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1 Subground Animalcule Retrieval (SUGAR) Project, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
2 Department of Earth Sciences, University of Southern California, 3651 Trousdale Parkway, Los Angeles, CA 90089-0740, USA
Correspondence
Hisako Hirayama
hirayamah{at}jamstec.go.jp
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ABSTRACT |
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-Proteobacteria, but was distantly related to recognized genera. On the basis of its physiological and molecular properties, strain C55T (=JCM12421T=DSM 16629T=ATCC BAA-941T) is proposed as the type strain of Thiobacter subterraneus gen. nov., sp. nov.
Micrographs of cell morphology and a diagram showing the effects of temperature, pH and Na+ concentration on growth of C55T are available as supplementary figures in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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-Proteobacteria are prevalent in terrestrial hot springs at high temperatures with neutral to alkaline pH (Huber et al., 1998
; Hugenholtz et al., 1998; Reysenbach et al., 1994; Stöhr et al., 2001; Takai et al., 2001, 2002; Yamamoto et al., 1998). Previous culture-independent analyses of microbial communities in subsurface geothermal aquifer waters (70–73 °C) in a Japanese gold mine identified two predominant phylotypes, pHAuB-D within the Aquificales and pHAuB-J within the -Proteobacteria, representing novel phylogenetic affiliations distantly related to previously cultivated strains (Takai et al., 2002). Numerous cultivation experiments to identify these previously uncultivated phylotypes were conducted by focusing on thermophilic chemolithotrophs capable of using inorganic substrates enriched in the aquifer, and they resulted in successful isolation of several potential novel thermophilic species and the description of a novel hydrogen- and sulfur-oxidizing bacterium, Sulfurihydrogenobium subterraneus (Takai et al., 2002, 2003; Inagaki et al., 2003). In this study, isolation and characterization of another novel thermophilic sulfur/thiosulfate-oxidizing bacterium within the -Proteobacteria are described. The 16S rRNA gene sequence of this bacterium was similar to those of the previously detected environmental clones pHAuB-J from the mine and OPB37 from sulfide-rich sediment in the Obsidian Pool (75–95 °C) in Yellowstone National Park, USA (Hugenholtz et al., 1998).
A number of thermophilic, hydrogen- and/or sulfur-oxidizing members of the -Proteobacteria have been described, including genera such as Hydrogenophilus (Hayashi et al., 1999; Stöhr et al., 2001), Thiomonas (Shooner et al., 1996), Thermothrix (Caldwell et al., 1976; Odintsova et al., 1996), Tepidimonas (Moreira et al., 2000) and Thiobacillus (Wood & Kelly, 1988). These organisms have been isolated from terrestrial hot-spring environments or wastewater-treatment plants, and most of them are facultatively autotrophic or strictly heterotrophic organisms. Thermothrix azorensis is obligately chemolithoautotrophic, using reduced sulfur compounds as the energy source. The new isolate showing obligately chemolithoautotrophic growth by the oxidation of reduced sulfur compounds is phylogenetically and physiologically compared with members of the genera within the -Proteobacteria.
Sample collection, enrichment and purification
A hot (70·4 °C) subsurface aquifer water from AW-S hole in the main deposit of the Hishikari gold mine, Kagoshima Prefecture, Japan, was obtained at the dewatering station in the mine (Izawa et al., 1990; Takai et al., 2002). At the time of sampling, 1 ml of the hot aquifer water was inoculated into 3 ml TSmj medium (see below) under a gas phase of 80 % N2, 15 % CO2 and 5 % O2 (200 kPa). After transportation of the inoculated medium to the laboratory without temperature control, cultivation was performed at 55 °C in a dry oven. Growth of motile, straight rods was observed after 3 days of incubation. A pure culture was obtained by using the repeated dilution-to-extinction technique (Baross, 1995) at 55 °C with the same medium as used for the enrichment. This culture was designated strain C55T. Its purity was confirmed routinely by microscopic examination and by repeated partial sequencing of the 16S rRNA gene using several PCR primers.
Culture medium and conditions
Strain C55T was routinely cultivated in TSmj medium. TSmj medium consists of 1 g Na2S2O3.5H2O, 0·5 g NaHCO3, 0·5 g NH4Cl, 1 g Na2SiO3.9H2O and 10 ml vitamin mixture (Balch et al., 1979) per litre of mj water (Takai et al., 2001). The mj water consists of (per litre of distilled, deionized water) 3·0 g NaCl, 14 mg K2HPO4, 80 mg CaCl2, 0·34 g MgSO4.7H2O, 0·42 g MgCl2.6H2O, 33 mg KCl, 0·05 mg NiCl2.6H2O, 0·05 mg Na2SeO3.5H2O, 0·01 mg Na2WO4, 2 mg Fe(NH4)2(SO4)2.6H2O and 1 ml trace mineral solution (Balch et al., 1979). To prepare TSmj medium, all chemical reagents other than vitamin solution and NaHCO3 were dissolved, and the pH of the medium was adjusted to around 7·0 with HCl before autoclaving. After autoclaving under an air atmosphere, a concentrated solution of vitamins and NaHCO3 was added to the medium. The concentrated NaHCO3 solution was separately sterilized by autoclaving and the vitamin solution was filter-sterilized. The medium, dispensed at 20 % of the bottle (Schott Glaswerke) or tube (Iwaki Glass) volume, was then purged with 80 % N2 and 20 % CO2. The bottle or tube was tightly sealed with a butyl rubber stopper and the headspace was then pressurized with a gas mixture (80 % N2, 18 % CO2 and 2 % O2) at 200 kPa unless otherwise indicated.
Morphology
Cells were observed under a phase-contrast Olympus BX51 microscope with the SPOT RT Slider CCD camera system (Diagnostic Instruments). Transmission electron microscopy of negatively stained cells was carried out as described by Zillig et al. (1990). Cells grown in TSmj medium under microaerobic conditions (2 % partial pressure of O2) at 55 °C in the mid-exponential phase of growth were negatively stained with 2 % (w/v) uranyl acetate and observed under a JEOL JEM-1210 electron microscope at an accelerating voltage of 120 kV. Cells of strain C55T were Gram-negative rods, about 1·1–1·9 µm long and 0·4–0·5 µm wide, and were motile with a polar flagellum (see Supplementary Figs A and B in IJSEM Online).
Growth characteristics
Growth of strain C55T was measured by direct cell counting after staining with 4',6-diamidino-2-phenylindole using a phase-contrast Olympus BX51 microscope. Duplicate cultures were prepared in 100 ml glass bottles each containing 20 ml medium, with shaking (100 r.p.m.) in a temperature-controlled dry oven. In TSmj medium, strain C55T grew at the temperature range of 35–62 °C, with optimal growth at 50–55 °C. No growth was observed below 30 °C or above 65 °C (see Supplementary Fig. C in IJSEM Online). The effect of pH on growth was tested at 55 °C. The pH of TSmj medium was readjusted with HCl or NaOH immediately before inoculation. The pH of the TSmj medium used for this experiment was found to be stable during cultivation up to a density of 2x106 cells ml–1, and therefore growth was monitored in cultures with a density below this value. Growth of strain C55T occurred at pH 5·2–7·7, with optimum growth at pH 6·5–7·0 (Supplementary Fig. D). No growth was observed at pH 5·1 or 8·5.
To determine the effect of mineral salt concentration on growth, variously diluted or concentrated mj waters containing constant amounts of Na2S2O3.5H2O, NaHCO3, NH4Cl, Na2SiO3.9H2O, vitamin mixture and trace mineral solution were tested. Growth of strain C55T was determined with several Na+ concentrations in the medium. Strain C55T grew at [Na+] between 20 and 280 mM. Optimum growth was seen at 70 mM [Na+], 55 °C and pH 6·5, with a 60 min doubling time (Supplementary Fig. E).
The effect of oxygen concentration in the gas phase was tested with TSmj medium under a series of gas mixtures of N2/CO2/O2 of 80 : 20 : 0, 80 : 19·5 : 0·5, 80 : 19 : 1, 80 : 18 : 2, 80 : 15 : 5, 75 : 15 : 10 or 65 : 15 : 20, at 200 kPa. Growth of strain C55T was observed at 0·5–10 % O2 with an increase in cell numbers from 3x108 to 2x109 cells ml–1. The maximum increase in growth of strain C55T was seen under 2 or 5 % O2 with 1–2x109 cells ml–1, whereas no growth was observed either in the absence of O2 or under 20 % O2. These results indicated that strain C55T is a microaerophilic organism.
Heterotrophic growth was examined in TSmj medium without NaHCO3 under a gas phase of 98 % N2 and 2 % O2 (200 kPa), containing potential organic carbon sources: 0·1 % (w/v) each of yeast extract, peptone, tryptone and Casamino acids, 5 mM each of formate, acetate, citrate, tartrate, fumarate, malate, succinate, lactate, oxalate and pyruvate, 0·02 % (w/v) each of glucose, galactose, sucrose, maltose and 0·01 % methanol. Strain C55T was not able to grow with any of the organic compounds tested as sole carbon sources. Furthermore, no stimulation of growth was observed with the addition of yeast extract or tryptone to TSmj medium containing thiosulfate, NaHCO3 and CO2 in a gas phase.
To determine potential electron donors other than thiosulfate for autotrophic growth, 1 or 5 mM each of Na2S, cysteine hydrochloride, disulfate (Na2S2O7) or elemental sulfur (3 %; w/v) was added to TSmj medium instead of thiosulfate as a sole electron donor with a gas phase of 80 % N2, 18 % CO2 and 2 % O2 (200 kPa). Molecular hydrogen was also examined in TSmj medium without thiosulfate with a gas phase of 80 % H2, 18 % CO2 and 2 % O2 (200 kPa). Elemental sulfur as an electron donor resulted in a similar maximum increase in cell numbers to that obtained with thiosulfate (1x109 cells ml–1), whereas Na2S (1 mM) produced lower cell numbers (1–2x108 cells ml–1) and other reduced sulfur compounds and hydrogen did not support growth of strain C55T as the sole electron donor. Na2S at 5 mM seemed to be toxic to strain C55T. No electron acceptor tested [NaNO3 (2 or 10 mM), NaNO2 (1 or 5 mM), ferric citrate (20 mM), ferrihydrite (20 mM), Na2SO3 (5 mM), Na2SO4 (5 mM)] supported growth of strain C55T. These results indicate that strain C55T is a chemolithoautotroph utilizing reduced sulfur compounds (thiosulfate, elemental sulfur or sulfide) as an energy source and molecular oxygen as the sole electron acceptor.
With regard to nitrogen sources for growth, strain C55T utilized nitrate, ammonium and Casamino acids, but could not utilize NaNO2 or N2.
The time-course of oxidation of thiosulfate during growth of strain C55T was monitored with TSmj medium at pH 6·5 under a gas phase of 80 % N2, 18 % CO2 and 2 % O2 (200 kPa) at 55 °C (Fig. 1). Concentrations of thiosulfate, sulfite and sulfate were analysed using the P/ACE MDQ capillary electrophoresis system (Beckman Coulter). Consumption of thiosulfate and production of sulfate were both observed during the growth of strain C55T. However, some inconsistency was observed in the stoichiometry of thiosulfate consumption and resulting sulfate production by strain C55T. During the early growth phase (0–3 h), 1·4 mM thiosulfate was consumed but only 0·2 mM sulfate was produced (7 % of the theoretical value) (Fig. 1). During the mid-exponential growth phase (3–5 h), 0·8 mM thiosulfate was consumed and 1 mM sulfate was produced (63 % of the theoretical value). In contrast, in the late exponential growth phase (5–7·5 h), consistency in stoichiometry was found, with 2·1 mM thiosulfate consumed and 4·3 mM sulfate produced (100 % of the theoretical value). However, in the stationary growth phase (7·5–16·5 h), only 0·1 mM thiosulfate was consumed whereas 1·2 mM sulfate was produced (600 % of the theoretical value). This result indicates possible accumulation of sulfur compounds in the cells of strain C55T, especially in the early stages of growth, because no obvious elemental sulfur precipitation was observed in the medium during growth. Accumulated sulfur compounds in the cells of strain C55T were found during fatty acid analysis (see below). From the concentrated fatty acid sample extracted from whole cells of strain C55T, considerable amounts of sulfur compounds were precipitated. Further GC-MS analysis of the sample detected a cyclic polysulfur (8S) peak among the peaks of fatty acids. Therefore, strain C55T seemed to transport thiosulfate into the cells and accumulate it as polysulfur, especially in the early stage of growth, for utilization as an energy source in the stationary phase. The production of sulfite was not observed during growth. The control medium (uninoculated) did not exhibit either thiosulfate oxidation or sulfate production. These results indicate that strain C55T is a respiratory sulfur-oxidizer, producing sulfate as an end product.
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Fatty acid composition and G+C content of genomic DNA
The cellular fatty acid composition of cells grown in TSmj medium at 55 °C in the late exponential growth phase was determined. 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. Extraction and analysis of fatty acid methyl esters were done as described by Takai et al. (2003). The major cellular fatty acids of strain C55T were C16 : 0 (72·8 %), C16 : 1 (23·1 %), C18 : 0 (2·3 %), iso-C18 : 0 (1·3 %) and C18 : 1 (0·4 %). The ratio of n-C16 fatty acids (95·9 % of the total fatty acids) in strain C55T was high in comparison with other thermophilic micro-organisms within the -Proteobacteria, such as Hydrogenophilus hirschii (58 %; Stöhr et al., 2001), Tepidimonas ignava (49 %; Moreira et al., 2000) or Tepidiphilus margaritifer (43 %; Manaia et al., 2003). Genomic DNA of strain C55T was prepared as described by Marmur & Doty (1962). The DNA G+C content was determined by direct analysis of deoxyribonucleotides using HPLC (Tamaoka & Komagata, 1984). The G+C content of the genomic DNA of strain C55T was 66·9 mol%, a value similar to that of other thermophilic members of the -Proteobacteria, including Hydrogenophilus thermoluteolus (63·5 mol%; Hayashi et al., 1999), Tepidiphilus margaritifer (64·8 mol%; Manaia et al., 2003), Thiobacillus aquaesulis (65·7 mol%; Wood & Kelly, 1988) and Tepidimonas ignava (69·7 %; Moreira et al., 2000) (Table 1).
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-Proteobacteria, and comparative evolutionary distance analysis demonstrated that the isolate represents a separate lineage of descent within the -Proteobacteria (Fig. 2). The highest similarity (98 %) was observed between the 16S rRNA gene sequences of strain C55T and the environmental clone pHAuB-J previously detected from the same hot aquifer water (Takai et al., 2002). The sequence of strain C55T was also similar to that of environmental clone OBP37 (95 %), which was detected from sulfide-rich sediment in the Obsidian Pool (75–95 °C) in Yellowstone National Park, USA (Hugenholtz et al., 1998). Other than these environmental clone sequences, strain C55T was distantly related to members of other genera within the -Proteobacteria, such as Azoarcus buckelii U120T (92·9 %; Mechichi et al., 2002), Sterolibacterium denitrificans Chol-1ST (92·1 %; Tarlera & Denner, 2003), Thiobacillus aquaesulis ATCC 43788T (91·8 %; Wood & Kelly, 1988), Tepidiphilus margaritifer N2-214T (90·8 %; Manaia et al., 2003), Tepidimonas ignava SPS-1037T (90·6 %; Moreira et al., 2000), Hydrogenophilus thermoluteolus HT-1T (89·1 %; Hayashi et al., 1999) and Thiomonas thermosulfata ATCC 51520T (85·5 %; Shooner et al., 1996).
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-Proteobacteria in hot springs and other high temperature environments (Hugenholtz et al., 1998; LaPara et al., 2000; Yamamoto et al., 1998). Yet relatively few thermophilic micro-organisms within the -Proteobacteria have been isolated and described, and almost none of these has been an obligate chemolithoautotroph (Table 1
). Thiobacillus aquaesulis ATCC 43788T and Thiomonas thermosulfata ATCC 51520T are facultatively chemolithoautotrophic sulfur-oxidizers, whereas Tepidimonas ignava SPS-1037T is an obligate heterotroph with the ability to use reduced sulfur compounds as an energy source. Species of the genus Hydrogenophilus are facultative chemolithoautotrophs by the oxidation of H2, and a chemo-organoheterotrophic Tepidiphilus margaritifer strain N2-214T is reported to show a positive hydrogenase activity. In comparison with these thermophilic species of -Proteobacteria isolated from terrestrial hot-spring environments or wastewater-treatment plants, strain C55T represents obligately chemolithoautotrophic growth by the oxidation of reduced sulfur compounds, and is the first thermophilic isolate from a subsurface geothermal environment within the -Proteobacteria. On the basis of its physiological and molecular properties, we consider that strain C55T represents a novel genus, Thiobacter gen. nov., with type species Thiobacter subterraneus sp. nov.
Description of Thiobacter gen. nov.
Thiobacter (Thi.o.bac'ter. Gr. neut. n. thion sulfur; N.L. masc. n. bacter a rod; N.L. masc. n. Thiobacter sulfur rod).
Cells are Gram-negative, motile and rod-shaped. Thermophilic aerobe. Growth occurs chemolithoautotrophically with reduced sulfur compounds as electron donors and with oxygen as an electron acceptor using CO2 as a carbon source. Phylogenetically affiliated to the -Proteobacteria. The type species is Thiobacter subterraneus.
Description of Thiobacter subterraneus sp. nov.
Thiobacter subterraneus (sub.ter.ra'ne.us. L. masc. adj. subterraneus under the earth, indicating the source of isolation).
Cells are straight with a polar flagellum, 1·1–1·9 µm long and 0·4–0·5 µm wide. Microaerobic (up to 10 % O2 in a gas phase, optimum 2–5 %). Temperature range for growth is 35–62 °C (optimum 50–55 °C). pH range for growth is 5·2–7·7 (optimum 6·5–7·0). Na+ concentration range for growth is 20–280 mM (optimum 70 mM). Chemolithoautotrophic growth occurs with elemental sulfur and reduced sulfur compounds, such as thiosulfate and sulfide, as electron donors and with molecular oxygen as the sole electron acceptor. Obligately autotrophic using CO2 as the sole carbon source. Nitrate and ammonium are used for the nitrogen source. The major cellular fatty acids are C16 : 0 (72·8 %), C16 : 1 (23·1 %), C18 : 0 (2·3 %), iso-C18 : 0 (1·3 %) and C18 : 1 (0·4 %). The DNA G+C content is 66·9±0·2 mol% (by HPLC).
The type strain, C55T (=JCM12421T=DSM 16629T=ATCC BAA-941T), was isolated from subsurface hot aquifer water in the Hishikari gold mine, Kagoshima Prefecture, Japan.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTMAIN TEXTREFERENCES |
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), the production of sulfate (
) and concomitant bacterial growth (
) of strain C55T.