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1 Subground Animalcule Retrieval (SUGAR) Project, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
2 Department of Earth Sciences, University of Southern California, 3651 Trousdale Pkwy, Los Angeles, CA 90089-0740, USA
Correspondence
Ken Takai
kent{at}jamstec.go.jp
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Published online ahead of print on 6 August 2004 as DOI 10.1099/ijs.0.63330-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Pd55T is AB167820.
An electron micrograph of strain Pd55T (Fig. A) and graphs showing the effects of temperature, pH and NaCl concentration on the growth rate of strain Pd55T (Fig. Ba–c) are available as supplementary material in IJSEM Online.
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; Campbell et al., 2001; Inagaki et al., 2003, 2004; Miroshnichenko et al., 2002, 2004; Takai et al., 2003a, 2004a). Nautilia lithotrophica strain 525T (Miroshnichenko et al., 2002) and Caminibacter hydrogeniphilus strain AM1116T (Alain et al., 2002) are strictly anaerobic, hydrogen-oxidizing, thermophilic chemolithomixotrophs isolated from nests of tube-dwelling polychaetes of deep-sea hydrothermal systems in the East Pacific Rise (EPR). Other isolates (strains Am-H and EX-18.2) from similar habitats have been reported as slightly thermophilic, anaerobic mixotrophs capable of using hydrogen as an energy source and elemental sulfur as a primary electron acceptor (Campbell et al., 2001). Together with a further isolate, Caminibacter profundus strain CRT, from the Rainbow site in the Mid-Atlantic Ridge (MAR) (Miroshnichenko et al., 2004), a second order within the class ‘Epsilonproteobacteria’, in addition to the order ‘Campylobacterales’, has been proposed – the Nautiliales (Miroshnichenko et al., 2004). However, classification of ‘Epsilonproteobacteria’ at the order level is still unresolved since the previous phylogenetic analysis, justifying the paraphyletic lineages between ‘Campylobacterales’ and Nautiliales, did not include all the recently isolated subgroups of ‘Epsilonproteobacteria’ such as Group A (e.g. Hydrogenimonas thermophila strain EP1-55-1%T and others; Takai et al., 2003a, 2004a), Group F (e.g. Sulfurovum lithotrophicum strain 42BKTT and others; Inagaki et al., 2004; Takai et al., 2003a) and Group G (e.g. strain BKB25Ts-Y; Takai et al., 2003a). These strains are aerobic to anaerobic, hydrogen- and/or sulfur-oxidizing, strict chemolithoautotrophs representing a variety of microhabitats in deep-sea hydrothermal systems. As these isolates and the numerous uncultivated rRNA gene clones were not included in this recent analysis, phylogenetic organization of the ‘Epsilonproteobacteria’ is still uncertain. In addition, the taxonomic criteria of the orders Nautiliales and ‘Campylobacterales’ are unclear with respect to their coverage of the newly described genera and the numerous uncultivated phylotypes (Takai et al., 2003a, 2004b). Probably, the confident taxonomy and systematics of ‘Epsilonproteobacteria’ require further exploration of as-yet-uncultivated members and their phylogenetic and physiological traits in naturally occurring microbial habitats, specifically in the deep-sea hydrothermal and cold seeping environments, and subsurface biota. In this study, a novel thermophilic, acidophilic bacterium was isolated from a self-temperature-recording in situ colonization system (STR-ISCS) deployed in a hydrothermal diffusing flow (maximum temperature of 78 °C) at the TOTO caldera in the Mariana Arc. Taxonomic characterization of this isolate, strain Pd55T, is described and a new genus and novel species, Lebetimonas acidiphila gen. nov., sp. nov., are proposed.
The STR-ISCS, a microbial habitat consisting of a stainless steel pipe with many small holes (5 mm diameter) and substratum of very porous natural pumice (Takai et al., 2003a), was deployed for 4 days in a diffusing hydrothermal flow with a maximum fluid temperature of 78 °C and a pH of 5·3 at the TOTO caldera in the Mariana Arc (12° 42·8007' N; 143° 32·3415' E), at a depth of 2922 m by means of the manned submersible Shinkai 6500 (dive no. 772) in August 2003. After deployment, it was recovered to the sea surface in a sample box from the submersible (dive no. 776). The in situ temperature of the hydrothermal fluid was measured by a self-temperature-recording thermometer (Rigosya) and the pH of the hydrothermal fluid was obtained in the onboard laboratory immediately after recovery using a gas-tight fluid sampler ‘WHATS’ (Water Hydrothermal-fluid Atsuryoku Tight Sampler) (Tsunogai et al., 2002).
The TOTO caldera deep-sea hydrothermal field in the Mariana Arc was discovered by Gamo et al. (2004) in 1999. Previous physical and chemical characterization of the hydrothermal fluid has suggested that the TOTO caldera deep-sea hydrothermal activity is accompanied by highly acidic hydrothermal fluids resulting from oxidation of volatile volcanic gas (H2S) to sulfate (Gamo et al., 2004). During a series of dive expeditions, a white-smoker hydrothermal vent with the lowest recorded pH value (pH 1·6) was found in the TOTO caldera, which reveals that the deep-sea hydrothermal activity in the TOTO caldera is a novel system driven by sub-seafloor mixing between the oxygenated sea water and the superheated volcanic gas, as proposed previously in the DESMOS caldera in the Manus Basin (Gamo et al., 1997). The STR-ISCS was deployed in one of the diffusing hydrothermal flows derived from the highly acidic hydrothermal fluid with further dilution of sea water. Thus, TOTO caldera hydrothermal activity is comparable to fumarole activity in terrestrial volcanoes and geothermal fields and this hydrothermal field may be described as a deep-sea hydrothermal fumarole. During the 4-day deployment, the temperature of the substratum in the colonization device shifted. The temperature fluctuated between 20 and 40 °C in the first 24 h, but gradually increased to 70 °C in the next 24 h. Finally, the temperature was stable at 65–70 °C for the last 2 days.
Immediately after recovery of the STR-ISCS on the ship, a portion of substratum (approx. 1 g wet weight) was suspended in 20 ml sterilized MJ synthetic sea water (Takai et al., 1999) containing 0·05 % (w/v) sodium sulfide in a 100 ml glass bottle (Schott Glaswerke) and tightly sealed with a butyl-rubber cap under a gas phase of 100 % N2 (100 kPa). The suspended slurry was used to inoculate a series of media, including MJAIS-YTF medium [MJAIS medium (Takai et al., 2003c) supplemented with yeast extract, tryptone, formate and other components under a gas phase of H2 : CO2 (80 : 20; 200 kPa); described below]. Cultures were incubated at 55 °C in a dry oven.
Growth of motile, short rods was observed in MJAIS-YTF medium after 2 days incubation at 55 °C. A pure culture was obtained using the dilution-to-extinction technique at 55 °C with the same medium used for the enrichment (Takai & Horikoshi, 2000). The isolate was designated strain Pd55T. Purity was confirmed routinely by microscopic examination and repeated partial sequencing of the 16S rRNA gene using several primers (Lane, 1991).
Cells were observed under a phase-contrast Olympus BX51 microscope with the SPOT RT Slider CCD camera system (Diagnostic Instruments). The Gram staining test was performed with a Gram Stain kit (Wako). Transmission electron microscopy of negatively stained cells was carried out as described by Zillig et al. (1990). Cells grown in MJAIS-YTF medium under a gas phase of H2 : CO2 (80 : 20; 200 kPa) at 55 °C in the mid-exponential phase of growth were used for microscopic observation. Cells of strain Pd55T were Gram-negative short rods, about 0·6–0·8 µm in diameter, 1·5–2·5 µm in length and motile with a polar flagellum (see Fig. A available as supplementary material in IJSEM Online). Spore formation was not observed under any of the culture conditions. The morphological features of strain Pd55T were similar to those of previously described thermophilic ‘Epsilonproteobacteria’, N. lithotrophica strain 525T (Miroshnichenko et al., 2002), C. hydrogeniphilus strain AM1116T (Alain et al., 2002) and H. thermophila strain EP1-55-1%T (Takai et al., 2004a).
Strain Pd55T was routinely cultivated in MJAIS-YTF medium. To prepare MJAIS-YTF medium, the MJAIS components plus 0·1 % (w/v) yeast extract, 0·1 % (w/v) tryptone and 0·02 % (w/v) formate were dissolved and the pH of the medium was adjusted to around pH 5·0 with HCl before autoclaving. After autoclaving under an air atmosphere, a concentrated vitamin solution (Balch et al., 1979) and NaHCO3, elemental sulfur and Na2S (Takai et al., 2003c) (pH adjusted to 7·0) were added to the medium under gas purging of 80 % H2 and 20 % CO2 and the pH was re-adjusted to pH 5·0 with HCl, unless otherwise noted. The four aforementioned components were separately sterilized by autoclaving except for the vitamin solution and elemental sulfur, which were filter- and steam-sterilized (three times at 95 °C for 3 h), respectively. The medium was dispensed at 20 % total bottle (Schott Glaswerke) or tube (Iwaki Glass) volume, tightly sealed with a butyl-rubber stopper under a gas phase consisting of 80 % H2 and 20 % CO2 at 200 kPa. All experiments described below were conducted in duplicate.
Growth of strain Pd55T was measured by direct cell counting after staining with 4',6-diamidino-2-phenylindole (Porter & Feig, 1980) using a phase-contrast Olympus BX51 microscope. The cultures were grown in 100 ml glass bottles (Schott Glaswerke) each containing 20 ml medium with shaking (100 r.p.m.) in a temperature-controlled dry oven. With MJAIS-YTF medium, strain Pd55T grew over the temperature range of about 30–68 °C, showing optimal growth at 50 °C; the generation time at 50 °C, pH 5·0, was about 120 min (see Fig. Ba, available as supplementary material in IJSEM Online). The effect of initial pH on growth was tested at 50 °C using MJAIS-YTF medium adjusted to various pH levels with 10 mM acetate/acetic acid buffer (pH 3–5), MES (pH 5–6), PIPES (pH 6–7) and HEPES (pH 7·0–7·5) at room temperature (see Fig. Bb, available as supplementary material in IJSEM Online). Growth occurred at initial pH 4·2–7·0, with optimum growth at about pH 5·2 (see Fig. Bb). No growth was observed below initial pH 3·4 or above initial pH 7·2. When the initial pH was 4·2–5·2, the pH of the medium increased during cultivation (final pH 5·7) (see Fig. Bb); however, the growth rate was determined in the early-exponential phase of growth and the effect of pH shift on growth was negligible. Strain Pd55T, when tested in MJAIS-YTF medium with variable amounts of NaCl added, grew in 6–50 g NaCl l–1, with optimum growth at 20 g NaCl l–1, 50 °C and pH 5·0 (see Fig. Bc, available as supplementary material in IJSEM Online). In general, the temperature and salt requirements of Pd55T were similar to those of N. lithotrophica strain 525T, C. hydrogeniphilus strain AM1116T and H. thermophila strain EP1-55-1%T (Table 1). However, the acidophilic growth of strain Pd55T was a novel physiological feature within the previously described thermophilic epsilonproteobacterial genera.
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Strictly autotrophic growth was examined in MJAIS-YTF medium lacking yeast extract, tryptone and formate under a gas phase of 80 % H2 and 20 % CO2 (200 kPa). Strain Pd55T was able to grow under strict chemolithoautotrophic conditions with H2 and S0 as the sole electron donor and acceptor, respectively. The maximal cell yield under strict chemolithoautotrophic conditions was almost the same as the yield in MJAIS-YTF medium (3–4x109 cells ml–1). However, when strain Pd55T was grown under strict chemolithoautotrophic conditions with H2 and S0, the culturability of the cells after growth was significantly reduced, i.e. the proportion of the culturable cell number after growth decreased to 10–5 of that in MJAIS-YTF medium. Culturability was examined in a series of 10–1 dilution cultivations with the strictly autotrophic medium or MJAIS-YTF medium. An improvement in culturability was observed by addition of 0·1 % (w/v) yeast extract, 0·1 % (w/v) tryptone, 0·1 % (w/v) Casamino acids, 5 mM formate, 5 mM acetate, 5 mM citrate, 5 mM tartrate, 5 mM fumarate, 5 mM succinate, 5 mM malate, 5 mM lactate or 5 mM pyruvate to the strictly autotrophic medium. Heterotrophic growth was determined in MJAIS-YTF medium lacking NaHCO3, yeast extract, tryptone and formate under a gas phase of 100 % H2 (200 kPa), containing the following potential carbon sources: 0·1 % (w/v) yeast extract, 0·1 % (w/v) peptone, 0·1 % (w/v) tryptone, 0·1 % (w/v) Casamino acids, 1 and 5 mM formate, 5 mM acetate, 5 mM glycerol, 0·025 % (v/v) methanol, 0·05 % (v/v) ethanol, 0·1 % (v/v) 2-propanol, 5 mM citrate, 5 mM tartrate, 5 mM fumarate, 5 mM maleate, 5 mM succinate, 5 mM propionate, 5 mM malate, 5 mM lactate, 5 mM oxalate, 5 mM thioglycollate, 5 mM pyruvate, 5 mM each of 20 amino acids, 0·1 % (w/v) glucose, 0·1 % (w/v) galactose, 0·1 % (w/v) sucrose, 0·1 % (w/v) fructose, 0·1 % (w/v) lactose, 0·1 % (w/v) maltose, 0·1 % (w/v) arabinose, 0·1 % (w/v) trehalose and 0·1 % (w/v) starch. Strain Pd55T was not able to grow with any of the heterotrophic substrates using H2 as an energy source and S0 as an electron acceptor. Utilization of these organic compounds as an alternative energy source instead of H2 was also examined in MJAIS-YTF medium lacking yeast extract, tryptone and formate under a gas phase of 80 % N2 and 20 % CO2 (200 kPa). None of the organic compounds sustained growth of strain Pd55T. In an attempt to determine potential electron donors and acceptors other than a combination of H2 and S0 for autotrophic growth, each of the potential electron donors such as thiosulfate (20 mM), sulfite (5 and 20 mM) or ferrous iron (20 mM) was tested with nitrate (10 mM) and fumarate (10 mM) as the electron acceptors, and each of the potential electron acceptors such as sulfite (2 and 10 mM), thiosulfate (10 mM), tetrathionate (10 mM), nitrate (10 mM), nitrite (1 and 5 mM), ferric citrate (20 mM), selenate (5 mM), arsenate (5 mM) or fumarate (10 mM) was tested with H2 as the electron donor. The anaerobic cultivation procedure in the absence of Na2S.9H2O and in the presence of ferric citrate (20 mM), selenate (5 mM) or arsenate (5 mM) has been described previously (Takai et al., 2003b). None of the combinations other than H2 and S0 supported growth of strain Pd55T. The potential nutrients required for growth such as selenite, tungstate and vitamins were examined under strict chemoautotrophic conditions in the absence of the test materials and the nitrogen source for growth (NH4Cl, NaNO2, N2, NaNO3 or yeast extract) was also examined under strict autotrophic conditions. Strain Pd55T utilized ammonium, nitrate and organic nitrogen compound as a nitrogen source, but could not utilize nitrite or molecular nitrogen. Selenium, tungsten and vitamins were not required for growth. These results indicate that strain Pd55T was a strict chemolithoautotroph utilizing H2 as the sole electron donor, S0 as the sole electron acceptor and CO2 as the sole carbon source for growth. However, the presence of organic compounds strongly improved the culturability of strain Pd55T although the mechanism is still unclear. Strain Pd55T resembles N. lithotrophica strain 525T, C. hydrogeniphilus strain AM1116T and H. thermophila strain EP1-55-1%T in utilization of molecular hydrogen as the primary electron donor, although it could not use formate as either energy or carbon source and it could not use any of the organic compounds tested as sole carbon source (Table 1
). Other than S0, N. lithotrophica strain 525T is able to utilize sulfite, C. hydrogeniphilus strain AM1116T is able to utilize nitrate and H. thermophila strain EP1-55-1%T is able to utilize nitrate and molecular oxygen as alternative electron acceptors (Table 1). Utilization of S0 as the sole electron acceptor of strain Pd55T differs markedly from the energy metabolisms of the previously described thermophilic genera within the ‘Epsilonproteobacteria’ (Table 1).
The time-course of the reduction of elemental sulfur and concomitant bacterial growth of strain Pd55T were examined in MJAIS-YTF medium under a gas phase of 80 % H2+20 % CO2 (200 kPa) (Fig. 1). The concentration of H2S in the gas phase during growth was measured using a GC Micro GC CP2002 (GL Sciences). The gas phase was periodically sampled with a 1 ml gas-tight syringe, which was directly applied to the GC or diluted once with helium gas and then applied. The consumption of molecular hydrogen and elemental sulfur was not measured because of the large amounts of hydrogen and sulfur in the medium required for growth; however, the concentration of hydrogen sulfide increased during growth of strain Pd55T (Fig. 1). Since the control medium that lacked a bacterial inoculum did not demonstrate reduction of elemental sulfur, bacterial reduction of elemental sulfur occurred during growth. Strain Pd55T was found to be a respiratory hydrogen-oxidizing, sulfur-reducing chemolithoautotroph.
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) and H. thermophila strain EP1-55-1%T (Takai et al., 2004a); C. hydrogeniphilus strain AM1116T (Alain et al., 2002) was resistant to kanamycin (100 µg ml–1).
The cellular fatty acid composition of cells grown in MJAIS-YTF medium at 55 °C in the late-exponential phase of growth was analysed. Lyophilized cells (100 mg) were placed in a Teflon-lined, screw-capped tube containing 3 ml anhydrous methanolic HCl and heated at 100 °C for 3 h. The extraction and analysis of fatty acid methyl esters were as described previously (Takai et al., 2003b). The major cellular fatty acids of strain Pd55T were C14 : 0 (4·3 %), C14 : 0 3-OH (9·8 %), C16 : 0 (12·5 %), C16 : 1 (9·7 %), C17 : 0 (4·4 %), C18 : 0 (26·5 %), C18 : 1 (22·2 %), anteiso-C19 : 0 (4·8 %) and C19 : 1 (5·8 %). This composition was generally similar to that of H. thermophila strain EP1-55-1%T (Takai et al., 2004a), although the cellular fatty acids anteiso-C19 : 0 (4·8 %) and C19 : 1 (5·8 %) were only present in strain Pd55T.
Genomic DNA of strain Pd55T was prepared as described by Marmur & Doty (1962). The G+C content of the DNA was determined by direct analysis of deoxyribonucleotides by HPLC (Tamaoka & Komagata, 1984). The DNA G+C content of strain Pd55T was 34·0 mol%, which was similar to those of N. lithotrophica strain 525T and H. thermophila strain EP1-55-1%T (34·7 and 34·6 mol%, respectively), but higher than that of C. hydrogeniphilus strain AM1116T (29 mol%) (Table 1).
The 16S rRNA gene was amplified by PCR using primers Bac27F and 1492R (DeLong, 1992; Lane, 1991), as described previously (Takai et al., 2001). The nearly complete sequence (1431 bp) of the16S rRNA gene from strain Pd55T was directly sequenced using both strands by the dideoxynucleotide chain-termination method with a DNA sequencer model 3100 (Perkin Elmer/Applied Biosystems). The rRNA gene sequence was analysed using the gapped-BLAST search algorithm (Altschul et al., 1997; Benson et al., 1998) and was most closely related (94·4 %) to the sequence of strain B455-1, isolated from a deep-sea hydrothermal environment in the Iheya North of the Okinawa Trough (Takai et al., 2003a). Similarities with the sequences of C. profundus strain CRT (Miroshnichenko et al., 2004) and N. lithotrophica strain 525T (Miroshnichenko et al., 2002), isolated from deep-sea hydrothermal systems in the MAR and EPR, respectively, were 92·1 and 92·0 %, respectively. The nearly complete sequence was manually re-aligned according to the secondary structures using ARB (Ludwig et al., 2004). Phylogenetic analyses were restricted to nucleotide positions that could be chosen using the 
-Proteobacteria filter of Hugenholtz (2002). Evolutionary distance matrix analysis (using the Jukes–Cantor correlation method) and neighbour-joining analysis were performed using ARB (Fig. 2). Bootstrap analysis was performed to provide confidence estimates for phylogenetic tree topologies. The phylogenetic tree indicated that strain Pd55T represented a novel lineage together with strain B455-1 prior to divergence of the genera Nautilia and Caminibacter (Fig. 2).
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) and C. hydrogeniphilus strain AM1116T (Alain et al., 2002) from tube-dwelling polychaetes nests of deep-sea hydrothermal systems in the EPR, but also the recently described species C. profundus strain CRT (Miroshnichenko et al., 2004) and the potential Nautilia spp. strains Am-H and EX-18.2 (Campbell et al., 2001). Similarity levels between the 16S rRNA gene sequences of strain Pd55T and either Nautilia (92·0 %) or Caminibacter (92·1 %) are within the common index of 16S rRNA gene sequence similarities for genus-level differentiation (90–96 %) (Gillis et al., 2001). In addition, phylogenetic characterization demonstrates that strain Pd55T represents a separate phylotype together with strain B455-1, which was isolated from the deep-sea hydrothermal environment in the Okinawa Trough (Takai et al., 2003a), diverging prior to differentiation of the genera Nautilia and Caminibacter. These results suggest that strain Pd55T can be genetically classified as representing a new genus within the ‘Epsilonproteobacteria’. The physiological properties of strain Pd55T reinforce differentiation from Nautilia and Caminibacter at the genus level (Table 1). Strain Pd55T grows optimally at much lower pH (5·2) and is able to grow in a much more acidic pH range (pH 4·2–7·0) than N. lithotrophica strain 525T, C. hydrogeniphilus strain AM1116T and C. profundus strain CRT (Table 1). Hydrogen-dependent energy metabolism is common among the previously described members of the genera Nautilia and Caminibacter, whereas strain Pd55T is an obligate chemolithoautotroph and can utilize only elemental sulfur as an electron acceptor (Table 1). On the basis of these physiological and molecular properties of strain Pd55T, a new genus, Lebetimonas gen. nov., is proposed. Strain Pd55T (=JCM 12420T=DSM 16356T) is proposed as the type strain of a novel species in this genus, Lebetimonas acidiphila sp. nov.
Description of Lebetimonas gen. nov.
Lebetimonas (Le.be.ti.mo'nas. L. n. lebes cauldron; L. fem. n. monas a unit, monad; N.L. fem. n. Lebetimonas cell from a cauldron).
Short rods, motile with a polar flagellum. Gram-negative. Strictly anaerobic. Thermophilic and acidophilic. Strictly chemolithoautotrophic. Able to utilize molecular hydrogen as an electron donor and elemental sulfur as an electron acceptor. NaCl absolutely required for growth. G+C content of genomic DNA is about 34 mol%. Major cellular fatty acids are C18 : 0 and C18 : 1. On the basis of 16S rRNA gene analysis, the genus Lebetimonas is related to the genera Nautilia and Caminibacter within the ‘Epsilonproteobacteria’. Members of the genus Lebetimonas occur in global deep-sea hydrothermal systems.
The type species is Lebetimonas acidiphila.
Description of Lebetimonas acidiphila sp. nov.
Lebetimonas acidiphila (a.ci.di'phi.la. L. adj. acidus, -a, -um sour; N.L. n. acidum acid; Gr. adj. philos loving; N.L. fem. adj. acidiphila acid-loving).
Each cell is a highly motile rod with a polar flagellum and a mean length of 1·5–2·5 µm and width of approximately 0·6–0·8 µm. Cells occur singly. Gram-negative. Strictly anaerobic. The temperature range for growth is 30–68 °C (optimum 50 °C). The pH range for growth is 4·2–7·0 (optimum pH 5·2). NaCl at 6–50 g l–1 is an absolute growth requirement; optimum growth occurs at 20 g l–1. Strict chemolithoautotrophic growth occurs with molecular hydrogen as an electron donor and with elemental sulfur as an electron acceptor. Elemental sulfur is reduced to hydrogen sulfide during growth. Nitrate or ammonium is required as a nitrogen source. Vitamins, selenium and tungsten are not required for growth. The major cellular fatty acids are C14 : 0 (4·3 %), C14 : 0 3-OH (9·8 %), C16 : 0 (12·5 %), C16 : 1 (9·7 %), C17 : 0 (4·4 %), C18 : 0 (26·5 %), C18 : 1 (22·2 %), anteiso-C19 : 0 (4·8 %) and C19 : 1 (5·8 %).
The type strain is Pd55T (=JCM 12420T=DSM 16356T), isolated from an in situ colonization system deployed in a hydrothermal diffusing flow (maximum temperature of 78 °C) at the TOTO caldera in the Mariana Arc. The DNA G+C content of strain Pd55T is 34·0 mol% (by HPLC).
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ACKNOWLEDGEMENTS |
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) and concomitant bacterial growth (
) of Lebetimonas acidiphila strain Pd55T.