International Journal of Systematic and Evolutionary Microbiology (2012), 62, 2463–2468
DOI 10.1099/ijs.0.038372-0
Deferrisoma camini gen. nov., sp. nov., a
moderately thermophilic, dissimilatory
iron(III)-reducing bacterium from a deep-sea
hydrothermal vent that forms a distinct phylogenetic
branch in the Deltaproteobacteria
G. B. Slobodkina,1 A.-L. Reysenbach,2 A. N. Panteleeva,3 N. A. Kostrikina,1
I. D. Wagner,2 E. A. Bonch-Osmolovskaya1 and A. I. Slobodkin1
1
Correspondence
Winogradsky Institute of Microbiology, Russian Academy of Sciences, Prospect 60-letiya,
Oktyabrya 7/2, 117312 Moscow, Russia
G. B. Slobodkina
[email protected]
2
Department of Biology and Center for Life in Extreme Environments, Portland State University,
PO Box 751, Portland, OR 97207-0751, USA
3
Bioengineering Center, Russian Academy of Sciences, Prospect 60-letiya Oktyabrya 7/1,
117312 Moscow, Russia
A moderately thermophilic, anaerobic, dissimilatory iron(III)-reducing bacterium (strain S3R1T)
was isolated from a deep-sea hydrothermal vent chimney located on the Eastern Lau Spreading
Centre in the Pacific Ocean at a depth of about 2150 m. Cells of strain S3R1T were ovals to short
rods with a single polar flagellum, Gram-stain-negative, 0.5–0.6 mm in diameter and 0.8–1.3 mm
long, growing singly or in pairs. The temperature range for growth was 36–62 6C, with an
optimum at 50 6C. The pH range for growth was 5.5–7.5, with an optimum at pH 6.5. Growth of
strain S3R1T was observed at NaCl concentrations ranging from 1.0 to 5.0 % (w/v), with an
optimum at 2.0–2.5 % (w/v). The isolate used acetate, fumarate, malate, maleinate, succinate,
propanol, palmitate, stearate, peptone and yeast extract as electron donors for growth and iron(III)
reduction. All electron donors were oxidized completely to CO2 and H2O. Iron(III) (in the form of
ferrihydrite, ferric citrate or ferric nitrilotriacetate) and elemental sulfur (S0) were the electron
acceptors that supported growth. The DNA G+C content was 64.4 mol%. Results of 16S rRNA
gene sequence analysis showed that the novel bacterium was related to representatives of the
orders Desulfuromonadales and Syntrophobacterales with 84–86 % sequence similarity and
formed a distinct phylogenetic branch in the Deltaproteobacteria. On the basis of its physiological
properties and results of phylogenetic analyses, it is proposed that the new isolate represents the
sole species of a novel genus, Deferrisoma camini gen. nov., sp. nov. The type strain of
Deferrisoma camini is S3R1T (5DSM 24185T 5VKM B-2672T).
Dissimilatory iron(III)-reducing micro-organisms play an
important role in the cycling of carbon and metals in various
ecosystems including thermal environments (Lovley et al.,
2004; Slobodkin, 2005). Deep-sea hydrothermal vents are rich
in iron minerals and provide an ecological niche for iron(III)reducing micro-organisms (Slobodkin et al., 2001). Several
thermophilic and hyperthermophilic iron-reducers of different taxonomic affiliation have been recovered from this
extreme habitat. Iron(III)-reducing archaea include members
Abbreviation: NTA, nitrilotriacetate.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene
sequence of strain S3R1T is JF802205.
A supplementary table is available with the online version of this paper.
038372 G 2012 IUMS
of the phyla Euryarchaeota and Crenarchaeota (Slobodkin
et al., 2001; Kashefi et al., 2002; Reysenbach et al., 2006;
Slobodkina et al., 2009b; Ver Eecke et al., 2009). The three
species of thermophilic, dissimilatory iron-reducing bacteria
isolated to date from deep-sea hydrothermal vents are two
members of the phylum ‘Deferribacteres’, Deferribacter abyssi
(Miroshnichenko et al., 2003) and Deferribacter autotrophicus
(Slobodkina et al., 2009a), and the deltaproteobacterium
Geothermobacter ehrlichii (Kashefi et al., 2003). Here, we
report the isolation and characterization of a novel moderately
thermophilic, dissimilatory iron(III)-reducing bacterium from
a deep-sea hydrothermal vent on the Eastern Lau Spreading
Centre in the Pacific Ocean that forms a well-separated phylogenetic branch in the class Deltaproteobacteria.
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G. B. Slobodkina and others
Strain S3R1T was isolated from a sample of an actively
venting hydrothermal chimney-like sulfide mineral deposit.
The sample was collected in June 2009 from the ABE
hydrothermal field (20u 45.89 S 176u 11.59 W; 2104–2163 m
depth) on the Eastern Lau Spreading Centre in the southwestern Pacific Ocean using the ROV JASON II. Once
collected, the samples were placed in an insulated box on the
submersible’s basket. Upon reaching the ship, the samples
were sectioned immediately and small fragments were used
as the inoculum. An enrichment culture was initiated by
inoculation of 10 % (w/v) of the sample into anaerobically
prepared, bicarbonate-buffered, sterile liquid medium supplemented with yeast extract (0.2 g l21) as a potential
electron donor and insoluble, poorly crystalline iron(III)
oxide [ferrihydrite; 90 mmol Fe(III) l21] as a potential
electron acceptor. The medium contained (g l21 distilled
water): KH2PO4, 0.33; NH4Cl, 0.33; KCl, 0.33; CaCl2 . 6H2O,
0.33; MgCl2 . 6H2O, 4; NaCl, 18; NaHCO3, 2. A vitamin
solution (10 ml l21; Wolin et al., 1963) and trace element
solution [1 ml l21, with the following composition (mmol
l21): (NH4)2SO4 . FeSO4 . 6H2O, 2.0; CoCl2 . 6H2O, 1.0;
NiCl2 . 2H2O, 1.0; Na2MoO4 . 2H2O, 0.1; Na2WO4 . 2H2O,
0.1; ZnSO4 . 7H2O, 0.5; CuCl2 . 2H2O, 0.01; Na2SeO4, 0.5;
H3BO3, 0.1; MnCl2 . 4H2O, 1.0; SrSO4, 0.05; CrO3, 0.01;
AlCl3 . 6H2O, 0.1; BaCl2, 0.1; Na2SiO3 . 9H2O, 0.5; KBr, 1.0;
KI, 1.0; Na2SO4, 5.0] were added. No reducing agents were
added to the medium. The pH of the medium was 6.5–6.8
(measured at 25 uC). Medium (10 ml) was dispensed in
17 ml Hungate tubes and the headspace was filled with CO2
(100 %). After incubation of the enrichments at 50 uC for
9 days, the colour of the ferrihydrite changed from brown to
black, indicating iron(III) reduction. After three subsequent
transfers and following serial 10-fold dilutions in the same
medium, only one morphological type was observed in
the highest dilution (1027) positive for iron(III) reduction.
Attempts to obtain separate colonies at 50 uC in agar blocks
or by the roll-tube method with 1 % agar as solidifying agent
in the medium with or without ferrihydrite or ferric citrate
(10 mM) were unsuccessful. A pure culture of strain S3R1T
was obtained by means of multiple serial dilutions in the
same medium.
Determination of temperature, pH and salinity ranges
for growth, light and electron microscopy, physiological
studies on substrate utilization, Fe(II) analysis, DNA
extraction and determination of DNA G+C content were
performed as described previously (Slobodkin et al., 1999).
Sulfide was measured colorimetrically with dimethyl pphenylenediamine (Trüper & Schlegel, 1964). Cellular fatty
acid (CFA) profiles were determined by GC-MS as methyl
ester derivatives prepared from 5 mg dry cell material
(Sasser, 1990). CFA content was determined as the
percentage of total ion current peak area. The 16S rRNA
gene was selectively amplified from genomic DNA by PCR
using primers 27F and 1492R (Lane, 1991). The PCR was
carried out in a 50 ml reaction mixture containing 50 ng
DNA template, 5 pmol each primer, 12.5 nmol each dNTP
and 3 U Taq DNA polymerase (Fermentas) in Taq DNA
2464
polymerase reaction buffer (Fermentas). Temperature cycling was done by using the following program: a first cycle
of 9 min at 94 uC, 1 min at 55 uC and 2 min at 72 uC and
then 30 amplification cycles of 1 min at 94 uC, 1 min at
55 uC and 1 min at 72 uC. The final extension was carried
out at 72 uC for 7 min. PCR products were purified using
the Wizard PCR Preps kit (Promega) as recommended by
the manufacturer. Both strands of the 16S rRNA gene were
sequenced using Big Dye Terminator version 3.1 (Applied
Biosystems) as described in the manufacturer’s instructions
and resolved using an ABI PRISM 3730 DNA Analyzer
(Applied Biosystems). A multiple sequence alignment was
generated using the NAST alignment tool (DeSantis et al.,
2006a) and the Greengenes database (DeSantis et al., 2006b;
http://greengenes.lbl.gov/cgi-bin/nph-index.cgi). The alignment generated was then checked manually (Hall, 1999)
and only unambiguously aligned positions were used (total
1100 nt). Evolutionary analyses were conducted in MEGA
version 5 (Tamura et al., 2011). The phylogenetic tree was
inferred using maximum-likelihood analysis. Pairwise
similarity values were calculated by means of EzTaxon
(Chun et al., 2007).
Cells of strain S3R1T were ovals or short rods, 0.5–0.6 mm
in diameter and 0.8–1.3 mm long, growing singly or in
pairs. Cells were highly motile due to a single polar
flagellum (Fig. 1a). Formation of endospores was not
observed. Ultrathin sections of cells of strain S3R1T
revealed a Gram-negative cell-wall type (Fig. 1b). The
temperature range for growth was 36–62 uC, with an
optimum at 50 uC. No growth was detected at 30 or 65 uC
after incubation for 2 weeks. The pH range for growth was
5.5–7.5, with an optimum at pH 6.5. No growth was
detected at pH 5.0 or 8.0. Growth of strain S3R1T was
observed at NaCl concentrations ranging from 1.0 to 5.0 %
(w/v) with an optimum at 2.0–2.5 % (w/v) NaCl; no
growth was evident at or below 0.7 % (w/v) NaCl or at or
above 5.5 % (w/v) NaCl. Strain S3R1T reduced ferrihydrite
to a black precipitate containing 25–30 mM iron(II). No
changes in colour or amount of precipitate were observed
in uninoculated controls with ferrihydrite during the
incubation period at 50 uC. In addition to the insoluble
form of iron(III), strain S3R1T used soluble forms of
iron(III), ferric citrate and ferric nitrilotriacetate [Fe(III)
NTA], but not ferric EDTA or ferric pyrophosphate
(10 mM each). The highest cell density (8–126107 cells
ml21) was observed when ferric citrate was used as the
electron acceptor, compared with either Fe(III) NTA or
ferrihydrite (1–26107 cells ml21). The doubling time with
ferric citrate was 2.6 h and with Fe(III) NTA and
ferrihydrite it was 7.3 h. Potential electron donors were
tested in the medium with either ferric citrate or
ferrihydrite in the absence of yeast extract. The isolate
used acetate, fumarate, malate, maleinate, succinate,
propanol (10 mM each), palmitate, stearate (1 mM each),
peptone and yeast extract (0.2 and 1.0 g l21 each) as
electron donors for growth and iron(III) reduction. All
electron donors utilized were oxidized completely to CO2
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Deferrisoma camini gen. nov., sp. nov.
Fig. 1. Cell morphology of strain S3R1T. (a) Electron micrograph
showing overall morphology of a cell and localization of the single
flagellum. Bar, 0.5 mm. (b) Ultrathin section showing cell-wall
structure. Bar, 0.1 mm.
or ferrihydrite as an electron acceptor. The strain did not
ferment glucose, fructose, maltose, sucrose, cellobiose,
arabinose (15 mM each), citrate or malate (10 mM each).
In addition to iron(III), strain S3R1T used elemental sulfur
(S0; 10 g l21) as an electron acceptor, reducing it to sulfide
with fumarate (10 mM) and yeast extract (0.2 g l21) as electron donors. However, growth with S0 did not exceed 5–
86106 cells ml21 and sulfide formation did not exceed
1 mM. H2/CO2 (80 : 20, v/v) did not support growth of
S3R1T with S0 as an electron acceptor. Strain S3R1T did not
reduce Mn(IV) (25 mM), sulfite (5 mM), sulfate, thiosulfate, nitrate, fumarate, 9,10-anthraquinone 2,6-disulfonate
(10 mM each) or oxygen (2.0 or 20 % in the gas phase)
with fumarate (10 mM), yeast extract (0.2 g l21) or H2/
CO2 (80 : 20, v/v) as electron donors. Growth of strain
S3R1T was inhibited by penicillin, ampicillin, novobiocin,
chloramphenicol (100 mg ml21 each). Kanamycin and neomycin (100 mg ml21 each) did not inhibit growth. The
major CFAs were iso-C17 : 0, iso-C15 : 0 and iso-C17 : 1v8 (34.0,
19.2, 17.2 % of total CFA, respectively); cC18 : 3 (9.7 %) and
branched C18 : 0 (8.2 %) were also present. Other fatty acids
were present in small or trace amounts (less than 5 % of total
fatty acid content; Table S1, available in IJSEM Online).
and H2O; formation of organic acids or alcohols was
not detected. Strain S3R1T was not able to utilize lactate,
pyruvate, tartrate, oxalate, formate, propionate, butyrate,
glycerol, methanol, ethanol, isopropanol, butanol, tryptone
(0.2 or 1.0 g l21) or H2/CO2 (80 : 20, v/v) with ferric citrate
The G+C content of the genomic DNA of strain S3R1T was
64.4 mol%. Analysis of the partial 16S rRNA gene sequence
of strain S3R1T (1481 bp) revealed that it belonged to the
class Deltaproteobacteria (Fig. 2), with the closest relatives
being the type strains of Desulfuromonas palmitatis (86.43 %
similarity) and Desulfoglaeba alkanexedens (86.39 %)
(Coates et al., 1995; Davidova et al., 2006).
Sulfate-reducing consortium clone MidBa15 (EF999371)
TCE bioremediation clone WC01 (GQ461655)
Heavy-metal-polluted soil clone G19-236 (GQ487978)
S3R1 clade
Yellow Sea sediment clone C13S-100 (EU617844)
Deferrisoma camini S3R1T (JF802205)
100
71
Sulfate-reducing consortium clone MidBa79 (FJ748774)
Thermodesulforhabdus norvegica A8444T (U25627)
100
Desulfacinum infernum Ba G1T (L27426)
Desulfoglaeba alkanexedens ALDCT (DQ303457)
Desulforhabdus amnigenus ASRB1T (X83274)
99
Desulfovirga adipica TsuA1T (AJ237605)
71
Syntrophobacter wolinii DSM 2805T (X70905)
Syntrophorhabdus aromaticivorans UIT (AB212873)
Desulfobacca acetoxidans ASRB2T (AF002671)
100
72
Smithella propionica LYPT (AF126282)
Syntrophus buswellii DSM 2612T (X85131)
Geobacter metallireducens GS-15 T (L07834)
99
Geoalkalibacter ferrihydriticus Z-0531 T (DQ309326)
Geoalkalibacter subterraneus Red1T (EU182247)
Desulfuromonas palmitatis SDBY1T (DPU28172)
Desulfuromonas acetoxidans strain (AY187305)
Pelobacter carbinolicus DSM 2380T (CP000142)
84
100
Malonomonas rubra Gra Mal 1T (Y17712)
Pelobacter acidigallici Ma Gal 2T (X77216)
Desulfovibrionales
Desulfovibrio desulfuricans ATCC 27774 T (M34113)
0.02
77
Syntrophobacterales
Syntrophobacteraceae
Desulfuromonadales
Syntrophorhabdaceae
Syntrophaceae
94
Fig. 2. Phylogenetic tree of strain S3R1T based on 16S rRNA gene sequences as inferred by maximum-likelihood analysis.
Bootstrap values greater than 50 % are shown. Bar, 0.02 changes per nucleotide position.
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2465
G. B. Slobodkina and others
thiosulfate, and grow at temperatures around 40 uC. The novel
isolate differs from described representatives of the orders
Desulfuromonadales and Syntrophobacterales by its growth
temperature optimum and range of electron acceptors that are
utilized. Strain S3R1T and related environmental clones (89–
93 % sequence similarity) form a very well-defined clade
related to the Syntrophobacterales (Fig. 2). It is evident from
the degree of 16S rRNA gene sequence similarity between
strain S3R1T and any of the reference strains represented in the
sequence databases that this strain represents a novel species
and genus, and might form the basis for a new family.
However, the decision to describe a higher taxon should await
phylogenetic and physiological characterization of additional
members of this novel lineage. On the basis of significant
phylogenetic distance and phenotypic differences from its
closest relatives, we propose to classify strain S3R1T as the type
strain of the type species of a new genus, Deferrisoma camini
gen. nov., sp. nov.
The new isolate is a moderate thermophile that depends
absolutely on iron(III) and S0 reduction. Strain S3R1T grows
only organotrophically, while most iron(III)-reducers that
inhabit deep-sea hydrothermal environments possess the
capacity for lithoautotrophic growth with molecular hydrogen (Kashefi et al., 2002; Slobodkina et al., 2009a, b; Ver
Eecke et al., 2009). Thus, strain S3R1T cannot function as a
primary producer in deep-sea ecosystems but rather participates in the anaerobic oxidation of compounds derived
from organic matter decomposition at zones of ferric iron
deposits. Within a multiplexed barcoded pyrosequencing
dataset of the variable region 4 (V4) of bacterial 16S rRNA
genes from 56 deep-sea hydrothermal vent samples from the
Mid-Atlantic Ridge, Guaymas Basin and the Eastern Lau
Spreading Centre, sequences similar to S3R1 were only
detected at Mariner on the Eastern Lau Spreading Centre
and at TAG on the Mid-Atlantic Ridge (not shown).
The novel strain is almost equally related to representatives of
the orders Desulfuromonadales (84.2–86.4 % sequence similarity) and Syntrophobacterales (85.2–86.4 %). The order
Desulfuromonadales includes moderately thermophilic ironand sulfur-reducers, while the thermophilic representatives of
the order Syntrophobacterales are sulfate-reducers, and dissimilatory iron(III) and S0 reduction has not been demonstrated in this group (Table 1). Strain S3R1T is phenotypically
more similar to the members of the Desulfuromonadales,
Geothermobacter ehrlichii, Geoalkalibacter subterraneus and
Desulfuromonas palmitatis; all these are iron(III)-reducers
incapable of fermentation and reduction of sulfate, sulfite and
Description of Deferrisoma gen. nov.
Deferrisoma (De.fer.ri.so9ma. L. pref. de- from; L. n. ferrum
iron; N.L. pref. deferri- prefix used to characterize dissimilatory iron reduction; Gr. neut. n. soma body; N.L. neut. n.
Deferrisoma iron-reducing body).
Cells are rod-shaped and motile with a single polar
flagellum. Gram-stain-negative. Anaerobic and moderately
thermophilic. Oxidize organic substrates completely with
iron(III) and S0 as electron acceptors. The type species is
Deferrisoma camini.
Table 1. Physiological traits of strain S3R1T and thermophilic and thermotolerant representatives of the orders Desulfuromonadales
and Syntrophobacterales
Strains: 1, strain S3R1T (data from this study); 2, Desulfuromonas palmitatis SDBY1T (data from Coates et al., 1995); 3, Geoalkalibacter subterraneus
Red1T (Greene et al., 2009); 4, Geothermobacter ehrlichii SS015T (Kashefi et al., 2003); 5, Desulfoglaeba alkanexedens ALDCT (Davidova et al., 2006);
6, Thermodesulforhabdus norvegica A8444T (Beeder et al., 1995); 7, Desulfacinum infernum BaG1T (Rees et al., 1995). +, Positive; 2, negative; ND,
no data available.
Desulfuromonadales
Characteristic
1
Source*
DSHV
Growth temperature (uC)
Range
36–60
Optimum
50
DNA G+C content (mol%) 64.4
Electron acceptors
Sulfate
2
+
S0
Thiosulfate
2
Sulfite
2
Nitrate
2
Fe(III)
+
Mn(IV)
2
Syntrophobacterales
2
3
4
5
Marine sediment
Oilfield production water
DSHV
Oily sludge
ND
40
54.7
30–50
40
52.5
35–65
55
62.6
17–50
31–37
53.6
44–74
60
51.0
40–65
60
64.0
2
+
2
2
2
+
+
2
+
2
2
+
+
+
2
2
2
2
+
+
2
+
2
+
2
+
2
2
+
2
+
2
+
+
2
ND
6
7
Oilfield Petroleum reservoir
2
ND
ND
ND
ND
ND
*DSHV, Deep-sea hydrothermal vent.
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Deferrisoma camini gen. nov., sp. nov.
Davidova, I. A., Duncan, K. E., Choi, O. K. & Suflita, J. M. (2006).
Description of Deferrisoma camini sp. nov.
Deferrisoma camini (ca.mi9ni. L. n. caminus a furnace; L.
gen. n. camini from a furnace, referring to the isolation of
the type strain from a hydrothermal chimney).
Displays the following properties in addition to those
described for the genus. Cells are 0.5–0.6 mm in diameter
and 0.8–1.3 mm long. The temperature range for growth is
36–62 uC, with an optimum at 50 uC. The pH range for
growth is 5.5–7.5, with an optimum at pH 6.5. The salinity
range for growth is 1.0–5.0 % (w/v) NaCl, with an
optimum at 2.0–2.5 % (w/v). Utilizes acetate, fumarate,
malate, maleinate, succinate, stearate, palmitate, propanol,
peptone and yeast extract as electron donors for iron(III)
reduction. Lactate, pyruvate, tartrate, oxalate, formate,
propionate, butyrate, glycerol, methanol, ethanol, isopropanol, butanol, tryptone and H2/CO2 are not used as
electron donors. Does not ferment glucose, fructose,
maltose, sucrose, cellobiose, arabinose, citrate or malate.
Iron(III) [in the form of ferrihydrite, ferric citrate or Fe(III)
NTA] and S0 are the electron acceptors that support
growth. Manganese(IV), sulfite, sulfate, thiosulfate, nitrate,
fumarate, 9,10-anthraquinone 2,6-disulfonate and oxygen
are not used as electron acceptors. Sensitive to penicillin,
ampicillin, novobiocin and chloramphenicol and resistant
to kanamycin and neomycin (each at 100 mg ml21). The
DNA G+C content of the type strain is 64.4 mol%. The
dominant cellular fatty acids are iso-C17 : 0, iso-C15 : 0 and
iso-C17 : 1v8.
T
T
T
The type strain is S3R1 (5DSM 24185 5VKM B-2672 ),
isolated from a deep-sea hydrothermal vent along the
Eastern Lau Spreading Centre in the south-western Pacific
Ocean.
Acknowledgements
This work was supported by the Russian Foundation for Basic
Research (grant 09-04-00251-a) and by the Programs ‘Molecular and
Cell Biology’ and ‘The Origin and Evolution of the Biosphere’ of the
Russian Academy of Sciences. We thank the crews of the R/V
Thompson and the DSROV Jason II for their assistance in obtaining
samples. This research was also supported by the United States
National Science Foundation (grants OCE-0728391 and OCE0937404 to A.-L. R.)
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