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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 and 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 accession number for the 16S rRNA gene sequence of strain 506T is AJ430586.
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), but representatives of this group have been found in many natural and artificial thermal habitats (Williams & Da Costa, 1992). At the time of writing, the genus Thermus is represented by eight species with high optimal growth temperatures (65–75 °C), while four species with lower temperature optima (50–65 °C) are classified in the genus Meiothermus (Nobre et al., 1996). A new genus, Marinithermus, has recently been described; its unique representative, Marinithermus hydrothermalis, isolated from a deep-sea hydrothermal vent, thrives between 50 and 72·5 °C (optimum 67·5 °C) (Sako et al., 2003). Most strains of the family Thermaceae are organotrophs, though the ability to grow lithotrophically with sulfur compounds was reported for Thermus scotoductus (Skirnisdottir et al., 2001). Some strains are also able to grow anaerobically with nitrate or nitrite as the terminal electron acceptor (Da Costa & Rainey, 2001). In this paper, we report the isolation, from a deep-sea hydrothermal vent, of a novel microaerophilic representative of the family Thermaceae that is capable of lithotrophic and organotrophic growth.
Samples were collected during the Amistad cruise (1999) at the 13°N hydrothermal vent field (12°48'N, 103°56'W) on the East Pacific Rise at a depth of 2600 m. Samples of hydrothermal fluids and chimneys were transferred in tightly stoppered 50 ml plastic tubes and stored at 4 °C. The enrichment medium contained the following (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, sodium acetate, 3·0, yeast extract, 0·1; NaHCO3, 0·5; trace elements (Balch et al., 1979), 10 ml l-1; vitamins (Wolin et al., 1963), 10 ml l-1. The medium was prepared anaerobically (Balch et al., 1979) and dispensed into 15 ml Hungate tubes; the headspace (5 ml) was filled with N2 (atmospheric pressure). No reducing agents were added to the medium. The pH of the medium was 6·5. Single colonies were isolated using the same medium solidified with 1·5 % agar (Difco) by using a serial 10-fold dilution technique in agar shake tubes. Agar shake tubes were incubated at 60 °C for 5 days. The morphology of the novel isolate was examined using a light microscope (Mikmed-1 model; LOMO). The ultrastructure of whole cells and thin sections was studied as described elsewhere (Bonch-Osmolovskaya et al., 1990). Oxidase activity was assayed with discs impregnated with dimethyl p-phenylenediamine (bioMérieux). Catalase activity was assayed by mixing a pellet of a freshly centrifuged culture with a drop of hydrogen peroxide (10 %, v/v). Physiological tests were performed in BM medium, which consisted of enrichment medium from which the sodium acetate and sodium nitrate had been omitted. Potential proteinaceous growth substrates were added to the BM medium at a concentration of 1 g l-1; carbohydrates, sodium salts of organic acids and alcohols were present at a concentration of 3 g l-1. When molecular hydrogen served as the substrate, the headspace (10 ml) was filled with a H2/CO2 mixture (4 : 1, v/v). Possible electron acceptors were added at a concentration of 2 g l-1. All experiments were performed in triplicate.
To determine the ability to grow microaerophilically, air was added to the headspace (10 ml) of tubes filled with BM medium (5 ml). The final oxygen concentration was varied from 0·5 to 9 %. The ability to grow aerobically was determined either on plates with agarized BM medium (2 % agar; Difco) supplemented with sucrose (2 g l-1) and tryptone (1 g l-1) or in 100 ml flasks containing the same medium (10 ml). Growth was monitored by measuring the increase in OD600 by using a Spectronic 401 spectrophotometer (Bioblock). All growth experiments were performed in duplicate using Bellco tubes under microaerophilic conditions. 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 (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) at a concentration of 10 mM. Appropriate amounts of 1 M Na2CO3 were added to adjust the pH of the medium to 9·0 and 9·5. The pH was determined at room temperature. To determine the optimum NaCl range for growth, NaCl concentrations were varied while the concentrations of the other inorganic components were maintained. The effects of different pH values and concentrations of NaCl were determined at 60 °C. Gaseous and liquid fermentation products were detected by means of GLC (Miroshnichenko et al., 1994). Gaseous and liquid products of nitrate reduction were studied as described elsewhere (Miroshnichenko et al., 2003). 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 disulfide 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 the 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). Purified PCR products were sequenced directly using a Taq Dye-Deoxy Terminator cycle sequencing kit (Applied Biosystems) according to the manufacturer's instructions. An Applied Biosystems 310 DNA Genetic Analyzer was used for electrophoresis of sequence reaction products. The 16S rDNA sequence of strain 506T was aligned manually with nucleotide sequences obtained from the GenBank and EMBL databases. The method of Jukes & Cantor (1969) was applied to calculate evolutionary distances. Phylogenetic trees were constructed using the methods of DeSoete (1983) and Felsenstein (1993).
Twelve samples from hydrothermal vents containing water and chimney material were used for the inoculation of enrichment medium (5 %, v/v) and incubated at 60 °C. After 5 days incubation, samples of the inner and outer chimney part from the ‘Genesis' site produced abundant growth of morphologically homogeneous micro-organisms. After several successive transfers, the enrichment culture was serially diluted and the highest dilutions were transferred to the same medium solidified with agar. After 5 days incubation at 60 °C, single colonies appeared. Colonies were spherical and non-pigmented, with diameters ranging from 0·3 to 1 mm. A single colony from the last dilution was transferred into liquid enrichment medium. The purification procedure was repeated twice, after which the culture was considered to be pure. Purity was confirmed by microscopic examination of the culture growing on medium containing glucose (3 g l-1), pyruvate (3 g l-1) and yeast extract (3 g l-1). The purified micro-organism was designated as strain 506T.
Cells of strain 506T were non-motile rods, 0·5–0·7 µm in diameter and of various lengths. On negatively stained electron microscope preparations, small spheres were often seen along the cell wall and between the cells (Fig. 1a). Flagella were never observed. When grown on proteinaceous substrates, old cultures of strain 506T formed filaments and large spheres (Fig. 1c) resembling the ‘rotund bodies' typical of aged cells of Thermus species (Brock & Edwards, 1970). Thin-section electron micrographic preparations revealed a Gram-negative cell wall structure. The cell wall had a complex multilayered structure with a characteristic corrugated outer layer (Fig. 1b). Spores were never observed. The isolate was microaerophilic, only being able to grow at oxygen concentrations below 6 %. No growth was observed in an atmosphere of air, either in liquid medium or on plates. In an agar tube (containing 5 ml BM medium supplemented with 2 g sucrose and 1 g tryptone l-1) with air in the headspace (10 ml), growth occurred only in a zone located 20 mm below the agar/air interface. Alternatively, strain 506T grew anaerobically using nitrate as the electron acceptor. Strain 506T grew within a temperature range of 40–68 °C, optimal growth being observed at 60 °C. At 60 °C, it grew between pH 5·5 and 8·4, with an optimum around 7·5. Strain 506T required NaCl for growth and grew at NaCl concentrations ranging from 10 to 50 g l-1, with an optimum at 30 g l-1. Strain 506T was oxidase- and catalase-positive. It was able to utilize a wide spectrum of carbohydrates in the presence of either nitrate or oxygen. The highest cell yield was observed in the presence of nitrate with fructose, maltose, sucrose, trehalose, galactose, rhamnose or xylose. It also utilized glucose, lactose and starch, but did not grow with ribose, galactose, arabinose, dextrin or cellobiose. Acetate and propionate were produced during growth with sucrose as a growth substrate and nitrate as the electron acceptor. Nitrite was the only product of denitrification. Strain 506T grew well with complex proteinaceous substrates such as beef extract, tryptone or papaic digest of soybean (1–1·5 g l-1). However, growth was strongly inhibited by higher concentrations of these substrates. The isolate did not grow with Casamino acids or yeast extract as sole sources of carbon and energy, though 100 mg yeast extract l-1 was required for growth. Strain 506T was able to utilize acetate, pyruvate and propionate as growth substrates. It also grew with methanol, ethanol and mannitol, though the cell yield was lower. Strain 506T was able to grow lithoheterotrophically using molecular hydrogen as the energy source, yeast extract as the carbon source and nitrate as the electron acceptor. Other electron acceptors (sulfate, elemental sulfur, thiosulfate, nitrite) did not support growth, regardless of growth substrate.
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). The polar lipid pattern was fairly simple, comprising only phospholipids; glycolipids were not detected (Fig. 2). The major phospholipid had an Rf value identical to that of the major phospholipid present in members of the genera Thermus and Meiothermus. The presence of MK-8 as the predominant respiratory quinone is consistent with reports of MK-8 in members of the genera Thermus, Meiothermus (Hensel et al., 1986; Chung et al., 1997) and Marinithermus (Sako et al., 2003). MK-8 is also the dominant respiratory lipoquinone present in members of the genus Deinococcus (Embley et al., 1987; Ferreira et al., 1997). However, the presence of MK-9, albeit at only 5 %, appears to be a unique feature of the novel isolate in comparison with the genera Deinococcus, Thermus and Meiothermus. MK-9 was not reported in Marinithermus hydrothermalis (Sako et al., 2003). The presence of iso- and anteiso-branched fatty acids is a feature of members of the genera Deinococcus, Thermus, Meiothermus and Marinithermus (Embley et al., 1987; Ferreira et al., 1997; Donato et al., 1990, 1991; Sato et al., 2003). However, members of the genera Thermus, Meiothermus and Marinithermus described to date do not produce significant amounts of iso-unsaturated fatty acids, as strain 506T does. In contrast, members of the genus Deinococcus produce a number of isomers of iso-unsaturated fatty acids, although their distribution may differ between species. 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 in members of the genera Thermus and Meiothermus. Strain 506T does not produce glycolipids in significant proportions, which makes it clearly distinguishable from members of the genera Thermus and Meiothermus. No information on phosphoglycolipids or glycolipids is available for Marinithermus hydrothermalis. The presence of the same major phospholipid (according to TLC studies) in strain 506T and members of the genera Thermus and Meiothermus is also consistent with the 16S rDNA sequence data. However, the absence of glycolipids strengthens the case for placing the novel strain in a new genus.
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). In neither dendrogram did strain 506T branch within the radiation of either Thermus or Meiothermus. Only low bootstrap values were found for the branching point of strain 506T in each of the phylogenetic patterns obtained.
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Phylogenetic analysis placed isolate 506T in the family Thermaceae. Indeed, it shares common phenotypic features with members of this family, including the characteristic cell wall structure, with a ‘cobblestone’ outer layer, the formation of ‘rotund bodies’, the possession of catalase and oxidase activities and the ability to grow anaerobically in the presence of nitrate, reducing it to nitrite. However, in contrast to all members of this group, strain 506T, being microaerophilic, is not able to grow with oxygen at atmospheric pressure. It exhibits the ability to utilize a broader range of carbohydrates, organic acids and alcohols. Another significant characteristic of the metabolism of the novel isolate is its ability to grow lithoorganotrophically with molecular hydrogen as the electron donor. On the basis of the phenotypic and genomic differences and the distinct phylogenetic position of isolate 506T, we propose a new genus, Oceanithermus gen. nov., with Oceanithermus profundus gen. nov., sp. nov. as the type species.
Description of Oceanithermus gen. nov.
Oceanithermus gen. nov. (O.ce.a.ni.ther'mus. L. n. oceanus the ocean; Gr. fem. n. therme heat; N.L. masc. n. Oceanithermus warmth-loving organism living in the ocean).
Cells are non-motile, Gram-negative rods, 0·5–0·7 µm in diameter and of variable length. Moderate thermophile. Neutrophile. Adapted to the salinity of sea water. Microaerophile. Flagella and spores are not observed. 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; MK-9 may account for about 5 % of the total. Fatty acids are iso- and anteiso-branched; unsaturated iso-branched fatty acids are also present. Phospholipids 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. The G+C content of the DNA of the type strain of the type species is 62·9 mol%. 16S rDNA analysis places Oceanithermus in the family Thermaceae. The type species is Oceanithermus profundus.
Description of Oceanithermus profundus sp. nov.
Oceanithermus profundus (pro.fun'dus. L. gen. n. profundus of the abyss, the depths of the ocean).
Displays the following properties in addition to those given in the genus description. Filaments and ‘rotund bodies' are formed by old cells grown on proteinaceous substrates. The optimal growth temperature is 60 °C. The optimal pH is 7·5 and the optimum salinity is 30 g l-1. Oxidase- and catalase-positive. Oxidizes carbohydrates, starch, peptides, organic acids and alcohols. 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 62·9 mol%. The type strain, strain 506T (=DSM 14977T=VKM B-2274T), was isolated from a deep-sea hydrothermal vent of the East Pacific Rise.
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ACKNOWLEDGEMENTS |
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