated by the symbiotic
sulfate reducers to sulfate and HS−. Thus, the symbioses may
be less obligate than originally thought.
ANME-2 Archaea in consortia also conduct nitrogen
fixation [84]. Nanometer secondary ion mass spectrometry
(nano-SIMS) analysis implied the flow of nitrogen com-
pounds from the Archaea to the sulfate reducers. Remark-
ably, the energy consuming nitrogen fixation is possible even
under the conditions of the extremely low energy yield of
AOM, though growth rates of the organisms were reduced
by a factor of 20. Since AOM is a mayor sink of methane in
marine sediments, nitrogen fixation by AOM may be as well
a relevant process in the global nitrogen cycle. By this way,
carbon, nitrogen, and sulfur cycles are linked by AOM.
Other recently described AOM processes may also be
independent of archaeal groups. AOM with iron (Fe3+)
and mangenese (Mn3+, Mn4+) has been described for
enrichment cultures from marine sediment samples, but a
direct involvement of either archaeal or bacterial phylotypes
is speculative [85]. A nitrite/nitrate dependent AOM is
conducted by Bacteria (NC10 phylum, candidatus Methy-
lomirabilis oxyfera; [86]). This process is clearly distinct from
ANME/SRB AOM and appears to be homologous to the
aerobic methane oxidation of methanotrophic Bacteria.
Another cell-cell interaction between the giant filamen-
tous thaumarchaeote candidatus Giganthauma karukerense
and a sulfur oxidizing gamma-Proteobacterium has been
described recently [87]. A closed cell monolayer of the
proteobacteria covers the surface of the large thaumarchaeote
filament. It is not known in how far the cells may interact
physiologically. It might be possible that the sulfur oxidizer
reduces the sulfide concentration in the immediate vicinity
of the host cell.
5. Interaction between Archaea and Eukarya
With respect to hitherto known mutualistic symbioses with
eukaryotes, most but not all Archaea are members of the
methanogenic Euryarchaeota. Methanogens are essential
in the degradation of organic substrates under anaerobic
conditions to methane and carbon dioxide, as terminal part
of the anaerobic food chain. It is reasonable to assume
that organisms with guts as anaerobic niches of nutrient
decomposition harbor also methanogens as commensals.
Archaea 5
Remarkably, a single methanogen phylotype, Methanobre-
vibacter smithii, is known to be the predominant Archaeon
in the human gut microflora [88]. Symbioses between
Archaea and eukaryotes, however, are not restricted to
the gut anaerobic food chain. Many of the anaerobic
protozoa, either free living or gut symbionts themselves,
contain methanogenic Archaea as endosymbionts. These
free-living protozoa are widespread in sapropels. Instead
of mitochondria, they contain hydrogenosome organelles
lacking a tricarboxylic acid cycle [89]. Hydrogenosomes
are descendants of mitochondria. In these organelles, ATP
is generated in a fermentative pathway by conversion of
acetyl-CoA to acetate; the reducing power is released as
molecular hydrogen [90]. Hydrogenosomes are a prereq-
uisite for the occurrence of endosymbiotic methanogens,
and hydrogenotrophic methanogens use hydrogen and car-
bon dioxide or formate as substrates for methanogenesis
[91]. Also acetoclastic methanogens may take benefit from
acetate generated by the hydrogenosome [92]. Regularly,
these symbionts are transmitted vertically in the protists.
Consequently, the phylotypes of the methanogens differ
with respect to the protist groups and their habitats.
Methanogens from free-living ciliates in freshwater habitats
are related to Methanomicrobiales, whereas endosymbionts
in ciliates from millipedes, cockroaches, and even frogs are
Methanobacteriales [93]. However, during culturing, ciliates
may also tend to lose their symbionts and also uptake of
Methanobacterium formicicum by the ciliate Trimyema com-
pressum has been reported [94]. Mechanisms of interactions
between the methanogens and protists are largely unknown.
Several morphological peculiarities have been described.
In the free-living ciliate Metopus contortus polymorphic
endosymbionts were observed; some cells appear to lose their
cell walls and become directly attached to hydrogenosomes
[95]. Also variations in size (putatively due to enlargement of
cells) and stellate shape of the endosymbiont with close con-
tact to hydrogenosomes have been observed repeatedly [96].
These results show that a peculiar crosstalk between the
symbiotic partners is necessary. Like in well-studied symbio-
sis between eukaryotes and bacterial endosymbionts (includ-
ing intracellular pathogens), protection against lysosomal
digestion or cytoskeletal rearrangements of the vacuole
containing the endosymbiont requires elaborate signaling
pathways between host and symbiont partners [97]. It is
reasonable to assume that the Archaean symbionts possess
respective signaling mechanisms. However, the endosymbi-
otic associations between several groups of protists (Ciliata,
and some representatives within groups of Archamoebae)
are the only known endosymbioses so far. Thus, this way
of interaction with eukaryotes does not appear to be a
mainstream in archaeal life styles [98, 99].
Sponges, organisms at the evolutionary basis of the
Metazoa, may be described as a diverse prokaryotic com-
munity in a eukaryote host, most of the prokaryotes with
largely unknown function [100]. Though the majority of the
organisms are free living in the sponge mesohyl, endosym-
bionts are common. Among cyanobacteria and heterotrophic
bacteria, also fission yeasts have been described that are
maternally transmitted via sponge eggs [101].
Archaea are ubiquitous in marine sponges, sometimes
even dominant [102], though their ecological role is poorly
understood. Since the composition of the archaeal com-
munity is distinct from seawater, a certain specificity of
the sponge/Archaeon association must be assumed [103].
Also rather specific associations between certain archaeal
phylotypes and sponges have been described. The association
between a sponge and the Thaumarchaeota (formerly Cre-
narchaeota; [104, 105]) Cenarchaeum symbiosum has been
first described for Axinella mexicana [106]. Three species
of the Mediterranean Axinella harbor filamentous marine
“group 1” Archaea colonizing the collagen surrounding the
sponge spicules [107]. Marine Euryarchaeota are associ-
ated with the demosponge Tentorium semisuberites mesohyl
[102]. The role of these symbioses is largely unknown,
also with respect to the unknown ecological role of the
marine Thaumarchaeota. Recent findings imply significance
in the sponge nitrogen metabolism [103, 108, 109]. A
vertical transmission of the ammonia-oxidizing Archaea
also indicates the specificity of the symbiotic relationship
[110]. Ammonia oxidizers may utilize ammonia excreted by
the sponge as a metabolic end product and may thereby
contribute to detoxification of the sponge tissue. This may be
in particular of relevance in highly polluted areas, where high
concentration of organic compounds and high ammonia
concentrations affect marine biocoenoses [103].
The important role of Thaumarchaeota in nitrogen
cycling, also with respect to symbioses, has been also
identified in some marine mollusks: strains phylogenetically
related to Nitrosopumilus maritimus were detected inside the
tissue of the colonial ascidian Cystodytes dellechiajei. Here,
nitrification of the Archaeon could be determined in situ
[111]. Recent studies on the diversity of ammonia oxygenase
genes also show that ammonia oxidizing archaeal commu-
nities differ in various coral species and are also distinct
from communities in the sediment or in the water column
[112, 113]. It must be expected that symbioses between other
groups of marine invertebrates and Thaumarchaeota are also
of relevance, in particular with respect to ammonia oxidation
[114].
Among arthropods, as the largest animal phylum, only
in the groups of millipedes, cockroaches, termites, and
scarabs relevant methane producing species are present [93].
Methanogens represent the terminal part of the anaerobic
food chain in the guts of these insects (especially termites).
In this symbiosis, these Archaea utilize the main degradation
products hydrogen, carbon dioxide, and acetate released
by the previous steps of anaerobic lignocellulose degra-
dation [115]. All methanogens, including the methanogen
endosymbiont-bearing ciliates, are in the hindguts of these
arthropods [116]. Free-living methanogens adhere to the
hindgut wall. Among these big groups, a correlation between
a specific diet (e.g., plant litter) and methane production
could not be found, and not all members of the mentioned
groups contain methanogens. However, in the group of
higher termites, soil feeding termites produce more methane
and contain more methanogens (according to 16S rRNA
analysis) than wood feeders [117]. In the soil feeding species
Cubitermes fungifaber, the composition of the communities
6 Archaea
vary across the species, which does not account for a pure
vertical transmission of the gut community, but a strong
influence of the community in food soil [118]. Remarkably,
also a Natronococcus-related sequence could be retrieved
from the gut. Related strains are obligate haloalkaliphilic
organisms of the family Halobacteriaceae, isolated from soda
lakes, and are aerobic heterotrophic Archaea [119]. The
Natronococcus-related strain may be well adapted to the first
section of the hindgut (P1 part). This section provides a
highly alkaline environment, reaching a pH around 12. For
Cubitermes ortognatus, an in depth analysis of archaeal com-
munities in four sections of the hindgut revealed remarkable
distinctions in particular between the alkaline P1 part
and the following P3–P5. Whereas Methanosarcinaceae–
related sequences dominated in P1, they were replaced by
Methanobacteriaceae-related clones in all other posterior
parts of the gut. Interestingly, also Thermoplasmatales and
Crenarchaeota contributed up to 40% to the archaeal com-
munity in these parts. The ecological role of these archaeal
groups have to be elucidated yet.
Methanogenesis in termites is a globally relevant
source of methane, with 20–29 Tg methane per year
[120]. Methanogens from all ruminants produce 91–107 Tg
methane per year, which is the second largest methane source
after wetlands. In ruminants, methanogens are in a similar
way the terminal part of the anaerobic lignocellulolytic food
chains as in termite hindguts and methanogen/ruminant
symbioses have been extensively studied. Some methanogens
like Methanobacterium bryantii or Methanobrevibacter rumi-
nantium were isolated from rumen fluids and were exten-
sively studied with respect to biochemistry and energetics
in methanogens, including genome analysis of Methanobre-
vibacter [121, 122]. Abundant adhesin-like sequences in
the Methanobrevibacter genome imply intensive interactions
between the methanogen and other rumen microbes. In
coculture experiments with Butyrivibrio proteoclasticus, sev-
eral Methanobrevibacter adhesins were upregulated and co-
aggregates of both cell types were observed [122]. Inter-
estingly, formate utilisation genes were also upregulated.
Butyrate, acetate (or lactate), formate, carbon dioxide, and
hydrogen gas are major fermentation products of Butyri-
vibrio during growth on xylan [123, 124]. Hydrogen and
formate may be utilized by Methanobrevibacter in this syn-
trophic interaction. In addition to free-living methanogens
in the rumen fluid, methanogens which are extra- and
intracellularly associated with ciliate protozoa are relevant
contributors to methane production. In ruminants, more
than one-third of the methane may be produced by these
consortia [125].
One might consider that the presence or absence of
methanogens in vertebrates generally depends on the diet
or the presence of specific anatomical differentiations of the
gut and all herbivorous animals harbor the entire anaerobic
food chain. Systematic analysis of the methane production
in guts of 253 vertebrate species revealed that methane
production and hence the presence of relevant amounts of
methanogens does depend on the phylogenetic lineage of the
animal rather than on the diet or the anatomy of the digestive
system [126]. In some phylogenetic lineages like ostriches,
intestinal methanogens got lost irrespective of the diet.
Methanogens are also missing within the large lineages of
Carnivora/Chiroptera/Eulipotyphla (formerly Insectivora),
even in herbivorous pandas (Ursidae/Carnivora). Though
in all other large lineages methane producers dominate,
nonproducers occur also in several “branches” of these lin-
eages. Generally, the results imply that once themethanogens
got lost in the course of evolution, they did not reappear
in the descending lineages [126]. One special case with
respect to the bird digestive system has drawn attention
recently. The hoatzin (Opisthocomus hoazin) is the only
known example for foregut fermentation in birds similar to
the ruminants [127, 128]. The rumen methanogens found
in hoatzins are more closely related to ruminant strains
than to methanogens found in feces of other birds, though
the composition of the methanogen community and the
phylotypes themselves were still distinct from those found in
ruminants [129].
In the intestines of primates, including humans, Archaea
are present. Methanobrevibacter smithii as the dominant
species draws particular attention: a syntrophic interaction
between Methanobrevibacter and Bacteroides thetaiotaomi-
cron, as studied in gnotobiotic mice, may affect the energy
balance of the host [130]. Methanobrevibacter utilizes the
Bacteroides fermentation product formate. This syntrophy
obviously determines the expression of Bacteroides enzymes:
the pathway directed towards formate and acetate produc-
tion is upregulated, whereas alternative pathways towards
propionate and butyrate are downregulated. The ongoing
human microbiome project will soon update our knowledge
on archaeal diversity and putative function in humans.
6. Concluding Remarks
Interactions between Archaea and other organisms are
definitely as specific as interactions with symbiotic Bac-
teria prokaryotes. Up to now, the mechanisms of surface
recognition are still poorly understood. The prominent
“model” pathogens Escherichia coli, Salmonella typhimurium,
Pseudomonas aeruginosa, and Vibrio spp. greatly extended
our knowledge on specific interactions of Proteobacteria
with animal host tissue. However, model organisms of this
kind are still missing in the archaeal world, due to the lack
of easy manageable molecular tools for functional studies, in
particular with respect to the generation of mutant strains. In
addition, we are still far away from even a rough estimate of
the true sizes of the large archaeal clades. Hence, we are still
unable to explore the diverse ways how Archaea may interact
with each other. The description of the few very diverse cases
that we know—considering the fundamental differences, for
example, between Nanoarchaeum and Ignicoccus or the SM1
and sulfur reducer interaction—gives us an impression on
the diverse ways how Archaea may interact and how diverse
the mechanisms may have to be expected (see Table 1).
The symbiotic interaction between prokaryotes also
leads to the question if the first eukaryote may be an
offspring of a symbiotic interaction between an Archaeum
and a Bacterium ([131] and references therein). Though
the different roles of ancient Archaea and Bacteria are still
Archaea 7
speculative, it becomes more and more obvious that tight
symbiosis between both prokaryotic cell types also direct us
to the roots of eukaryote evolution.
Acknowledgments
The Authors are indebted to a DFG grant to M. Hoppert
(Ho 1830/2-1) and a fellowship of the Studienstiftung des
Deutschen Volkes to A. Dreier. This is Courant Research
Centre Geobiology publication no. 112.
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