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1 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 6, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan
2 Biological Resource Centre (NBRC), National Institute of Technology and Evaluation (NITE), 2-5-8 Kazusakamatari, Kisarazu, Chiba 292-0818, Japan
3 Graduate School of Science, Tohoku University, Sendai, Miyagi 980-8578, Japan
4 Institute for Marine Resource and Environment, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan
Correspondence
Satoshi Hanada
s-hanada{at}aist.go.jp
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain St55BT is AB107956.
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; Marteinsson et al., 1995; Takai & Horikoshi, 1999; Takai et al., 2001, 2003). In recent years, many novel thermophilic bacteria have been found in and around these hydrothermal vents (Alain et al., 2002b; Götz et al., 2002; Huber et al., 2002; Jeanthon et al., 2002; Miroshnichenko et al., 2003a, b; Nakagawa et al., 2003; Sako et al., 2003; Vetriani et al., 2004; Wery et al., 2001).
Investigations of thermophilic isolates in the domain Bacteria have focused on chemoautotrophs (e.g. oxidizers of hydrogen and sulfur compounds and anaerobes that reduce sulfur and nitrogen compounds). The ecosystem in hydrothermal vents does not consist solely of chemoautotrophs, but probably contains many heterotrophic thermophiles as decomposers or scavengers. In fact, many novel chemoheterotrophic bacteria have been isolated recently from hydrothermal environments. Among the heterotrophs isolated are three species belonging to the family Thermaceae: Marinithermus hydrothermalis (Sako et al., 2003), Oceanithermus profundus (Miroshnichenko et al., 2003a) and Vulcanithermus mediatlanticus (Miroshnichenko et al., 2003b). These novel species of the Thermaceae, recently proposed in rapid succession, are all ‘true’ marine organisms that require NaCl for growth. Before these marine species were found, all species in this family (belonging to the genera Thermus and Meiothermus) were inhabitants of freshwater environments, or were isolated from marine environments but were merely halotolerant and not halophilic (Marteinsson et al., 1995). These marine species were rod-shaped micro-organisms able to grow by respiration with oxygen as a terminal electron acceptor. However, the two species O. profundus and V. mediatlanticus are relatively sensitive to oxygen, and grow well at oxygen concentrations of less than 6 % (v/v) and 4–8 % (v/v), respectively (Miroshnichenko et al., 2003a, b). The microaerophiles are also able to use nitrate as an electron acceptor under anaerobic conditions.
Recently, a novel thermophilic, sulfur-reducing bacterium, designated strain St55BT, was isolated from a chimney in a vent deposit sample in a submarine hydrothermal field. The chimney sample containing strain St55BT was collected from Suiyo Seamount in Izu-Bonin Arc, Western Pacific (28° 34' N 140° 39' E; depth, 1380 m) by the vessel ROV Hakuyo 2000 (Shin Nippon Kaiji) on 9 August 2001. The chimney sample was approximately 50 cm in diameter and 30 cm in length. A black smoker (300 °C) was discharging from this chimney. Mineralogical zoning was recognized in this chimney sample: the central part is essentially composed of chalcopyrite (CuFeS2), the middle part is composed of sphalerite (ZnS), pyrite (FeS2) and anhydrite (CaSO4), while sphalerite and pyrite are essential constituents of the outer part, together with arsenic sulfides. Elemental sulfur was also found in the middle and outer parts by X-ray diffraction analyses. The middle part of this chimney was used for this study.
For enrichment, vials (each with a butyl-rubber stopper and an aluminium cap) with basal medium were used. The basal medium under a N2/CO2 (4 : 1, v/v) atmosphere was composed of the following (l–1): KH2PO4, 0·75 g; K2HPO4, 0·78 g; MgCl2.6H2O, 0·36 g; CaCl2.2H2O, 0·1 g; NH4Cl, 0·54 g; NaHCO3, 5 g; NaCl 30 g; trace-element solution DSM 334 (DSMZ, 1993), 10 ml; vitamin solution DSM 141 (DSMZ, 1993), 10 ml. A fragment of the chimney was incubated at 55–85 °C in the enrichment medium, which was basal medium supplemented with sulfur (10 g l–1) and yeast extract (2 g l–1), and supplied with O2 (N2/CO2/O2, 75 : 20 : 5, by vol.). After a 1-week incubation, growth of micro-organisms was observed at 55 °C; the culture was transferred to fresh enrichment medium several times. A similar enrichment medium solidified with 2 % (w/v) agar was used for isolation. An inoculated agar plate was incubated at 55 °C in a sealed nylon bag with an oxygen-absorbing agent (Anaero Pack Campylo; Mitsubishi Gas Chemical Co.) for microaerophiles. Colourless colonies formed on the agar plate after 4 days incubation; strain St55BT was then isolated. The isolate was generally maintained in basal medium supplied with 2 g yeast extract l–1 and 20 mM sodium nitrate under anaerobic conditions (see below).
Strain St55BT was characterized morphologically as comprising non-motile rods (about 0·5 µm wide and 1·5–2·0 µm long; Fig. 1a, b). Occasionally (at exponential phase under good growth conditions), cells tended to connect to each other forming chain-linked circular structures, called ‘rotund bodies’, that are often observed in some species of the genus Thermus (Brock & Edwards, 1970) and in O. profundus (Miroshnichenko et al., 2003a) (Fig. 1c, d). The isolate had negatively Gram-stained cells with a thick cell-wall structure (Fig. 1b, d). Spore formation and pigmentation were not observed. Oxidase and catalase activities (Tamaki et al., 2003) were positive and weakly positive, respectively. However, when strain St55BT grew anaerobically with nitrate as an electron acceptor (see below), oxidase was not produced.
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) of strain St55BT was determined (AB107956). After alignment with the ARB program (http://www.arb-home.de/), the phylogenetic tree (Fig. 2) was constructed by the neighbour-joining method with the CLUSTAL W program (Saitou & Nei, 1987; Thompson et al., 1994). Strain St55BT was found to be a member of the family Thermaceae in the phylum ‘Deinococcus–Thermus’ and was very close to O. profundus (Miroshnichenko et al., 2003a), with a sequence similarity of 99·5 %.
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) revealed that the isolate could use nitrate (5 mM), nitrite (2·5 mM) and elemental sulfur (10 g l–1) as electron acceptors in place of oxygen. However, it could not grow with the following acceptors: sulfate (5 mM), thiosulfate (5 mM), sulfite (2·5 mM), DMSO (5 mM), fumarate (5 mM), Fe(III) citrate (5 mM) (Heising et al., 1999) and selenate (5 mM). The culture with elemental sulfur showed slow growth, but sulfur certainly supported growth under anaerobic conditions. Miroshnichenko et al. (2002) reported that O. profundus could not use elemental sulfur as an electron acceptor. However, we also observed faint growth of O. profundus in our basal medium supplemented with elemental sulfur (10 g l–1), sucrose (10 mM) and yeast extract (0·1 g l–1). The turbidity of the culture was apparently lower than that of a culture with nitrate or oxygen as an electron acceptor; growth of O. profundus on elemental sulfur was similar to that in strain St55BT. The isolate required a small amount of yeast extract (0·1 g l–1) for growth under any growth conditions. In the presence of 5 mM nitrate and 0·1 g yeast extract l–1, the isolate grew on each of the following as a sole source of energy and carbon: yeast extract (1 g l–1), tryptone (1 g l–1), Casamino acids (1 g l–1), butyrate (20 mM), formate (40 mM), glutamate (20 mM), lactate (20 mM), propionate (20 mM), pyruvate (20 mM), succinate (20 mM), L-alanine (20mm) and L-cysteine (20 mM). The following substrates could not support growth: H2/CO2 (4 : 1, v/v), acetate (40 mM) + H2/CO2 (4 : 1, v/v), arabinose (10 mM), fructose (10 mM), galactose (10 mM), glucose (10 mM), inositol (10 mM), mannose (10 mM), raffinose (10 mM), sucrose (10 mM), xylose (10 mM), acetate (20 and 40 mM), citrate (20 mM), fumarate (20 mM), malate (20 mM), L-arginine (20 mM), L-asparagine (20 mM), L-histidine (20 mM), L-leucine (20 mM), L-methionine (20 mM), L-serine (20 mM), ethanol (20 mM), 2-propanol (20 mM) and methanol (20 mM).
Temperature, pH and NaCl-concentration ranges for growth were determined using 25 ml Hungate tubes containing 10 ml medium (Hattori et al., 2000). The medium contained 2 g yeast extract l–1 as an energy source and 20 mM nitrate as an electron acceptor under N2/CO2 (4 : 1, v/v). The temperature for growth of strain St55BT ranged from 30 to 65 °C, with an optimum at 60 °C. The pH range for growth at 60 °C was 6·0–8·0, with an optimum at pH 6·5. The isolate required NaCl for growth and grew at NaCl concentrations of 1–5 % (w/v), with optimum growth at 3 % (w/v).
Fatty acid methyl ester analysis with a GC/MS system (Hanada et al., 2002) revealed that the main cellular fatty acids of strain St55BT grown at 55 °C were iso-C15 : 0 (48 % of total fatty acids) and anteiso-C15 : 0 (13 %). The strain also contained iso-C15 : 1 (5 %), C16 : 1 (6 %), iso-C16 : 0 (4 %), iso-C17 : 1 (6 %) and two kinds of branched C17 : 0 (18 %) as minor components. All members of the genera Thermus, Meiothermus or Marinithermus contain predominantly iso- and anteiso-branched saturated fatty acids (Da Costa & Rainey, 2001; Sako et al., 2003). The cellular fatty acids of strain St55BT consisted mainly of iso- and anteiso-branched, odd-carbon-numbered fatty acids, like other related species. The closest relative, O. profundus, is known to include significant amounts (33 % of total fatty acids) of unsaturated fatty acids (Miroshnichenko et al., 2003a). While such a high content of unsaturated fatty acids is rarely observed in thermophilic bacteria, our fatty acid methyl ester analysis of O. profundus grown at 55 °C also indicated that the related species clearly contains a large amount of them (approx. 37 %). In our isolate, strain St55BT, unsaturated fatty acids such as iso-C15 : 1, C16 : 1 and iso-C17 : 1 were also detected, but they represented only 18 % of the total cellular fatty acids, equivalent to half that present in O. profundus. The fatty acid methyl ester profile of strain St55BT grown at 45 °C was almost identical to that of cells grown at 55 °C. In general, the unsaturated fatty acid content tends to increase when cells are grown at lower temperatures, but the content in strain St55BT was stable even if it was grown at low temperatures.
MK-8 was detected as the major quinone of strain St55BT by using HPLC (Shintani et al., 2000). Trace amounts of MK-6(H2), MK-7, MK-7(H8) and MK-9 were also detected. The genomic DNA G+C content (Mori et al., 2000) of strain St55BT was 71·1 mol%. The G+C content of the reference species, O. profundus, was 68·6 mol% when measured by the same method, whereas the value reported by Miroshnichenko et al. (2003a) was 62·9 mol%.
Differential characteristics of St55BT are summarized in Table 1 in comparison with those of the most related species, O. profundus (Miroshnichenko et al., 2003a). O. profundus is a thermophilic, microaerophilic micro-organism isolated from a deep-sea hydrothermal vent site in East Pacific Rise. The 16S rRNA gene sequence and also some phenotypic features were very similar to those of strain St55BT. However, strain St55BT clearly differed from O. profundus in the following respects: (i) strain St55BT grew with nitrite as an electron acceptor under anaerobic conditions, unlike O. profundus; (ii) O. profundus utilized various sugars and alcohols, but strain St55BT was unable to use these substrates and preferred complex compounds such as yeast extract, tryptone and Casamino acids; (iii) the genomic DNA G+C content differentiated the isolate (71·1 mol%) from O. profundus (68·9 mol%); (iv) the unsaturated fatty acid content of the isolate (18 %) was clearly lower than that in O. profundus (33–37 %); and (v) the pH for optimum growth of the isolate was slightly acid (pH 6·5).
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) are also shown in Table 1
. The DNA relatedness between strain St55BT and O. profundus was less than 20 %, suggesting strongly that these two organisms should be classified as different species (Wayne et al., 1987). For the reasons described above, we propose strain St55BT as a novel species with the name Oceanithermus desulfurans sp. nov.
A lot of bacteria able to use elemental sulfur in anaerobic respiration that have been isolated, including Caminibacter hydrogeniphilus (Alain et al., 2002a), Nautilia lithotrophica (Miroshnichenko et al., 2002), Desulfurobacterium thermolithotrophum (L'Haridon et al., 1998) and members of the genus Marinitoga (Alain et al., 2002b), are strictly anaerobic sulfur-reducing bacteria that live in deep-sea hydrothermal vents. Persephonella marina (Götz et al., 2002) and some strains in the 
-Proteobacteria (Takai et al., 2003) are facultatively anaerobic bacteria that are capable of reducing elemental sulfur. Members of the genus Oceanithermus can use elemental sulfur as an electron acceptor under anaerobic conditions, and this is the first report of a sulfur-reducer in the family Thermaceae. A shortage of oxygen easily occurs in deep-sea environments where reduced sulfur compounds are supplied constantly. The ability to reduce elemental sulfur is advantageous to Oceanithermus species under such conditions. Oceanithermus species may be significant contributors to the sulfur cycle in deep-sea hydrothermal vents.
Emended description of the genus Oceanithermus Miroshnichenko et al. 2003
Cells are non-motile, Gram-negative rods, and ‘rotund bodies' are observed. Moderately thermophilic. Non-sporulating. Microaerophilic. Growth also occurs by anaerobic respiration with nitrate and elemental sulfur. Some species use nitrite as an electron acceptor. MK-8 is the major respiratory quinone. The major cellular fatty acids are iso- and anteiso-branched types. Unsaturated fatty acids were also detected (18–37 %). The genomic DNA G+C content is 62·9–71·1 mol%. The phylogenetic position, based on 16S rRNA gene sequences, is in the family Thermaceae. The type species is Oceanithermus profundus.
Description of Oceanithermus desulfurans sp. nov.
Oceanithermus desulfurans (de.sul'fu.rans. N.L. part. adj. desulfurans making free of/reducing sulfur).
Cells are rods, about 0·5 µm wide and 1·5–2·0 µm long, and ‘rotund bodies' are observed under good growth conditions. Gram reaction is negative. Non-motile, non-pigmented and non-sporulating. Chemoheterotrophic. Microaerophilic and facultatively anaerophilic. Anaerobic growth occurs in the presence of elemental sulfur, nitrate or nitrite as an electron acceptor, but sulfate, thiosulfate, sulfite, DMSO, fumarate, Fe(III) citrate and selenate do not support growth. Yeast extract is necessary for growth. Yeast extract, tryptone, Casamino acids, butyrate, formate, glutamate, lactate, propionate, pyruvate, succinate, L-alanine and L-cysteine are used as carbon and energy sources. No growth occurs with H2/CO2, acetate + H2/CO2, arabinose, fructose, galactose, glucose, inositol, mannose, raffinose, sucrose, xylose, acetate, citrate, fumarate, malate, L-arginine, L-asparagine, L-histidine, L-leucine, L-methionine, L-serine, ethanol, 2-propanol or methanol. Grows at 30–65 °C; optimum growth is at 60 °C. The pH range for growth is 6·0–8·0, with optimum growth at pH 6·5. Growth occurs at 1–5 % (w/v) NaCl and the optimum growth concentration is 3 % (w/v). MK-8 is the major quinone. The major cellular fatty acid is iso-C15 : 0. Unsaturated fatty acids (18 %) are also present. The genomic DNA G+C content is 71·1 mol%.
The type strain is St55BT (=NBRC 100063T=DSM 15757T), isolated from a chimney in the Suiyo Seamount (at a depth of 1390 m) in the Izu-Bonin Arc, Western Pacific.
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ACKNOWLEDGEMENTS |
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