MINIREVIEW
Diversity and ecophysiological features of thermophilic
carboxydotrophic anaerobes
Tatyana G. Sokolova1, Anne-Meint Henstra2, Jan Sipma3, Sofiya N. Parshina1,4, Alfons J.M. Stams4 &
Alexander V. Lebedinsky1
1
Winogradsky Institute of Microbiology, Russian Academy of Sciences, Moscow, Russia; 2Subdepartment of Environmental Technology, Wageningen
University, Wageningen, The Netherlands; 3Department of Chemical, Agricultural Engineering and Agricultural Technology, University of Girona,
Girona, Spain; and 4Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands
Correspondence: Tatyana G. Sokolova,
Winogradsky Institute of Microbiology,
Russian Academy of Sciences, Prospect 60 Let
Oktyabrya, 7/2, Moscow 117312, Russia. Tel.:
17 499 135 4458; fax: 17 499 135 6530;
e-mail: [email protected]
Received 1 October 2008; revised 21 January
2009; accepted 31 January 2009.
First published online 17 March 2009.
DOI:10.1111/j.1574-6941.2009.00663.x
Abstract
Both natural and anthropogenic hot environments contain appreciable levels of
carbon monoxide (CO). Anaerobic microbial communities play an important role
in CO conversion in such environments. CO is involved in a number of redox
reactions. It is biotransformed by thermophilic methanogens, acetogens, hydrogenogens, sulfate reducers, and ferric iron reducers. Most thermophilic COoxidizing anaerobes have diverse metabolic capacities, but two hydrogenogenic
species are obligate carboxydotrophs. Among known thermophilic carboxydotrophic anaerobes, hydrogenogens are most numerous, and based on available data
they are most important in CO biotransformation in hot environments.
Editor: Ian Head
Keywords
carbon monoxide; anaerobic carboxydotrophic
thermophiles; hydrogenogens; CO
dehydrogenases; CODH–ECH gene clusters.
Introduction
Carbon monoxide (CO) is an atmospheric trace gas. Its
concentration in the Earth’s atmosphere is 0.06–0.15 p.p.m.
(IPCC, 2001). The low CO level in the atmosphere is due
to its reactivity with OH and consumption by aerobic
carboxydobacteria inhabiting soils (for references, see
King & Weber, 2007). CO is a potent electron donor (E0 0 is
520 mV for the CO/CO2 couple), and, although it may be
inhibitory to iron proteins of both aerobes and anaerobes
(Adams, 1990), CO is utilized by many microorganisms.
The biodiversity, biochemistry, and ecology of bacteria that
grow aerobically with CO have been intensively studied and
reviewed (Zavarzin & Nozhevnikova, 1977; Meyer et al.,
1990; Conrad, 1996; King & Weber, 2007). A number of
anaerobes are also known to metabolize CO. Many of them
are thermophiles isolated and described in recent years.
Here, we discuss the presence of CO as a substrate in hot
anaerobic environments, its transformation pathways, and
the phylogenetic and functional diversity of thermophilic
carboxydotrophic anaerobes.
FEMS Microbiol Ecol 68 (2009) 131–141
CO levels and sources in hot anaerobic
environments
The CO levels in hydrothermal environments vary from 0.6
to 5540 p.p.m. in gases (Sato et al., 2002; Tassi et al., 2003;
Shock et al., 2005; Chiodini et al., 2006; Garofalo et al.,
2007), or may be as high as 5000 nM of dissolved CO
detected in fluids emanating at the Rainbow vent site on
the Mid-Atlantic Ridge (Charlou et al., 2002). Trace levels of
CO were observed in methanogenic bioreactors (Hickey
et al., 1987; Bae & McCarty, 1993). Some bioreactors are
fed with synthesis gas, consisting of H2, CO, and CO2, as a
cheap source of hydrogen used in various biological reductive reactions, but a content of 5–60% CO in the synthesis
gas limits its direct industrial application (Sipma et al., 2006,
2007). CO in hydrothermal environments originates from
volcanic gases (Menyailov & Nikitina, 1980; Symonds et al.,
1994; Allard & Barton, 2004). CO may be produced in a
process linked to oxygenic photosynthesis (Hoehler et al.,
2001) or may be a product of thermochemical or photochemical degradation of organic matter (Conrad & Seiler,
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132
1985; Schade et al., 1999; Hellebrand & Schade, 2008). CO is
also an intermediate in the reversible reaction of acetyl-CoA
synthesis or cleavage by anaerobes using the Wood–Ljungdahl pathway (Ragsdale, 2004). Small amounts of CO may
be released in this reaction as demonstrated under laboratory conditions for Moorella thermoacetica (Diekert et al.,
1984) and Methanothermobacter thermautotrophicus (Conrad & Thauer, 1983; Eikmanns et al., 1985).
Microbial CO transformation pathways in
hot environments
In hydrothermal environments, CO may serve as an electron
donor in a number of redox reactions that provide energy for
microbial metabolism. Oxidation with oxygen and nitrate
may be driven by aerobic carboxydotrophs; among them,
very few thermophiles have been described (King & Weber,
2007). CO may be oxidized in reactions with water by some
methanogens, acetogens, and hydrogenogens or in reactions
with sulfate or ferric iron by some sulfate reducers and iron
reducers (Sipma et al., 2006; Slobodkin et al., 2006).
Many reactions involving CO may be potential metabolic
energy sources as calculated from the actual concentrations
measured in the hydrothermal Obsidian Pool of Yellowstone
National Park, a hot spring that may be considered a typical
model ecosystem (Shock et al., 2005). Thirty-five such
reactions involving CO were identified, and 147 reactions
involving other reduced compounds (CH4, Fe21, pyrite, H2,
and H2S). It was found that reactions involving CO are
among the most favorable for energy conservation by
microorganisms. In the order of decreasing energy output,
oxygen, nitrate, nitrite, sulfur, sulfate, ferric iron, and H2O
are oxidants for CO. Hot springs are open systems, which
allows many different redox reactions to take place simultaneously (Shock et al., 2005).
Anaerobic CO transformation by the microbial communities of three pH-neutral hot springs of Uzon Caldera
(Kamchatka) with temperatures from 60 to 90 1C was traced
using 14CO (Slepova et al., 2007a). The major part of 14CO
was oxidized to 14CO2. Less than 5% was transformed to
volatile fatty acids in samples from the spring with a
temperature of 60 1C and o 1% in springs with higher
temperatures. 14C incorporation into methane or cells was
not detectable. The actual rate of CO transformation was
calculated to be about 0.09 mmol CO L1 sediment day1
(Slepova et al., 2007b). From these hot springs, moderately
and extremely thermophilic carboxydotrophic hydrogenogenic anaerobes of the genera Carboxydocella and Dictyoglomus were isolated (Slepova et al., 2007b).
Experiments with sludges from seven different full-scale
anaerobic bioreactors revealed that CO conversion to
methane at 30 1C occurred via acetate, while incubation of
the same sludges at 55 1C revealed fast evolution of H2 upon
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T.G. Sokolova et al.
CO conversion in five tested sludges (Sipma et al., 2003).
The main CO conversion routes found for anaerobic
bioreactor sludges are shown in Fig. 1. From anaerobic
reactor sludge, a carboxydotrophic hydrogenogenic sulfatereducing thermophilic bacterium, Desulfotomaculum carboxydivorans, was isolated (Parshina et al., 2005b).
Thus, the experiments on CO transformation by microbial communities of hydrothermal environments and bioreactors suggest a significant role of carboxydotrophic
hydrogenogenic prokaryotes in this process.
CO metabolism in anaerobes
Utilization of CO by thermophilic anaerobes is catalyzed by
Ni-containing CO dehydrogenases (CODHs) and acetylCoA synthases (ACSs). CODHs and CODH/ACS complexes
are widespread among anaerobes and are found in methanogens, acetogens, sulfate reducers, and iron reducers.
CODH/ACS complexes catalyze both catabolic and anabolic
acetyl-CoA synthesis and cleavage reactions, in which CO is
an intermediate that travels along a hydrophobic channel
between the CODH and ACS active sites (Ragsdale, 2004).
The capacity to use exogenous CO by CODH/ACS complexes is a debatable topic. Many relevant papers infer direct
and preferential incorporation of CO into the acetate
carboxyl group (Stupperich & Fuchs, 1984; Martin et al.,
1985; Henstra et al., 2007), but preferential incorporation of
CO2-derived CO has also been reported (Ragsdale, 2004).
The common opinion that, both in acetogens and methanogens, CO is not a direct precursor of the methyl group of
acetate is more definite. Neither is it a direct precursor for
methane in methanogens. In both cases, CO is first oxidized
to CO2 (Stupperich & Fuchs, 1984; Martin et al., 1985; Ferry
& House, 2006; Henstra et al., 2007).
It may be expected that the main enzymes responsible for
the utilization of exogenous CO by anaerobes are the
CODHs that are not part of a CODH/ACS complex. Our
analysis of 988 available microbial genomes (c. 60 thermophiles) revealed 64 genomes (including 10 thermophiles,
Table 1) that contained Ni-CODH genes. Note that these
values are considerably higher than King & Weber (2007)
(a)
(b)
H2 /CO
CH4
CO
CH3COO–
CO
H2 /CO
H2
?
CH4
CH3COO–
Fig. 1. Schematic presentation of the main CO conversion routes by
anaerobic full-scale wastewater-treating sludge samples at (a) 30 1C and
(b) 55 1C. Lines with cross represent conversion routes that were absent.
The line thickness corresponds to the rates of the processes.
FEMS Microbiol Ecol 68 (2009) 131–141
133
Thermophilic carboxydotrophic anaerobes
Table 1. Numbers of genes encoding Ni-CODHs and ACSs, numbers of CODH/ACS, ECH, and CODH/ECH gene clusters in the genomes of
thermophiles that contain at least one CODH or ACS gene
Species
Carboxydothermus hydrogenoformans
Thermosinus carboxydivorans
Caldanaerobacter subterraneus ssp.
tengcongensis
Moorella thermoacetica
Methanosaeta thermophila
Methanocaldococcus jannaschii
Methanopyrus kandleri
Methanothermobacter thermautotrophicus
Archaeoglobus fulgidus
Clostridium thermocellum
CODH
genes
ACS
genes
CODH/ACS gene
clusters
ECH gene
clusters
CODH/ECH gene
clusters
Growth on
CO
5
3
1
1
0
0
1
0
0
1
1
2
1
1
1
1
1
ND
2
3
2
3
1
3
1
1
1
2
1
1
1
0
1
1
1
1
1
0w
0
1
0
2
1
2
0
1
0
0
0
0
0
0
0
1
ND
ND
ND
1
1
ND
The table is based on our analysis at the NCBI ‘BLAST with microbial genomes’ site (http://www.ncbi.nlm.nih.gov/sutils/genom_table.cgi).
The NCBI site uses the former name Thermoanaerobacter tengcongensis.
w
Archaeoglobus fulgidus was the only organism (not only among thermophiles) in which the ACS gene did not cluster with any of the CODH genes
present.
ND, no data.
estimated the frequency of occurrence of the aerobic COoxidizing capacity (eight of 330 genomes). Of the 64
genomes that contained one or more Ni-CODH genes, as
few as seven, including that of the thermophile M. thermautotrophicus (Table 1), encoded only CODHs as part of
CODH/ACS gene clusters. It may be speculated that these
organisms are mainly capable of dealing with endogenous
CO. The remaining genomes contained Ni-CODH genes
additional to those in CODH/ACS gene clusters or lacked
ACS (Table 1). It may be speculated that these organisms are
adapted to deal with exogenous CO.
In the metabolism of many microorganisms possessing
Ni-CODHs, so-called energy-converting hydrogenases
(ECHs, Table 1) play an important role. ECHs form a
subclass within the class of [NiFe]-hydrogenases (Hedderich, 2004; Vignais & Billoud, 2007). ECHs are multisubunit
membrane-bound enzyme complexes able to pump ions out
of cells at the expense of proton reduction with lowpotential electrons, including those derived from CO (E0 0
is 520 mV for the CO/CO2 couple and 414 mV for the
H2/H1 couple). ECHs can also mediate the reverse transfer
of electrons from hydrogen to low-potential electron carriers
at the expense of the transmembrane ion gradient; these
electrons can then be used for the reduction of CO2 to CO
(Meuer et al., 2002; Hedderich, 2004).
CO utilization by methanogenic archaea
Methanothermobacter thermautotrophicus DH, isolated from
sewage sludge (Zeikus & Wolfe, 1972), is the only thermophilic methanogen tested for the capacity to grow on CO. It
converts CO according to the equation 4CO12H2O =
CH413CO2 (DG0 0 = 52.7 kJ mol1 CO). The growth rate
FEMS Microbiol Ecol 68 (2009) 131–141
on CO was only 1% of that on CO2/H2 (Daniels et al., 1977).
It may be expected that the capacity for growth on CO can
also be found in other thermophilic methanogens, because,
among mesophiles, more studied in this respect, six representatives of the genera Methanosarcina, Methanobacterium,
and Methanobrevibacter were reported to grow on CO
(Daniels et al., 1977; O’Brien et al., 1984; Rother & Metcalf,
2004).
Methanothermobacter thermautotrophicus DH genome
contains a single CODH gene, and, judging from its
genomic environment, this CODH is part of a CODH/ACS
complex (Table 1). Methanocaldococcus jannaschii, Methanopyrus kandleri, and Methanosaeta thermophila contain in
their genomes additional CODH genes beyond CODH/ACS
gene clusters and thus seem to be better able to use
exogenous CO than M. thermautotrophicus. Methanothermobacter thermautotrophicus has been found in various hot
environments, including hot springs in Yellowstone National Park and Iceland (Sandbeck & Ward, 1982) and
biogas reactors.
Thermophilic acetogenic CO-oxidizing
bacteria
Many acetogens can grow on CO (Drake et al., 2006). CO
conversion has been documented for 10 acetogens, including four moderate thermophiles: M. thermoacetica, Moorella
thermoautotrophica, Thermoanaerobacter kivui, and Moorella perchloratireducens, recently described by Balk et al.
(2008). Moorella thermoautotrophica and M. thermoacetica
can grow on CO at high partial pressures as the sole energy
source (Savage et al., 1987; Daniel et al., 1990). Moorella
thermoacetica and T. kivui can oxidize CO during growth on
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134
T.G. Sokolova et al.
other substrates (Diekert & Thauer, 1978; Yang & Drake,
1990). Most M. thermoacetica strains (11 of 13 tested)
possess this ability (Daniel et al., 1990). Acetogens grow on
CO according to the equation (Drake & Daniel, 2004):
4CO þ 2H2 O ! CH3 COOH þ 2CO2
ðDG00 ¼ 41:4 kJ mol1 COÞ
The genome of M. thermoacetica contains two CODH
genes (Table 1). Only one of them is part of a CODH/ACS
gene cluster. Thus, M. thermoacetica is among those rather
numerous organisms in which CO oxidation is not just a
side effect of the capacity for acetate synthesis or cleavage.
Moorella thermoautotrophica, originally isolated from a
hot spring (Wiegel et al., 1981), was found in temporarily
heated soils (see Drake & Daniel, 2004) and cyanobacterial
mats in hot springs (Bateson et al., 1989). As shown by
BLASTN at the NCBI site (http://www.ncbi.nlm.nih.gov/blast/
Blast.cgi), 16S rRNA genes exhibiting 99% similarity to M.
thermoacetica have been obtained from bioreactors, hot
springs, and oil reservoirs. The diverse metabolic capacities
of this organism make it highly competitive. It grows both
autotrophically and heterotrophically, fermentatively or by
respiration using various electron donors and acceptors
(Drake & Daniel, 2004). In the presence of nitrate, M.
thermoacetica and M. thermoautotrophica can grow on CO
if O-methyl groups (of vanillate or syringate) are provided.
In these organisms, CO2 reduction both to THF-CH3 and to
CO is blocked by nitrate (Drake & Daniel, 2004).
Hydrogenogenic CO-oxidizing
thermophilic anaerobes
Hydrogenogenic CO-oxidizing prokaryotes are capable of
lithotrophic metabolism based on the reaction CO1
H2O ! CO21H2 (DG0 0 = 20 kJ mol1 CO) (carboxydotrophic hydrogenogenesis, Svetlitchnyi et al., 2001). All
thermophilic hydrogenogenic CO oxidizers isolated so far
are obligate anaerobes.
Hydrogenogenic carboxydotrophic thermophiles were
first found in freshwater and coastal marine hydrothermal
vents of Kuril Islands (Svetlichny et al., 1991b). Since then,
15 species of such organisms belonging to Firmicutes,
Dictyoglomi, Euryarchaeota, and Crenarchaeota have been
found in various hot environments (Tables 2 and 3).
Hyperthermophilic representatives of hydrogenogens belong to the Archaea. Most of hydrogenogenic carboxydotrophs are neutrophiles; only Thermincola carboxydiphila is
alkalitolerant. Most of them grow rapidly at 100% CO in the
gas phase, except for the recently isolated ‘Dictyoglomus
carboxydivorans’ and ‘Thermofilum carboxyditrophus’, able
to grow at CO concentrations not higher than 15% and
45%, respectively (Slepova et al., 2007b). However, the levels
Table 2. Isolation sources of thermophilic CO-oxidizing hydrogenogenic prokaryotes
Organism
Isolates from terrestrial hot springs
Carboxydothermus
hydrogenoformans
Carboxydothermus siderophilus
Thermincola carboxydiphila
Thermincola ferriacetica
Carboxydocella
thermautotrophica
Carboxydocella sporoproducens
Location of isolation source
Sample description
Kunashir Island, Kurils
Mud from hot swamp
Geyser Valley, Kamchatka
Bolshaya river, Baikal region
Kunashir Island, Kurils
Geyser Valley, Kamchatka
Pink filaments
Mud and cyanobacterial mat
Water and ochre deposits
Cyanobacterial mat and mud
72/8.4
51–72/6.8–9.5
65/6.8–7.0
60/8.6
Cyanobacterial mat and mud
60/6.6
Slepova et al. (2006)
Core sample and clay
Mud and water
55/5.8
50/7.5
T.G. Sokolova, unpublished data
Sokolova et al. (2004a)
Water and sediment
Water and sediment
97/6.0
80/7.2
T.G. Sokolova, unpublished data
Sokolova et al. (2007)
Water and mud
Water and mud
80/6.5
90/6.5
Slepova et al. (2007b)
Slepova et al. (2007b)
Karymsky volcano,
Kamchatka
‘Carboxydocella ferrireducens’ Uzon Caldera, Kamchatka
Thermosinus carboxydivorans
Norris Basin, Yellowstone
National Park
Caldanaerobacter strain 2707
Kunashir Island, Kurils
Thermolithobacter
Raoul Island (Archipelago
carboxydivorans
Kermadeck)
‘Dictyoglomus carboxydivorans’ Uzon Caldera, Kamchatka
‘Thermofilum carboxyditrophus’ Uzon Caldera, Kamchatka
Isolates from deep-sea hot vents
Caldanaerobacter subterraneus Okinawa Trough
ssp. pacificus
Thermococcus AM4
East Pacific Rise
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Sampling site
temperature
(1C)/pH
68/5.5
Mud
ND
Active chimney colonized by
Alvinella
ND
References
Svetlichny et al. (1991a)
Slepova et al. (2009)
Sokolova et al. (2005)
Zavarzina et al. (2007)
Sokolova et al. (2002)
Sokolova et al. (2001), Fardeau
et al. (2004)
Sokolova et al. (2004b)
FEMS Microbiol Ecol 68 (2009) 131–141
135
Thermophilic carboxydotrophic anaerobes
Table 3. Thermophilic hydrogenogenic CO-oxidizing prokaryotes
Organism
CO-trophy
Bacteria; Firmicutes; Clostridia
Clostridiales; Peptococcaceae
Carboxydothermus
Facultative
hydrogenoformans
Carboxydothermus
Facultative
siderophilus
Thermincola carboxydiphila Obligate
Thermincola ferriacetica
Facultative
Acceptors
Optimal
temperature
Acceptors
( 1C)/
during
optimal Minimal
growth
pH of doubling
on CO
growth time (h) References
1/1
2
AQDS, S0, SO2
3 , S2O3 ,
fumarate, nitrate
AQDS,
fumarate
/
Fe(III), AQDS
Autotrophy/
fermentation
/
/
Desulfotomaculum
Facultative
1/ carboxydivorans
Clostridiales; Syntrophomonadaceae
Carboxydocella
Obligate
1/ thermautotrophica
Carboxydocella
Facultative
1/1
sporoproducens
‘Carboxydocella
Facultative
/1
ferrireducens’
Clostridiales; Veillonellaceae
Thermosinus
Facultative
/1
carboxydivorans
Thermoanaerobacteriales; Thermoanaerobacteriaceae
Caldanaerobacter
Facultative
/1
subterraneus ssp. pacificus
Caldanaerobacter strain
Facultative
/1
2707
Bacteria; Firmicutes; Thermolithobacteria
Thermolithobacterales; Thermolithobacteraceae
Thermolithobacter
Facultative
1/1
carboxydivorans
Bacteria; Dictyoglomi; Dictyoglomi (class)
Dictyoglomales; Dictyoglomaceae
‘Dictyoglomus
ND
/ND
carboxydivorans’
Archaea; Euryarchaeota; Thermococci
Thermococcales; Thermococcaceae
Thermococcus AM4
Facultative
/
Archaea; Crenarchaeota; Thermoprotei
Thermoproteales; Thermofilaceae
‘Thermofilum
Facultative
/ND
carboxyditrophus’
Fe(III),
AQDS
–
–
Fe(III) oxide, AQDS, MnO2, ND
S2O23
2
2
SO2
SO2
4 , SO3 , S2O3
4
70–72/7.0 2
70/7.0
9.0
55/8.0 1.3
57–60/ 1.5
7.0–7.1
55/6.8–7.2
Svetlichny et al.
(1991a), Henstra &
Stams (2004)
Slepova et al. (2009)
Sokolova et al. (2005)
Zavarzina et al. (2007)
Parshina et al. (2005b)
–
–
58/7.0
1.1
Sokolova et al. (2002)
–
–
60/6.8
1.0
Slepova et al. (2006)
Fe(III), AQDS
Fe(III)
60/6.8
1.0
T.G. Sokolova,
unpublished data
2
Fe(III), SeO2
3 S2 O 3
Fe(III),
SeO23
60/6.8–7.0 1.5
Sokolova et al. (2004a)
S2O2
3
–
70/6.8–7.1 7.1
S2O2
3
–
Sokolova et al. (2001),
Fardeau et al. (2004)
T.G. Sokolova,
unpublished data
–
–
ND
ND
75/ND
ND
Slepova et al. (2007b)
S0
S0
85/7.0
3.1
Sokolova et al. (2004b)
ND
ND
92/ND
ND
Slepova et al. (2007b)
75/7.0
3.2
70/6.8–7.0 8.3
Sokolova et al. (2007)
The hierarchical classification is according to the J.P. Euzéby’s site http://www.bacterio.cict.fr/classification.html.
H was an intermediate during the growth of Desulfotomaculum carboxydivorans on CO with SO2.
2
4
of CO in natural hot environments are much lower.
Microorganisms growing on CO in such environments
are likely able to use very low CO concentrations. For
example, Carboxydothermus hydrogenoformans consumed
CO to below detectable levels of 2 p.p.m., when the
FEMS Microbiol Ecol 68 (2009) 131–141
CO2 concentration was kept low (A.M. Henstra et al.,
unpublished data).
Only two species, Carboxydocella thermautotrophica and
T. carboxydiphila, are obligate carboxydotrophs. In contrast
to C. thermautotrophica, T. carboxydiphila does not grow
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136
autotrophically; it requires acetate as a carbon source
(Sokolova et al., 2002, 2005). Some organisms are unable to
reduce exogenous electron acceptors (Table 3). Several
hydrogenogens reduce Fe(III) during growth on CO; H2
remains, however, the predominant reduced product (Sokolova et al., 2005; Slepova et al., 2009). The recently
isolated Carboxydothermus siderophilus can grow on CO
and other substrates only if Fe(III) or anthraquinone-2,6disulfonate (AQDS) are provided. Desulfotomaculum carboxydivorans produces hydrogen sulfide when grown on CO
with sulfate; without sulfate, H2 is the only reduced product
(Parshina et al., 2005b). More than half of the hydrogenogenic CO-oxidizing thermophiles can grow fermentatively
on a limited range of substrates (Table 3).
From the thermophilic hydrogenogenic carboxydotroph
C. hydrogenoformans and the mesophile Rhodospirillum
rubrum, also capable of this process, CODH–ECH enzyme
complexes were isolated and characterized (Fox et al., 1996;
Soboh et al., 2002). Their remarkable similarity was noted,
as well as the remarkable similarity of the so-called coo gene
clusters encoding them (Soboh et al., 2002). They include a
CODH gene (cooS), a ferredoxin-like protein gene (cooF),
genes of a six-subunit ECH, and genes encoding accessory
proteins.
With the aim to search for the coo gene cluster in
phylogenetically diverse thermophilic hydrogenogenic carboxydotrophs, primers were designed proceeding from the
consensus sequence of the CODH genes of R. rubrum (cooS)
and C. hydrogenoformans (cooS-I) and from the consensus
sequence of the ECH gene cooH of these two organisms.
With the use of these primers, the presence of rather closely
related genes and their localization within a single gene
cluster was demonstrated in Thermosinus carboxydivorans,
C. thermautotrophica, T. carboxydiphila, Thermolithobacter
carboxydivorans, and Desulfotomaculum carboxydivorans
(Lebedinsky et al., 2005).
Thus, it was demonstrated that the coo enzyme complex,
encoded by the coo gene cluster, plays a key role in hydrogenogenic carboxydotrophy in phylogenetically diverse bacteria. On the other hand, the coo gene cluster is specific to
hydrogenogenic carboxydotrophs. Our above-discussed
analysis of 988 microbial genomes revealed just a single case
of ambiguous occurrence of a coo-type gene cluster in an
organism (Rhodopseudomonas palustris BisB18) whose ability to grow on CO has not been tested. In organisms in
which the CODH–ECH interplay results in the reverse
reaction, i.e. CO2 reduction by H2 to CO [this ECH
function, proven for at least Methanosarcina barkeri (Meuer
et al., 2002), is probably widespread], the CODH and ECH
genes do not cluster. Thus, the primers specific for the coo
gene cluster may be an informative tool for molecular
ecological studies, a positive PCR indicating the presence of
hydrogenogenic carboxydotrophs. Moreover, the presence
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T.G. Sokolova et al.
of a CODH–ECH gene cluster can be used as a marker for
hydrogenogenic carboxydotrophy while interpreting genomics and metagenomics data. This conclusion is supported
by the examination of the recently shotgun-sequenced genomes of Thermococcus sp. AM4 and Caldanaerobacter subterraneus ssp. pacificus. Both these genomes contain a CODH
gene clustered with ECH genes (A.V. Lebedinsky, J.M.
Gonzalez, & T.G. Sokolova, unpublished data), although
these gene clusters considerably differ from the coo gene
cluster in terms of the gene primary structure and order.
According to our analysis, CODH–ECH gene clusters of the
new type, as the ‘classical’ coo gene clusters, also do not occur
in organisms other than hydrogenogenic carboxydotrophs.
An exception is the CODH–ECH gene cluster that we found
in the genome of C. subterraneus ssp. tengcongensis, an
organism not tested for the ability to grow on CO (Table 1).
All known hydrogenogenic CO-oxidizing thermophiles,
except Desulfotomaculum carboxydivorans, an isolate from
bioreactor sludge, were isolated from geographically distant
natural hot environments with pH values from 5.5 to 10.0
and temperatures from 50 to 90 1C (Table 2). A close relative
of Desulfotomaculum carboxydivorans, Desulfotomaculum sp.
RL50JIII (99.9% 16S rRNA gene similarity), was isolated
from a geothermal underground mine in Japan (Kaksonen
et al., 2006); its ability to grow on CO was not examined.
Data on the distribution of individual species of hydrogenogenic CO-oxidizing thermophiles are limited. Carboxydocella species are widespread in Kamchatkan hot springs
with temperatures of 50–70 1C and pH from 5.5 to 8.6
(Sokolova et al., 2002; Slepova et al., 2006, 2007b). Only one
environmental rRNA gene clone related to Carboxydocella is
currently available in public databases; the sequence of clone
TOYO-6C is 99% similar to the 16S rRNA gene of Carboxydothermus ferrireducens. Clone TOYO-6C was obtained
from a Cu–Pb–Zn mine (48 1C, pH 6.8) in Japan (Nakagawa
et al., 2002). Thermincola species have been found in
terrestrial hot springs, but they also occur in other habitats.
16S rRNA genes with high similarity to Thermincola have
been detected in oil reservoirs by Liew and Jong (GenBank
accession EF095439), enrichments from a geothermally
active mine in Japan (Kaksonen et al., 2006), and biofilms
formed by electricity-generating communities enriched
from marine sediments (Mathis et al., 2007). rRNA phylotypes with 100% 16S rRNA gene sequence identity to ‘T.
carboxyditrophus’ are abundant in the Yellowstone National
Park hot springs.
Thirteen enrichments of coccoid cells growing on CO
with H2 and CO2 production at 80 1C were obtained from
24 samples of hydrothermal venting structures collected at
East Pacific Rise 131N (Sokolova et al., 2004b), and six such
enrichments, from 10 chimney samples collected at MidAtlantic Ridge (Ashadze and Logachev thermal fields). One
of the East Pacific Rise enrichments was the source of
FEMS Microbiol Ecol 68 (2009) 131–141
137
Thermophilic carboxydotrophic anaerobes
isolation of Thermococcus AM4. From the Mid-Atlantic
Ridge enrichments, four pure cultures of hydrogenogenic
carboxydotrophs were isolated, with 16S rRNA genes similar
to that of Thermococcus barophilus (T.G. Sokolova, A.V.
Lebedinsky, & J. Querellou, unpublished data). Thus, it
may be inferred that hydrogenogenic carboxydotrophic
hyperthermophiles, particularly phylogenetically diverse
thermococci capable of this process, may be abundant
members of the microbial communities inhabiting deepsea hot vents.
CO oxidation by dissimilatory Fe(III)reducing thermophiles
Carboxydothermus ferrireducens (Slobodkin et al., 2006),
formerly Thermoterrabacterium ferrireducens, is a moderately thermophilic, anaerobic, dissimilatory Fe(III)-reducing bacterium isolated from a hot spring in Yellowstone
National Park (Slobodkin et al., 1997). This organism can
grow by utilizing organic substrates or H2 as electron
donors, and, apart from Fe(III) or AQDS, it can also reduce
sulfite, thiosulfate, elemental sulfur, nitrate, and fumarate
(Slobodkin et al., 1997; Henstra & Stams, 2004). Carboxydothermus ferrireducens grows on CO without hydrogen
or acetate production with ferrihydrite as the electron
acceptor, forming magnetite precipitate (Slobodkin et al.,
2006), or with AQDS or fumarate as electron acceptors
(Henstra & Stams, 2004). Unlike C. hydrogenoformans, this
bacterium cannot grow on CO without electron acceptors.
CO-utilizing sulfate-reducing bacteria and
archaea
The ability of some sulfate-reducing bacteria to oxidize CO
at low concentrations (4–20%) is long known (Yagi, 1959;
Davidova et al., 1994). The moderately thermophilic species
Desulfotomaculum nigrificans grows with low concentrations
of CO; 20% CO inhibited growth completely (Klemps et al.,
1985; Parshina et al., 2005b) (Table 4). Strain RHT-3 (Mori
et al., 2000) can grow at up to 50% CO (Parshina et al.,
2005b). CO conversion by four thermophilic sulfate-reducing bacteria, Desulfotomaculum thermoacetoxidans CAMZ
(DSM 5813) (Min & Zinder, 1990), Thermodesulfovibrio
yellowstonii ATCC 51303 (Henry et al., 1994), Desulfotomaculum kuznetsovii DSM 6115 (Nazina et al., 1988, 1999), and
Desulfotomaculum thermobenzoicum ssp. thermosyntrophicum DSM 14055 (Plugge et al., 2002), was studied in pure
cultures (Table 4) and cocultures with the thermophilic
hydrogenogenic carboxydotrophic bacterium C. hydrogenoformans (Parshina et al., 2005a). Desulfotomaculum thermoacetoxidans and T. yellowstonii were extremely sensitive to
CO; their growth on pyruvate was arrested at CO concentrations above 2% in the gas phase. In contrast, D. kuznetsovii and D. thermobenzoicum ssp. thermosyntrophicum could
grow under 50–70% CO. These two bacteria coupled CO
oxidation to sulfate reduction, but a large proportion of CO
was converted to acetate. In a coculture with C. hydrogenoformans, D. kuznetsovii and D. thermobenzoicum ssp. thermosyntrophicum could grow under 100% CO, most
probably using hydrogen formed by C. hydrogenoformans as
the electron donor for sulfate reduction (Parshina et al.,
2005a). Desulfotomaculum carboxydivorans (Parshina et al.,
2005b), which grows as a hydrogenogenic carboxydotroph
in the absence of sulfate, was discussed above.
Recently, it was shown that the anaerobic extremely
thermophilic euryarchaeote Archaeoglobus fulgidus VC-16 is
capable of autotrophic growth with CO. Oxidation of CO to
CO2 was coupled to sulfate reduction; acetate and formate
were formed as minor products. In the absence of sulfate,
the only products of CO metabolism are acetate, formed via
the reductive acetyl-CoA pathway with formyl-methanofuran as an intermediate, and formate (Henstra et al., 2007).
Archaeoglobus fulgidus can also completely oxidize various
organic compounds in the presence of sulfate or grow
Table 4. Sulfate-reducing bacteria utilizing CO as the sole energy and carbon source
Organism
Source of isolation
Desulfotomaculum nigrificans DSM
574
D. thermobenzoicum ssp.
thermosyntrophicum DSM 14055
D. kuznetsovii DSM 6115
Sewage mud, soil
55
20
Anaerobic sludge
55
50–70 Acetate, H2S, CO2
Desulfotomaculum sp. RHT-3
D. carboxydivorans CO-1-SRB
Archaeoglobus fulgidus VC 16
FEMS Microbiol Ecol 68 (2009) 131–141
CO
(%)
Products formed
T
( 1C)
With sulfate
Without sulfate
H2S, CO2
No growth
Underground thermal 55–60 50
mineral water
Sea-based landfill site 55
50
Acetate, H2S, H2S, CO2
H2S, CO2
Anaerobic sludge
55
100
Submarine hot spring; 75–80 80
Italy, Vulcano island
H2S (via H2), CO2
CO2, acetate, H2S,
formate (transient)
References
Klemps et al. (1985),
Parshina et al. (2005a)
No growth
Plugge et al. (2002),
Parshina et al. (2005a)
No growth
Nazina et al. (1988),
Parshina et al. (2005a)
No growth
Mori et al. (2000),
Parshina et al. (2005a)
H2, CO2
Parshina et al. (2005b)
CO2, acetate,
Stetter et al. (1987),
formate (transient) Henstra et al. (2007)
2009 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
c
138
chemolithoautotrophically on H2 with thiosulfate, but not
with sulfate as the electron acceptor (Zellner et al., 1989).
Archaeoglobus species occur in both shallow and abyssal
marine hydrothermal systems (Burggraf et al., 1990). Archaeoglobus fulgidus VC16 was isolated from submarine
solfataric fields near Vulcano Island, Italy (Stetter et al.,
1987). Archaeoglobus fulgidus strains were also isolated from
hot oil field waters (Stetter et al., 1993; Beeder et al., 1994).
Conclusion
CO biotransformation in hot anaerobic environments occurs and provides a niche for diverse CO-oxidizing prokaryotes. Genomic analysis shows that many anaerobes contain
multiple CODH genes and are thus apparently adapted to
take advantage of exogenous CO. Further microbiological,
molecular ecological, and genomic research will undoubtedly reveal still greater diversity of CO-oxidizing anaerobes.
A significant role in CO transformation in thermal environments is likely to be played by hydrogenogenic CO oxidizers.
Acknowledgements
This work was supported by the program of Presidium of
the Russian Academy of Sciences ‘Molecular and Cell
Biology’, the Technology Foundation STW, the applied
science division of NWO, the Netherlands, Shell Global
Solutions (Amsterdam, the Netherlands), and Paques B.V.
(Balk, the Netherlands).
Note added in proof
Quite recently, the range of thermococci capable of hydrogenogenic growth on CO has ben extended. Presence of this
capacity has been successfully tested, proceeding from the
results of genomic analyses, in two originally organotrophic
isolates, T. onnurineus (Lee et al., 2008) and T. barophilus
(A.V. Lebedinsky and T.G. Sokolova, unpublished data).
Both genomes contain CODH–ECH gene clusters very
similar to that present in the genome of Thermococcus AMY.
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