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1 Laboratory of Marine Microbiology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
2 Subground Animalcules Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Marine Science & Technology Center, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Correspondence
Yoshihiko Sako
sako{at}kais.kyoto-u.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The DDBJ/EMBL/GenBank accession number for the 16S rDNA sequence of strain T1T is AB079382.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Brock et al., 1972; Grogan et al., 1990; Huber et al., 1992; Sako et al., 1996a, b, 2001). Members of the genus Thermus are probably the most frequently isolated extremely thermophilic aerobes from terrestrial hot-water environments. Although some strains grow mixotrophically (Skirnisdottir et al., 2001), almost all strains of the genus Thermus are obligate heterotrophs that live in various terrestrial hot environments at temperatures higher than about 55 °C and neutral to alkaline pH (Brock & Boylen, 1973; Pask-Hughes & Williams, 1975; Kristjánsson & Alfredsson, 1983; Williams & da Costa, 1992). Under anaerobic conditions, some strains of the genus Thermus are able to grow with NO3-, Fe(III) and S0 as terminal electron acceptors instead of O2 (Williams & da Costa, 1992; Sharp et al., 1995; Kieft et al., 1999).
In deep-sea hydrothermal vent environments, however, most thermophiles had been thought to be strict anaerobes until the recent discovery of facultatively aerobic thermophiles from deep-sea hydrothermal vent chimneys (Blöchl et al., 1997; Reysenbach et al., 2000a). In addition, many strictly aerobic and thermophilic bacterial strains, including Thermus thermophilus Gy1211, have been isolated from deep-sea hydrothermal vent environments in the Mid-Atlantic Ridge and Guaymas Basin (Marteinsson et al., 1995, 1999). These results suggest that strictly or facultatively aerobic microbial populations of thermophiles occur in relatively oxidative microhabitats of deep-sea hydrothermal vent environments and that their diversity and function in the whole microbial community have potentially been underestimated.
In this study, fully aerobic thermophilic micro-organisms were cultivated from a deep-sea hydrothermal vent chimney at the Suiyo Seamount in the Izu-Bonin Arc, Japan. From this hydrothermal system, various previously uncultivated bacterial and archaeal rDNA sequences were obtained by a culture-independent molecular survey (Takai & Horikoshi, 1999), although enrichment and cultivation of aerobic thermophiles have not yet been examined. A novel, strictly aerobic thermophile was isolated from the surface layer of a black smoker chimney structure. Here, the physiological and molecular properties of the novel isolate are characterized and the potential distribution of such aerobic thermophiles in deep-sea hydrothermal vents is discussed.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. The chimney was mainly composed of anhydrite (top part), barite (surface layer) and pyrite and chalcopyrite (inside structure); pyrite or chalcopyrite crystals were observed at the passage of hot fluid (vent surface). Each of the subsamples (approx. 10 g) was suspended in 20 ml sterilized MJ synthetic sea water (described below) containing 0·05 % (w/v) sodium sulfide in a 100 ml glass bottle (Schott Glaswerke) tightly sealed with a butyl rubber cap under a gas phase 100 % N2 (100 kPa). These suspended portions of the subsamples were used to inoculate a series of media, including MJYPV medium (described below) on board the surface vessel.
Enrichment and purification.
The enrichment was performed in screw-capped test tubes (Pyrex; 180x18 mm) containing 5 ml medium with air; cultures were incubated at 70 and 85 °C. The tubes of MJYPV medium inoculated only with a subsample of surface layer became turbid after 1 day incubation at both temperatures and the other subsamples did not provide positive enrichments even after 5 days incubation at 70 and 85 °C. The enrichment cultures grown at 70 °C contained slightly motile, long rod-shaped cells, whereas those at 85 °C contained highly motile coccoids. To obtain a pure culture of long rod cells grown at 70 °C, the enriched cells were streaked onto MJYPV plates hardened with 0·5 % (w/v) gelrite gellan gum (Sigma). After 1 day of incubation at 70 °C, white colonies formed on the plates. Well-isolated colonies were picked and the cells were incubated in fresh liquid MJYPV medium at 70 °C. To ensure purity, the streaking and isolation step was repeated at least three times for each isolate. The first pure culture was designated strain T1T and was investigated in detail.
Culture media and conditions.
The isolate was routinely cultivated in MJYPV medium, which contained the following components in 1 l MJ synthetic sea water (Sako et al., 1996b): 1 g yeast extract (Difco), 1 g tryptone (Difco) and 10 ml vitamin solution (Balch et al., 1979). To prepare MJYPV medium, 1 g yeast extract and 1 g tryptone were dissolved in 1 l MJ synthetic sea water and the pH of the medium was adjusted to approximately 7·0 with NaOH prior to autoclaving, unless otherwise noted. Filter-sterilized vitamin solution (Balch et al., 1979) was added after autoclaving. For testing the effects of pH on growth, the pH of MJYPV medium containing 20 mM MES (pH 5·0–6·0), PIPES (pH 6·25–7·0), HEPES (pH 7·3–8·0) or CAPSO (pH 8·5 and above) was adjusted to the required value with H2SO4 or NaOH at room temperature. The pH was checked after autoclaving and was axenically readjusted with H2SO4 or NaOH at room temperature if necessary. The pH of all media was stable during the cultivation period. NaCl requirements were determined with a varying concentration of 0–6 % (w/v) NaCl in MJ synthetic sea water.
In an attempt to examine whether the isolate was able to grow under anaerobic conditions, H2+CO2 (80 : 20) and N2+CO2 (80 : 20) (200 kPa) were tested as gas phases with MJYPV medium in the presence or absence of possible alternative electron acceptors such as 0·1 % (w/v) NaNO3, Na2SO3, NaNO2 or Na2S2O3 or 3 % (w/v) S0. To ensure anaerobic growth conditions, a 10 % (w/v) Na2S.9H2O solution (pH 7·5, adjusted with H2SO4 and separately autoclaved) was added to the medium to a final concentration of 0·05 % (w/v). Autotrophic growth was determined with air using MJ synthetic sea water containing 1 % (v/v) vitamin solution, supplemented with a possible electron donor (0·1 % Na2S2O3, tetrathionate, NaNO2 or Na2SO3 or 3 % S0) and 0·2 % (w/v) NaHCO3 as a carbon source.
Measurement of growth.
Growth of the isolate was determined by measuring turbidity at 600 nm using a spectrophotometer (UV-160A; Shimadzu) and by direct cell counts after staining with 4',6-diamidino-2-phenylindole (DAPI) (Porter & Feig, 1980) using a Nikon Eclipse E800 microscope equipped with a colour chilled 3 CCD camera system (C5810; Hamamatsu Hokutonikusu). Duplicate cultures were grown in cotton-plugged 300 ml Erlenmeyer flasks containing 100 ml medium in an air-batch rotary shaker (RGS-32.TT; Sanki Seiki) and were shaken at 100 r.p.m. in all cases. Temperatures were measured inside control flasks alongside the cultures; temperatures were stable during the cultivation period. Growth at various pH values and NaCl concentrations was determined at 67·5 °C and the growth conditions for all other cultivation tests were 67·5 °C and pH 7·0, unless otherwise noted.
Biochemical properties.
Catalase activity was determined by the formation of oxygen bubbles with 3 % hydrogen peroxide solution. Oxidase activity was determined by the oxidation of 1 % (w/v) TMPD (N,N,N',N'-tetramethyl-p-phenylenediamine dihydrochloride) solution on filter paper at room temperature using T. thermophilus HB8T (=ATCC 27634T) as a positive control. Gelatin, starch and casein hydrolysis were examined as described previously (Marteinsson et al., 1995).
Light and electron microscopy.
Cells were routinely observed with a differential interference microscope (UFX; Nikon). For observation by TEM, cells were fixed with 1 % (v/v) glutaraldehyde in 0·1 M Na2HPO4/KH2PO4 (pH 7·2) buffer and post-fixed with 1 % (v/v) OsO4. The fixed cells were then dehydrated with an increasing concentration series of ethanol and embedded in epoxy resin. Ultrathin sections were stained with uranyl acetate and lead acetate and examined under an H-700H EM (Hitachi) at an accelerating voltage of 100 kV. Negative staining of cells for EM was achieved with 2 % (v/v) phosphotungstic acid.
Organic substrates for growth.
In an attempt to find organic substrates that could support or stimulate growth of the isolates, various organic substrates were tested instead of both yeast extract and tryptone in MJYPV medium. Each of the following substrates was added alone or with 0·01 % yeast extract at concentrations of 0·02 and 0·2 % (w/v): L-arginine, L-asparagine, L-aspartate, L-glutamate, L-phenylalanine, L-proline, L-serine, L-valine, Casamino acids, gelatin, D-(-)-fructose, D-(+)-glucose, galactose, myo-inositol, D-sorbitol, D-(+)-xylose, D-(+)-cellobiose, lactose, maltose, D-(+)-trehalose, sucrose, chitin, starch, sodium acetate, citrate, glycerol, L-malate, sodium pyruvate, casein, yeast extract and tryptone peptone (Difco). The cells were pre-cultured in each medium prior to inoculation of the same medium. These tests were performed at temperatures of 62·5 and 67·5 °C in shake flasks and run in duplicate.
Cellular fatty acid composition and respiratory quinone analyses.
The cellular fatty acid composition was analysed using cells grown in MJYPV medium at 67·5 °C at the late-exponential growth phase. Cellular fatty acid composition and respiratory quinone analyses were performed at NCIMB Japan Corporation, Shizuoka, Japan. Quinones were extracted from freeze-dried cells with chloroform/methanol (2 : 1, v/v) and acetone and purified by TLC. They were separated with HPLC equipped with a Shim-pack VP-ODS column (Shimadzu) for identification (Tamaoka et al., 1983).
Fatty acids were converted to methyl esters by treatment with anhydrous methanolic HCl. Fatty acid methyl esters were analysed by GC using a non-polar capillary column and flame-ionization detection.
Isolation and base composition of DNA.
Genomic DNA of strain T1T was prepared as described by Lauerer et al. (1986). The G+C content of the genomic DNA was determined by direct analysis of deoxyribonucleotides using HPLC with a DNA-GC kit (Yamasa Shouyu) after digestion of the DNA with nuclease P1 (Tamaoka & Komagata, 1984).
Amplification of 16S rRNA gene and sequence determination.
The 16S rRNA gene was amplified by PCR using Eubac 27F and 1492R primers (DeLong, 1992). The 1·5 kb PCR product was sequenced directly by the dideoxynucleotide chain-termination method using an ABI 373A automated DNA sequencer (Applied Biosystems). The almost complete sequence (1493 bp) of the 16S rDNA of strain T1T was aligned manually with a subset of 16S rDNA sequences obtained from the DNA Database of Japan (DDBJ) and the Ribosomal Database Project II (RDP-II) (Maidak et al., 2001) using CLUSTAL X (Thompson et al., 1997). Phylogenetic analyses were restricted to nucleotide positions that could be aligned unambiguously in all sequences (Takai & Horikoshi, 1999; Takai & Sako, 1999). Neighbour-joining analysis (Saitou & Nei, 1987) of 1265 homologous positions was accomplished using CLUSTAL X. Bootstrap analysis was used to provide confidence estimates for phylogenetic tree topologies.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Morphology
Cells of strain T1T were Gram-negative rods, about 7·5–9·4 µm long and 0·9–1·0 µm wide in the exponential growth phase (Fig. 1a). In the stationary growth phase, the cells tended to form filaments. ‘Rotund bodies’, occasionally observed in many Thermus strains (Brock & Edwards, 1970), were never observed microscopically. EMs of thin sections showed that the isolate had a cell wall structure typical of Gram-negative bacteria. The cells have an envelope consisting of a cytoplasmic membrane with a simple outline and a cell wall with an inner, electron-dense thin layer, presumably representing the peptidoglycan (Fig. 1b).
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The isolate grew at temperatures of about 50·0–72·5 °C, showing optimum growth at 67·5 °C; the generation time at 67·5 °C was about 30 min. No growth was observed at 75 or 45 °C (Fig. 2a). Growth of the isolate at 67·5 °C occurred between pH 6·25 and 7·75, with optimum growth at about pH 7·0. No growth was detected below pH 6·25 or above pH 7·75 (Fig. 2b). The isolate absolutely required NaCl for growth and was able to grow in 0·5–4·5 % NaCl. Optimum growth was detected at around 3 % NaCl at 67·5 °C. No growth was observed below 0·5 % or above 5 % NaCl (Fig. 2c).
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Fatty acid, quinone and DNA base composition
When the isolate was grown at 67·5 °C, the major cellular fatty acids were iso-C15 : 0 (40·4 %), iso-C17 : 0 (28·5 %), C16 : 0 (12·9 %), anteiso-C15 : 0 (6·0 %), anteiso-C17 : 0 (5·4 %), iso-C16 : 0 (2·8 %) and iso 3-OH C11 : 0 (1·0 %). Menaquinone-8 was the major respiratory quinone. This fatty acid and respiratory quinone composition was similar to those of members of the genus Thermus, as described previously (Hensel et al., 1986; Prado et al., 1988). However, the presence of iso 3-OH C11 : 0 in the fatty acid composition of the isolate distinguished it from Thermus species.
The G+C content of the genomic DNA of strain T1T was 68·6 mol%. This value is very similar to those of members of the genus Thermus (Duffield & Cossar, 1995).
Phylogenetic analyses
The almost complete 16S rRNA gene sequence (1493 bp) from strain T1T was determined and was most closely related to sequences from members of the genus Thermus, such as Thermus igniterrae RF-4T (88·6 %) (Chung et al., 2000) and Thermus oshimai SPS17T (88·6 %) (Williams et al., 1996). This low phylogenetic relatedness is below the common index of 16S rDNA sequence similarity for differentiation of micro-organisms at the genus level (90–96 %) (Gillis et al., 2001), although most of physiological and chemotaxonomic features (temperature and pH ranges for growth, G+C content of the genomic DNA, major fatty acid and quinone compositions) of strain T1T were similar to those displayed by members of the genus Thermus. To determine the phylogenetic position of the isolate, evolutionary distances based on 16S rRNA gene sequences of representative members of the Bacteria were calculated and a phylogenetic tree was constructed using the neighbour-joining method (Fig. 3). In the phylogenetic tree, the isolate was on a distinct branch deeply separated from a cluster of the branches of Thermus strains, which also supported phylogenetic differentiation of the isolate from members of the genus Thermus.
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; Harmsen et al., 1997; Takai et al., 2000, 2001; Takai & Horikoshi, 2000; Holden et al., 2001; Wery et al., 2001). Most of these thermophilic bacteria and archaea are strict anaerobes with fermentative metabolisms, and several strains within the orders Archaeoglobales (Burggraf et al., 1990; Huber et al., 1997) and Desulfurococcales (Jannasch et al., 1988; Pley et al., 1991; Blöchl et al., 1997) have anaerobic respiratory metabolisms using sulfate, sulfite and elemental sulfur as electron acceptors. Considering the successful retrieval of strain T1T from the surface zone of the chimney structure and the strict O2-dependence of its metabolism, active populations of this strain might be distributed in relatively oxidative microhabitats such as the surface area of chimney structures in deep-sea hydrothermal vent environments. Recent culture-independent molecular analyses have indicated the prevalence of putative mesophilic 
-Proteobacteria in the surface area of chimney structures and sulfide materials (Moyer et al., 1994, 1995; Reysenbach et al., 2000b). The finding of strictly aerobic, heterotrophic thermophiles such as strain T1T and Rhodothermus strains from the surface microhabitats of the chimney structure may provide a new insight into the ecological significance of the aerobic, thermophilic decomposers in the circulation of organic compounds in deep-sea hydrothermal vent ecosystems.
The isolate represents a distinct lineage within the family Thermaceae. Many strains of Thermus and Meiothermus have been isolated from terrestrial geothermal environments, although some strains, such as T. thermophilus Gy1211, have been obtained from shallow and deep-sea hydrothermal vent environments (Hudson et al., 1986; Kristjánsson et al., 1986; Hjörleifsdóttir et al., 1989; Manaia & da Costa, 1991; Marteinsson et al., 1999). A distinctive physiological feature commonly displayed by all Thermus strains, including marine isolates, is that they do not show an absolute requirement for NaCl for growth. Strain T1T is the first isolate within the phylum Thermus/Deinococcus that grows optimally under a salinity equivalent to that of sea water and has an absolute requirement for NaCl for growth. On the basis of these results, a new genus, Marinithermus gen. nov., is proposed. The type species is Marinithermus hydrothermalis gen. nov., sp. nov., of which the type strain is strain T1T (=JCM 11576T =DSM 14884T).
Description of Marinithermus gen. nov.
Marinithermus (ma.ri.ni.ther'mus. L. adj. marinus of the sea; Gr. adj. thermos hot; N.L. n. Marinithermus an organism living in marine hot places).
Rod-shaped bacterium, Gram-negative, with branched chain fatty acids and menaquinone-8. Thermophilic. Growth suited to the pH and salinity of sea water; able to grow at 55–70 °C, pH 6·2–7·7 and 1·0–4·5 % NaCl. Aerobic, heterotrophic, able to utilize organic complex substrates, amino acids, carboxylic acids and sugars. The G+C content is approximately 68 mol%. 16S rDNA sequence comparison locates Marinithermus in a novel lineage deeply branched prior to the divergence of the genus Thermus. The type species is Marinithermus hydrothermalis.
Description of Marinithermus hydrothermalis sp. nov.
Marinithermus hydrothermalis (hy.dro.ther.ma'lis. N.L. masc. adj. hydrothermalis pertaining to a hydrothermal vent).
Cells are Gram-negative, non-motile, straight rods, 7·5–9·4x0·9–1·0 µm, that occur in pairs or are filamentous under optimal conditions. Colonies are whitish and 2·5–3·0 mm in diameter. Aerobic, thermophilic, neutrophilic heterotroph. Growth occurs at temperatures of 50·0–72·5 °C (optimum 67·5 °C), at pH 6·25–7·75 (optimum pH 7·0) and in the presence of 0·5–4·5 % NaCl (optimum 3 % NaCl). Generation time under optimal conditions is about 30 min. Cytochrome oxidase- and catalase-negative. The major cellular fatty acid components are iso-C15 : 0 (40·4 %), iso-C17 : 0 (28·5 %), C16 : 0 (12·9 %), anteiso-C15 : 0 (6·0 %), anteiso-C17 : 0 (5·4 %), iso-C16 : 0 (2·8 %) and iso 3-OH C11 : 0 (1·0 %). The major quinone is menaquinone-8. Growth occurs on complex organic substrates such as yeast extract and tryptone peptone. The DNA base composition of the type strain, strain T1T (=JCM 11576T =DSM 14884T), is 68·6 mol%. Isolated from a deep-sea hydrothermal vent chimney at Suiyo Seamount in the Izu-Bonin Arc, Japan (28°34·287'N, 140°38·663'E; depth 1385 m).
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ACKNOWLEDGEMENTS |
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