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1 Institute of Microbiology, Russian Academy of Sciences, Prospect 60-letiya Oktyabrya 7/2, 117811 Moscow, Russia
2 UMR 6539, Centre National de la Recherche Scientifique & Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer, 29280 Plouzané, France
3 A. N. Bach Institute of Biochemistry, Russian Academy of Sciences, Leninsky Prospect 33, 119071 Moscow, Russia
4 DSMZ – German Collection of Microorganisms and Cell Cultures, Mascheroder Weg 1b, 38124 Braunschweig, Germany
Correspondence
M. L. Miroshnichenko
alfamirr{at}mail.ru
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain TRT is AJ507298.
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). Many have been isolated from terrestrial freshwater environments, although some Thermus strains originated from shallow-water hot springs (da Costa & Rainey, 2001). However, a strain of Thermus thermophilus was isolated from a deep-sea vent at Guaymas Basin (Marteinsson et al., 1999), confirming the presence of thermophilic aerobes in the hydrothermal environment (Marteinsson et al., 1995). All representatives of the family Thermaceae isolated to date from shallow-water hot vents are halotolerant, growing optimally in the absence of NaCl (da Costa & Rainey, 2001). The only obligately marine representatives of this group, Marinithermus hydrothermalis (Sako et al., 2003) and Oceanithermus profundus (Miroshnichenko et al., 2003b), were isolated very recently from the deep-sea hydrothermal environment. In this paper, we describe a novel member of the family Thermaceae, recovered from an in situ collector deployed on a hydrothermal vent of the Mid-Atlantic Ridge, that is also obligately dependent on a salinity equivalent to that of sea water.
An in situ growth chamber or vent cap (Reysenbach et al., 2000) designed to concentrate the micro-organisms discharged by hydrothermal emissions was deployed in May 2001 on the Mid-Atlantic Ridge (36°16'N, 33°54'W) by the remote-operated vehicle (ROV) Victor during the Iris cruise. After in situ incubation, the vent cap was closed by the hydraulic arm of the ROV before transportation to the surface. Once on board, the content (aquarium filtering wool and liquid) was removed aseptically, immediately transferred to 50-ml glass vials and flooded with a sterile solution of 3 % (w/v) sea salts (Sigma). The vials were then closed tightly with butyl rubber stoppers (Bellco), pressurised with N2 (100 kPa), reduced with sodium sulphide and stored at 4 °C until processed further.
Enrichment medium (EM) contained (g l-1 unless indicated): NH4Cl, 0·33; KCl, 0·33; KH2PO4, 0·33; CaCl2.2H2O, 0·33; MgCl2.6H2O, 0·33; NaCl, 25·0; NaNO3, 3·0, yeast extract, 0·1; trace elements (Balch et al., 1979), 10 ml; and vitamins (Wolin et al., 1963), 10 ml. The medium was prepared anaerobically (Balch et al., 1979) and dispensed in Bellco tubes; the headspace (25 ml) was filled with H2/CO2 (80 : 20, overpressure of 2 atm). No reducing agents were added to the medium. The pH of the medium was 6·5. Single colonies were isolated by using a serial tenfold dilution technique in agar shake tubes with the same medium solidified with 1·5 % agar (Difco) and supplemented with sodium acetate (1 g l-1). The gas phase in this case was replaced by N2 (100 %). Agar shake tubes were incubated at 60 °C for 5 days. The morphology of the novel isolate was examined using an Olympus BX-60 microscope. The ultrastructure of whole cells and thin sections was studied as described elsewhere (Bonch-Osmolovskaya et al., 1990). Physiological studies of the novel isolate were carried out using medium GM, containing (g l-1): NaCl, 30; yeast extract, 0·5; tryptone, 1; sucrose, 2; and KNO3, 1. MOPS (10 mM) was used as buffer. The pH of the medium was adjusted with 5 M NaOH before autoclaving. The medium was prepared anaerobically but without any reducing agent. Potential proteinaceous growth substrates were added at a concentration of 1 g l-1, carbohydrates, sodium salts of organic acids and alcohols at a concentration of 3 g l-1. When molecular hydrogen served as a substrate, the headspace (10 ml) was filled with a H2/CO2 mixture (80 : 20, v/v). To determine the influence of oxygen on growth, oxygen was added at concentrations from 0·5 to 21 % to the headspace (25 ml) of Bellco tubes filled with GM medium (5 ml) from which KNO3 was omitted. Possible electron acceptors (thiosulphate, sulphate or nitrite) were added in medium GM without KNO3 at a concentration of 0·2 %. Elemental sulphur (10 g l-1) was also tested as a possible electron acceptor. Oxidase activity was assayed using disks impregnated with dimethyl-p-phenylene diamine (bioMérieux). Catalase activity was assayed by mixing a pellet of a fresh culture with a drop of hydrogen peroxide (10 %, v/v). All experiments were performed in triplicate.
The pH range for growth was determined in BM medium supplemented with 2 g sucrose and 2 g sodium nitrate l-1 using various buffers at a concentration of 10 mM (MES for pH 5·0–6·0, PIPES for pH 6·5 and 7·0, HEPES for pH 7·5, Tris for pH 8·0 and 8·5). Appropriate amounts of 1 M Na2CO3 were added to adjust the pH of the medium to 9·0 and 9·5. pH values were determined at room temperature. To determine the optimum NaCl range for growth, NaCl concentrations were varied while maintaining the concentrations of other inorganic components. The effects of different pH values and concentrations of NaCl were determined at 60 °C. Growth was monitored by measuring the increase in OD600 using a Spectronic 401 spectrophotometer (Bioblock). Gaseous and liquid fermentation products were detected by GLC (Miroshnichenko et al., 1994). Gaseous and liquid products of nitrate reduction were studied as described elsewhere (Miroshnichenko et al., 2003a). Respiratory quinones and polar lipids were extracted and analysed as described previously (Tindall, 1990a, b). Fatty acids were extracted and analysed as methyl esters as described previously. The presence of unsaturation was confirmed by hydrogenation (Brian & Gardner, 1968) and the position of unsaturation was located by the formation of dimethyl disulphide (DMDS) adducts using the method of Nichols et al. (1986) and the instrumentation and conditions described previously (Strömpl et al., 1999). DNA was isolated after disruption of cells using a French pressure cell (Thermo Spectronic) and purified by hydroxyapatite chromatography (Cashion et al., 1977). The DNA was hydrolysed with P1 nuclease and nucleotides were dephosphorylated with bovine alkaline phosphatase (Mesbah et al., 1989). The resulting deoxyribonucleosides were analysed by HPLC as described by Tamaoka & Komagata (1984). Genomic DNA extraction, PCR-mediated amplification of the 16S rDNA and sequencing of PCR products were carried out as described by Rainey et al. (1996). Phylogenetic analysis followed the methods of Miroshnichenko et al. (2003a).
After deployment on the Rainbow vent site, the aquarium filtering wool within the vent cap was heavily coated with very fine black sulphide particles. This material was used for inoculating the EM medium. The tubes were incubated at 60 °C. After 3 days, the enrichment produced abundant growth of morphologically different rod-shaped micro-organisms. After several successive transfers of the enrichment culture, the gas phase was replaced with N2 and acetate was added as a substrate. Stable growth of large, non-motile rods was obtained on this medium. This culture was serially diluted and the highest dilutions were transferred to the same medium solidified with agar. After 5 days of incubation at 60 °C, round, slightly creamy colonies appeared. Single colonies (0·3–1 mm in diameter) from the last dilution were transferred into the same medium without agar. The purification procedure was repeated twice before the culture was considered to be pure. Purity was confirmed by microscopic examination of the culture after growth on a test medium containing glucose (3 g l-1), pyruvate (3 g l-1) and yeast extract (3 g l-1). The isolated strain was designated TRT.
Cells of strain TRT were non-motile rods, 0·5–0·7 µm in diameter and variable in length (Fig. 1a). Flagella, spores and ‘rotund bodies’, which are typical of the majority of members of the family Thermaceae (Brock & Edwards, 1970), were never observed. Thin-section electron preparations revealed a Gram-negative structure of cell wall with a ‘cobblestone’ outer layer, consistent with that of representatives of the family Thermaceae (da Costa & Rainey, 2001) (Fig. 1b). The isolate was able to grow at oxygen concentrations from 0·5 to 21 %. Oxygen concentrations that promoted fastest growth ranged from 4 to 8 % under agitation. However, the growth yield was two to three times higher when the strain was cultivated with 12–16 % oxygen. A long lag phase (20 h) was observed when air was applied as headspace. The novel isolate was able to grow anaerobically in the presence of nitrate serving as electron acceptor. Strain TRT grew within a temperature range of 37–80 °C, with an optimum at 70 °C. At 70 °C, it grew between pH 5·5 and 8·4, with an optimum around 6·7. Strain TRT required NaCl for growth and grew at NaCl concentrations ranging from 1 to 5 % with an optimum at 3 %. Strain TRT was able to utilize a wide spectrum of carbohydrates in the presence of both nitrate and oxygen. It grew well on media containing complex proteinaceous substrates (tryptone, yeast extract, bio-trypticase and Bactopeptone) and sugars (fructose, maltose, sucrose, trehalose, galactose, arabinose and xylose). It also utilized glucose, lactose, starch and maltodextran, but growth was lower with these substrates. No fermentation products were detected during growth of the novel isolate with sucrose and nitrate. It was able to utilize acetate, pyruvate, succinate, fumarate and butyrate as growth substrates. It also grew with methanol, ethanol, propanol and mannitol. The novel isolate did not grow with casein, malate, lactate, propionate or cellobiose. Strain TRT was able to grow lithoheterotrophically (100 mg yeast extract l-1 was necessary) using molecular hydrogen as an energy source and nitrate or oxygen as electron acceptors. Nitrate, when present, was reduced to nitrite, which was the only product of denitrification. Other possible products of nitrate reduction (
, N2, NO, N2O) were not detected. Other electron acceptors (sulphate, elemental sulphur, thiosulphate, nitrite) did not support growth, regardless of the growth substrate.
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). The combination of GLC-MS on the underivatized fatty acids and the DMDS adducts does not allow unambiguous identification of either the position of the cyclopropane rings or the position of branching. However, cyclopropane rings are generally derived from unsaturated fatty acids in which the aliphatic backbone has the same number of carbon atoms. One may, therefore, speculate that the cyclopropane-containing fatty acids are iso-branched, although further work is needed to confirm this. The polar lipid pattern was fairly simple, comprising both phospholipids and glycolipids (Fig. 2). The major phospholipid had an Rf value identical to that of the major phospholipid present in members of the genera Oceanithermus, Thermus and Meiothermus, whereas the major glycolipid had an Rf value close, but not identical, to that of the major glycolipid of Thermus aquaticus DSM 625T (data not shown).
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; Chung et al., 1997; Sako et al., 2003; Miroshnichenko et al., 2003b). The presence of iso- and anteiso-branched fatty acids is a feature of members of these genera and also Deinococcus (Embley et al., 1987; Ferreira et al., 1997; Donato et al., 1990, 1991; Sako et al., 2003; Miroshnichenko et al., 2003b). However, in contrast to members of the genera Marinithermus, Thermus and Meiothermus described to date, strain TRT produces significant amounts of iso-unsaturated fatty acids. The fatty acid composition of Oceanithermus profundus shows similar trends to that of strain TRT; however, branched-chain and cyclopropane-ring-containing compounds were detected only in strain TRT. Members of the genera Thermus and Meiothermus described to date produce both phospholipids and glycolipids (Donato et al., 1990, 1991). Although members of the genus Deinococcus may also produce glycolipids, in addition to a novel series of phosphoglycolipids (Embley et al., 1987; Ferreira et al., 1997), the latter are absent from members of the genera Thermus and Meiothermus. Strain TRT produced a glycolipid with an Rf value similar to that of the compound detected in T. aquaticus, its presence distinguishing strain TRT from members of the genera Meiothermus and Oceanithermus. The presence of the same major phospholipid (based on TLC studies) in strain TRT and members of the genera Oceanithermus, Thermus and Meiothermus is also consistent with results from 16S rDNA sequence data. Taken together, the presence of MK-8, the occurrence of phospholipids and glycolipids similar to those found in T. aquaticus and the presence of both saturated and unsaturated iso- and anteiso-branched fatty acids are indicative of the unique chemical composition of strain TRT and may serve to distinguish it for all other genera in the family Thermaceae. The DNA base composition of strain TRT was 68·4 mol% G+C.
Phylogenetically, strain TRT was a member of the phylum Deinococcus–Thermus of the Bacteria. Similarity values of the 16S rRNA gene sequence of this strain to those of the representatives of other genera in this phylum were below 90 %, illustrating the isolated position of the novel isolate. In phylogenetic trees, strain TRT forms a separate branch at the root of the family Thermaceae (Fig. 3). While membership of the phylum is supported by high bootstrap values, there was no indication of a close relationship to any of the existing genera of the family Thermaceae.
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, 1996, 1999; Sako et al., 2003, Miroshnichenko et al., 2003b). Such niches might occur in narrow zones with moderate temperatures, where hot, reduced fluid interacts with cold, oxygenated oceanic waters (Marteinsson et al., 1995). Such an environment, where sharp oxygen gradients with tremendous temporal and spatial variability occur, may facilitate colonization by organisms able to thrive in more than one type of chemical environment. Phylogenetically distinct thermophilic bacteria able to grow in both microaerobic and anaerobic conditions have recently been isolated from deep-sea hydrothermal systems. These are two lithoautotrophic thermophilic species of a new genus Persephonella (Götz et al., 2002) and Oceanithermus profundus, a species of a new genus of the family Thermaceae also capable of chemolithotrophy (Miroshnichenko et al., 2003b). Strain TRT is an additional deep-sea hydrothermal vent representative, capable of nutritional versatility. Phylogenetically, strain TRT belongs to the family Thermaceae, sharing many common features with its members. Within this family, Oceanithermus profundus exhibits some features similar to those of the novel isolate: ability to grow microaerobically, ability to grow lithoheterotrophically with molecular hydrogen, obligate requirement for NaCl and capacity for anaerobic respiration in the presence of nitrate. However, strain TRT differs from it by its higher temperature of growth, the ability to grow under air and chemical composition. Based on phenotypic and genomic differences and the distinct phylogenetic position of isolate TRT, we propose a new genus, Vulcanithermus gen. nov., with the type species Vulcanithermus mediatlanticus sp. nov.
Description of Vulcanithermus gen. nov.
Vulcanithermus (Vul.ca.ni.ther'mus. L. n. Vulcanus the Roman god of fire; Gr. adj. thermos hot; N.L. masc. n. Vulcanithermus heat-loving organism, living in the vicinity of volcanic areas).
Cells are non-motile, Gram-negative rods, 0·5–0·7 µm in diameter and variable in length. Moderately thermophilic. Neutrophilic. Adapted to the salinity of sea water. Microaerophilic. Capable of aerobic growth. Able to utilize a broad range of carbohydrates, some proteinaceous substrates, organic acids and alcohols. Capable of anaerobic growth with nitrate, which is reduced to nitrite. Capable of chemolithoheterotrophic growth with molecular hydrogen. Sole respiratory lipoquinones present are menaquinones, with MK-8 predominating. Fatty acids are iso- and anteiso-branched, with unsaturated iso-branched fatty acids also present, as are branched-chain cyclopropane fatty acids. Phospholipids and glycolipids are the only polar lipids present. The major phospholipid present has an Rf identical to that of the major phospholipid present in Thermus and Meiothermus species, while the major glycolipid has an Rf value close, but not identical, to that of the major glycolipid present in T. aquaticus. The G+C content of the DNA of the type species is 68·4 mol%. 16S rDNA sequence analysis places Vulcanithermus in the family Thermaceae. The type species is Vulcanithermus mediatlanticus.
Description of Vulcanithermus mediatlanticus sp. nov.
Vulcanithermus mediatlanticus (me.di.at.lan'ti.cus. L. adj. medius middle; L. masc. adj. atlanticus Atlantic; N.L. adj. mediatlanticus from the middle of the Atlantic).
Displays the following properties in addition to those given in the genus description. Optimal growth temperature is 70 °C. The optimal pH is around 6·7. The optimum salinity is 3 % NaCl. The chemical composition of the species is identical to that of the genus. The G+C content of the DNA of the type strain is 68·4 mol%. The type strain, TRT (=DSM 14978T =VKM B-2292T =JCM 11956T), was isolated from the Rainbow deep-sea hydrothermal vent field on the Mid-Atlantic Ridge.
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ACKNOWLEDGEMENTS |
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da Costa, M. S. & Rainey, F. A. (2001). Family I. Thermaceae fam. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, pp. 403–404. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springer.
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-naphthol-positive and slowly periodate–Schiff-positive). The structures of these polar lipids are currently not known, but PL3 has an Rf identical to that of the major phospholipid of Oceanithermus, Thermus and Meiothermus species (see text for discussion).