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1 Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Marine Science & Technology Center, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
2 The DEEPSTAR Group, Frontier Research System for Extremophiles, Japan Marine Science & Technology Center, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
3 Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, USA
4 NASA Jet Propulsion Laboratory, 4800 Oak Grove Drive, Pasadena, CA 91109-8099, USA
Correspondence
Ken Takai
kent{at}jamstec.go.jp
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ABSTRACT |
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Published online ahead of print on 25 October 2002 as DOI 10.1099/ijs.0.02506-0.
The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of Sulfurihydrogenibium subterraneum HGMK1T is AB071324.
Growth curves showing the effects of temperature, pH and sea-salt concentration on growth of Sulfurihydrogenibium subterraneum are available as supplementary material in IJSEM Online.
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; Reysenbach et al., 1994, 2000a), Iceland (Skirnisdottir et al., 2000; Takacs et al., 2001) and Japan (Yamamoto et al., 1998), in subterranean hot springs (Marteinsson et al., 2001) and even in deep-sea hydrothermal vent systems (Reysenbach et al., 2000b). These phylotypes form a clade, probably corresponding to a novel family, that is separate from the Hydrogenobaculum–Aquifex–Hydrogenobacter–Thermocrinis lineage (family Aquificaceae) within the order Aquificales (Takai et al., 2002). Due to their resistance to cultivation, the physiological properties and ecological impacts of these novel phylotypes of Aquificales have been poorly understood.
Recently, Reysenbach et al. (2000c) have for the first time succeeded in isolating previously uncultivated phylotypes of hydrogen-oxidizing, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent site in the East Pacific Rise (EPR) and subsequently found its relatives in other mid-ocean ridge deep-sea hydrothermal systems such as the Guaymas Basin (Götz et al., 2002) and the Central Indian Ridge (Van Dover et al., 2001). Another novel hydrogen-oxidizing thermophile associated with this phylogenetic group was obtained from a shallow marine hydrothermal vent in Vulcano, Italy (Stöhr et al., 2001). Very recently, previously uncultivated phylotypes of Aquificales that had been frequently detected in terrestrial geothermal environments were finally isolated from subsurface hot aquifer water in a Japanese gold mine (Takai et al., 2002). Based on these findings, it is becoming evident that the physiological and metabolic characteristics of this novel lineage of the Aquificales are, for the most part, similar to those of the members of the Aquificaceae, despite clearly separate phylogenetic relationships between them. This report describes a polyphasic taxonomic study carried out on strain HGMK1T, which was isolated recently from subsurface hot aquifer water in a Japanese gold mine. A novel species and genus, Sulfurihydrogenibium subterraneum, is proposed.
Strain HGMK1T was isolated from subsurface hot aquifer water (temperature 70·4 °C; pH 6·25) in the Hishikari gold mine, Kagoshima Prefecture, Japan (Takai et al., 2002). After successful enrichment with mjANHOX medium as described previously (Takai et al., 2002), strain HGMK1T was obtained as a pure culture using the dilution-to-extinction technique (Takai & Horikoshi, 2000). The 16S rRNA gene sequence of the isolate was determined as described previously (Takai et al., 2002) and subjected to sequence similarity analysis against the prokaryotic SSU rRNA database and the non-redundant nucleotide sequence databases of GenBank, EMBL and DDBJ using gapped-BLAST (Altschul et al., 1997; Benson et al., 1998). The sequence was then aligned manually to prokaryotic SSU rDNA data from the Ribosomal Data Project II (Maidak et al., 2000) and the phylogenetic tree was reconstructed as previously described (Takai et al., 2002).
The 16S rRNA gene sequence of the isolate was identical to the partial sequence of the environmental rDNA clone pHAuB-D, recovered from the same hot aquifer water in a culture-independent molecular survey (Takai et al., 2002). The most similar rDNA sequences were those from the environmental clones SRI-40 (97·5 %) (Skirnisdottir et al., 2000) and NAK-14 (97·5 %) (Yamamoto et al., 1998), respectively obtained from Icelandic and Japanese hot spring microbial mats (Fig. 1), and from the cultivated strains Persephonella guaymasensis EX-H2T (91·1 %) and Persephonella marina EX-H1T (90·6 %) (Götz et al., 2002) (Fig. 1). This low phylogenetic relatedness to identified bacteria was just within the common index of 16S rDNA sequence similarity for genus-level differentiation (90–96 %) (Gillis et al., 2001). Phylogenetic analysis indicated that the isolate represented a distinct branch, probably corresponding to a new genus, distantly related to a cluster of Persephonella strains (Fig. 1).
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). The cells are motile, Gram-negative rods, approximately 1·5–2·5 µm long and 0·3–0·5 µm wide, with a polar flagellum. The cells occur singly in the exponential and stationary growth phases. Transmission electron microscopic observation of negatively stained cells revealed that the cellular surface was covered with a wavy structure often observed in Aquificales strains (Reysenbach et al., 1994; Takai et al., 2001).
Strain HGMK1T is a strict chemolithoautotroph capable of growth solely with molecular hydrogen, thiosulfate or elemental sulfur as an electron donor and carbon dioxide as a carbon source (Takai et al., 2002). Other reduced sulfur compounds such as sulfide and cysteine hydrochloride did not serve as electron donors. None of the complex organic substrates (yeast extract, peptone, tryptone, Casamino acid and starch), amino acids, carbohydrates or organic acids tested either supported or improved growth of the isolate. When either hydrogen or thiosulfate was used as an electron donor, the isolate was able to utilize molecular oxygen, nitrate, soluble (ferric citrate) and insoluble (ferrihydrite) iron (III), arsenate, selenate and selenite as electron acceptors. Nitrite, manganese (IV), arsenite, sulfite, sulfate and fumarate were unable to support growth as potential electron acceptors. Strain HGMK1T grew at about 40–70 °C, showing optimal growth at 65 °C; the doubling time at 65 °C and pH 7·5 was about 80 min. No growth was observed at 35 or 75 °C. Growth at 65 °C occurred between pH 6·4 and 8·8, with optimum growth at about pH 7·5 and over the concentration range of sea salts of 0–48 g l-1, with optimum growth at 4·8 g sea salts l-1 at pH 7·5. Details of the experiments used to determine the growth properties of the novel isolate were reported previously (Takai et al., 2002); growth curves showing the effects of temperature, pH and sea-salt concentration on strain HGMK1T are available as supplementary material in IJSEM Online.
The cellular fatty acid composition was analysed using cells grown in mjANHOX medium at 65 °C in the late-exponential growth phase. Lyophilized cells (300 mg) were placed in a Teflon-lined, screw-capped tube containing 5 ml anhydrous methanolic HCl and heated to 100 °C for 3 h. The resulting fatty acid methyl esters (FAMEs) were extracted twice with n-hexane and concentrated under a stream of nitrogen gas. FAMEs were analysed by GLC (model GC-380; GL-Science) or GLC-MS (GCMS-QP5050; Shimadzu). The FAME standards (C4–C24) were purchased from Supelco. The major cellular fatty acids were C12 : 0 (3·1 %), C16 : 0 (1·9 %), C18 : 1 (13·6 %), C18 : 0 (25·4 %), C20 : 1 (53·7 %) and C20 : 0 (2·3 %). The DNA G+C content was determined by direct analysis of deoxyribonucleotides by HPLC (Tamaoka & Komagata, 1984) and was 31·3 mol%.
Comparison with related genera and species
Phylogenetic analysis indicated that strain HGMK1T is most closely related to the uncultivated environmental clones SRI-40 (Skirnisdottir et al., 2000) and NAK-14 (Yamamoto et al., 1998), but distantly related to the cultivated strains P. guaymasensis EX-H2T, P. marina EX-H1T (Götz et al., 2002) and Hydrogenothermus marinus VM1T (Stöhr et al., 2001). P. marina EX-H1T and P. guaymasensis EX-H2T were respectively isolated from deep-sea hydrothermal vent sulfide structures in the EPR (9°N) and the Guaymas Basin (Götz et al., 2002). In addition, related strains possibly belonging to the genus Persephonella were obtained from similar microhabitats in other geographically distinct deep-sea hydrothermal vent sites of the Central Indian Ridge (Van Dover et al., 2001) and the Suiyo Seamount (Nakagawa et al., 2003).
Considering the recovery of all Persephonella strains and their phylogenetic association with various environmental rDNA clones (Reysenbach et al., 2000b) limited to deep-sea hydrothermal vent environments, the members of Persephonella are most likely indigenous to microhabitats that occur in deep-sea hydrothermal vent environments. Similarly, Hydrogenothermus marinus VM1T was obtained from a shallow marine hydrothermal system in Vulcano, Italy (Stöhr et al., 2001), and its ecological niche was speculated to be in relatively shallow marine hydrothermal environments. The preferred occurrence of Persephonella and Hydrogenothermus populations is also supported by their halophilic growth (growing optimally at around the salt concentration of sea water; Table 1). At present, however, the ecological niches of the novel isolate and phylogenetic relatives representing closely related environmental rDNA clones are thought to be terrestrial or subterranean hot water environments. Strain HGMK1T may thus represent a novel lineage of micro-organism within the Aquificales, preferentially inhabiting geothermal freshwater systems.
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), but this characteristic is commonly observed in Aquifex pyrophilus Kol5AT (Huber et al., 1992), Hydrogenobaculum acidophilum 3H-1T (Shima & Suzuki, 1993; Stöhr et al., 2001) and Hydrogenobacter thermophilus TK-6T (Kawasumi et al., 1984; Suzuki et al., 2001). To our knowledge, however, anoxic hydrogen and sulfur/thiosulfate oxidation with iron (III), selenate, selenite or arsenate was described for the first time in the metabolism of strain HGMK1T. Thus, this versatile energy-generating metabolism may be a distinctive feature that separates this isolate not only from other genera within the Persephonella–Hydrogenothermus clade, but also from genera within the Aquificaceae.
The cellular fatty acid composition of the novel isolate was similar to that of all members of the Aquificales, whereas the G+C content of the genomic DNA was lower (31·3 mol%) than in Persephonella species (approx. 37 mol%) and Hydrogenothermus marinus VM1T (43 mol%) (Table 1). On the basis of the physiological and molecular properties of the novel isolate, a new genus, Sulfurihydrogenibium gen. nov., is proposed. The type species is Sulfurihydrogenibium subterraneum sp. nov., with the type strain HGMK-1T (=JCM 11477T=ATCC BAA-562T=DSM 15120T).
Description of Sulfurihydrogenibium gen. nov.
Sulfurihydrogenibium (Sul.fu.ri.hy.dro.ge.ni'bi.um. L. neut. n. sulfur sulfur; N.L. neut. n. hydrogenum hydrogen; Gr. n. bios life; N.L. neut. n. Sulfurihydrogenibium sulfur- and hydrogen-eating life).
Straight to slightly curved rods, motile with a polar flagellum. Gram-negative. Facultatively anaerobic to microaerobic. Neutrophilic and thermophilic. Strictly chemolithoautotrophic. NaCl not absolutely required for growth. Able to utilize molecular hydrogen and reduced sulfur compounds as electron donors and molecular oxygen, nitrate, iron (III), selenate and arsenate as electron acceptors. G+C content of genomic DNA is about 31 mol%. Major cellular fatty acids are C18 : 1, C18 : 0 and C20 : 1. On the basis of 16S rRNA gene analysis, most closely related to the genera Persephonella and Hydrogenothermus. Occurs in terrestrial and subterranean geothermally heated freshwater systems. The type species is Sulfurihydrogenibium subterraneum.
Description of Sulfurihydrogenibium subterraneum sp. nov.
Sulfurihydrogenibium subterraneum (sub.ter.ra'ne.um. L. neut. adj. subterraneum under the earth, indicating the environment of isolation).
Motile, straight to slightly curved rods with a mean length of 1·5–2·5 µm and a width of approximately 0·3–0·5 µm. Cells occur singly. Exhibits the following properties in addition to those described for the genus. Temperature range for growth is 40–70 °C (optimum 65 °C). pH range for growth is 6·4–8·8 (optimum pH 7·5). Sea salts in the concentration range 0–48 g l-1 are not an absolute growth requirement; optimum growth occurs at 4·8 g l-1. Strictly chemolithoautotrophic growth occurs with molecular hydrogen, elemental sulfur or thiosulfate as electron donor and with molecular oxygen, nitrate, iron (III), selenate, selenite or arsenate as electron acceptor. Elemental sulfur and thiosulfate are oxidized to sulfate during growth. Nitrate, iron (III) and arsenate are respectively reduced to molecular nitrogen, iron (II) and arsenite. Elemental selenium is produced by bacterial selenate or selenite reduction. The major cellular fatty acids are C12 : 0 (3·1 %), C16 : 0 (1·9 %), C18 : 1 (13·6 %), C18 : 0 (25·4 %), C20 : 1 (53·7 %) and C20 : 0 (2·3 %). The DNA G+C content of the type strain is 31·3 mol% (by HPLC). The 16S rDNA sequence exhibits 91·1 and 90·6 % similarity to sequences from P. guaymasensis EX-H2T and P. marina EX-H1T.
The type strain, strain HGMK-1T (=JCM 11477T=ATCC BAA-562T=DSM 15120T), was isolated from subsurface hot aquifer water occurring in the Hishikari gold mine, Kagoshima Prefecture, Japan.
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ACKNOWLEDGEMENTS |
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