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1 IRD, UR 101 Extrêmophiles, IFR-BAIM, Universités de Provence et de la Méditerranée, ESIL, case 925, 163 avenue de la Méditerranée, 13288 Marseille cedex 09, France
2 Laboratoire de Microbiologie Marine, CNRS–INSU-UMR 6117, Université de la Méditerranée, Marseille Luminy, France
Correspondence
B. Ollivier
ollivier{at}esil.univ-mrs.fr
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ABSTRACT |
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The GenBank accession number for the 16S rDNA sequence of strain AM13T is AF458778.
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; Polz & Cavanaugh, 1995). Microbial hydrothermal vent communities also include free-living bacteria associated with the discharged vent fluids, free-living microbial mats and micro-organisms within the deep-sea hydrothermal vent plume (Karl, 1995). Although increasing attention has been paid to the thermophilic and hyperthermophilic micro-organisms that inhabit deep-sea hydrothermal vents, because of their high biotechnological potential, mesophilic and psychrophilic micro-organisms are known to be significant components of the microbial community along the physico-chemical gradient of the vent ecosystem (Jeanthon, 2000). The occurrence of mesophilic sulfate-reducing bacteria (SRB) was made evident by (i) significant sulfate-reduction activities in vent sediments (Elsgaard et al., 1994; Jørgensen et al., 1992) and (ii) their isolation from various samples collected at different hydrothermal sites (Elsgaard et al., 1995). However, none of them has yet been characterized.
Here, we report the isolation from deep-sea hydrothermal chimneys of SRB that are phylogenetically similar to Desulfovibrio profundus (Bale et al., 1997) and the characterization of a novel mesophilic, barophilic species (strain AM13T) of the genus Desulfovibrio, Desulfovibrio hydrothermalis sp. nov.
Strains BL5, H9, H1 and AM13T were isolated from a deep-sea hydrothermal chimney sample stored in sea water at 4 °C until processing. The samples were collected by the deep-submergence vehicle Nautile in June 1999 from the Grandbonum vent site at latitude 13° N along the East-Pacific Rise during the AMISTAD cruise at a depth of 2600 m. Desulfovibrio zosterae DSM 11974T and D. profundus DSM 11384T were obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany. Enrichment and isolation were performed using SRB growth medium containing the following (l-1 distilled water): NH4Cl, 1·0 g; K2HPO4, 0·3 g; KH2PO4, 0·3 g; MgCl2.6H2O, 3·0 g; CaCl2.2H2O, 0·1 g; NaCl, 25 g; KCl, 0·2 g; Na2SO4, 3·16 g; sodium acetate, 0·5 g; sodium lactate, 2·24 g; cysteine hydrochloride, 0·5 g; yeast extract (Difco Laboratories), 0·5 g; bio-Trypticase (bioMérieux), 0·5 g; trace mineral element solution (Balch et al., 1979), 10 ml; resazurin, 1·0 mg. The pH was adjusted to 7·0 with 10 M KOH and the medium was boiled under a stream of O2-free N2 gas and cooled to room temperature. Aliquots of 5 or 20 ml were then dispensed respectively into Hungate tubes or serum bottles, under a stream of N2/CO2 gas (80 : 20, v/v), and the vessels were autoclaved for 45 min at 110 °C. Prior to inoculation, Na2S.9H2O and NaHCO3 were injected from sterile stock solutions to obtain respective final concentrations of 0·04 % (w/v) and 0·2 % (w/v). A chimney sample was inoculated in 20 ml SRB medium and incubated at 35 °C without agitation to initiate an enrichment culture. The culture was purified by repeated use of the roll-tube method (Hungate, 1969) with medium solidified with 2 % (w/v) agar (Difco). Several colonies that developed were picked and cultured in the culture medium. The process of isolation was repeated several times until the isolates were deemed to be axenic.
pH, temperature and NaCl ranges for growth were determined using SRB medium according to Hernandez-Eugenio et al. (2000). Substrates were tested at a final concentration of 20 mM in SRB medium. To test for electron acceptors, sodium thiosulfate, sodium sulfate, sodium sulfite, elemental sulfur and nitrate were respectively added to the medium at final concentrations of 20 mM, 20 mM, 2 mM, 2 % (w/v) and 10 mM. For disproportionation studies, SRB medium without lactate but containing 20 mM thiosulfate and 2 mM acetate was used. Disproportionation was verified by the formation of sulfate (Madsen & Aamand, 1991) and sulfide (Cord-Ruwisch, 1985). Growth and product formation were analysed after 2 weeks of incubation at 35 °C. Cells of strain AM13T from the early stationary phase of growth were used for pressurization tests. The culture broth was diluted in 20 ml tubes containing sterile medium to obtain an initial OD600 of 0·05. Half of the tubes were incubated at 260 atm hydrostatic pressure at 37 °C and the other half were incubated at 1 atm at 37 °C. At the appropriate times, three tubes from each pressure condition were removed to monitor the OD600 of the two cultures. Phase-contrast microscopy (model Eclipse E600; Nikon) was used for routine examinations of the cultures and to obtain photomicrographs. Thin sections for electron microscopy were prepared as described by Fardeau et al. (1997). Electron micrographs were taken with a Hitachi model H600 electron microscope at 75 kV.
Unless otherwise indicated, duplicate culture tubes were used throughout these studies. Growth was measured by inserting tubes directly into a model Cary 50 Scan spectrophotometer (Varian) and measuring the OD580. Sulfide was determined photometrically as colloidal CuS by the method of Cord-Ruwisch (1985). Fermentation products were determined as described by Fardeau et al. (1993). Desulfoviridin was determined as described by Postgate (1959). The G+C content of DNA was determined at the DSMZ using HPLC as described previously (Hernandez-Eugenio et al., 2000). DNA–DNA hybridization studies were also performed at the DSMZ (Chamkha et al., 2001). The methods for purification and extraction of DNA and the amplification and sequencing of the 16S rRNA gene have been described previously (Andrews & Patel, 1996). The sequencing reaction was performed by PCR amplification in a final volume of 20 µl using 100 ng PCR products (or 500 ng plasmid), 5 pmol primer and 8 µl BigDye Terminator premix according to the Applied Biosystems protocol. After heating to 96 °C for 3 min, the reaction was subjected to 30 cycles of 30 s at 96 °C, 30 s at 55 °C and 4 min at 60 °C (Perkin Elmer 9700 thermal cycler). Removal of excess BigDye Terminators was performed by using exclusion columns. The samples were dried in a vacuum centrifuge and dissolved in 1·6 µl deionized formamide/EDTA pH 8·0 (5 : 1). The samples were loaded onto an Applied Biosystems 373XL sequencer and run for 12 h on a 4·5 % denaturing acrylamide gel. The 16S rRNA gene sequence was aligned manually with reference sequences of various members of the genus Desulfovibrio using the sequence alignment editor BioEdit (Hall, 1999). Reference sequences were obtained from the Ribosomal Database Project II (Maidak et al., 2001), EMBL and GenBank databases (Benson et al., 1999). Positions of sequence and alignment uncertainty were omitted from the analysis. Pairwise evolutionary distances based on 1190 unambiguous nucleotides were computed by using the method of Jukes & Cantor (1969). Dendrograms were constructed by using the neighbour-joining method (Saitou & Nei, 1987). Confidence in the tree topology was determined by using bootstrapped trees (Felsenstein, 1985).
Sulfate-reducing enrichment cultures were obtained after 4 days incubation at 35 °C. Microscopic observations revealed the presence of motile, vibrio-shaped bacteria. The enrichment was subcultured in Hungate roll tubes. Single, brown, discus-shaped colonies (1–2 mm diameter) that developed after 7 days incubation at 35 °C were picked and serially diluted in roll tubes before the culture was considered pure. Four strains (BL5, H9, H1 and AM13T) were isolated. The purity of these strains was confirmed by the morphological homogeneity of cells observed under a phase-contrast microscope and by the absence of growth in liquid sulfate-free SRB medium supplemented with 20 mM glucose under aerobic or anaerobic conditions. Strains BL5 and H9 were found to be phylogenetically similar to D. profundus, whereas strains H1 and AM13T were phylogenetically distinct (see details below) from D. zosterae. Strain AM13T was characterized further. Microscopic observations revealed that the cells of strain AM13T were motile, Gram-negative, vibrio-shaped or sigmoid and occurred mainly singly (Fig. 1a). Cells were 3–5 µm long and 0·5–1·2 µm wide. Sporulation was never observed. Electron microscopy of ultrathin sections of cells indicated the presence of a multilayered Gram-negative type of cell envelope, as reported for members of the genus Desulfovibrio (Fig. 1b).
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). Strain AM13T used hydrogen, formate, lactate, fumarate, malate, pyruvate, ethanol, glycerol and choline in the presence of sulfate as an electron acceptor. Lactate was oxidized incompletely to acetate, CO2 and H2S. H2 and formate were used only in the presence of acetate as a carbon source. No growth was observed on the following substrates using sulfate as electron acceptor: acetate, succinate, propionate, butyrate, benzoate, methanol, 1-propanol, fructose, xylose, glucose and alanine. Pyruvate was fermented to acetate, hydrogen and CO2 in sulfate-free medium. Sulfate, thiosulfate and sulfite, but not elemental sulfur or nitrate, served as electron acceptors in the presence of lactate as energy and carbon source.
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-Proteobacteria and is related to D. zosterae (similarity 96·4 %) (Fig. 3). The G+C content of DNA of strain AM13T was 47 mol%. DNA–DNA hybridization studies indicated that strain AM13T and D. zosterae have an overall relatedness value of 23·8 %, whereas strain BL5 and D. profundus have an overall relatedness value of 68·7 %.
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). Within this domain, only one thermophilic sulfate-reducing archaeon, Archaeoglobus profundus, has been isolated at great depths (Burggraf et al., 1990). Despite the great interest of scientists in studying thermophilic or hyperthermophilic micro-organisms, it is generally admitted that mesophiles, as well as moderate thermophiles, may represent the most abundant microbes in hydrothermal vents (Campbell et al., 2001; Jeanthon, 2000). This is exemplified by the isolation of (i) metabolically diverse non-filamentous mesophilic bacteria from the dorsal integument of Alvinella pompejana (Prieur & Jeanthon, 1987; Prieur et al., 1990; Raguénès et al., 1996), (ii) several mesophilic sulfur-oxidizing bacteria (Durand et al., 1993; Jannasch et al., 1985; Ruby & Jannasch, 1982; Wirsen et al., 1998) and (iii) moderate thermophiles belonging to the 
-Proteobacteria (Campbell et al., 2001). Sulfate reduction activity was evident in sediments from Guaymas Basin (Elsgaard et al., 1994; Jørgensen et al., 1992) and successful isolation was achieved from various samples collected at different marine hydrothermal environments, thus suggesting the probable ecological significance of SRB in the biogeochemistry of such environments. Despite this ecological importance, only one thermophilic and no mesophilic SRB have been fully characterized (Burggraf et al., 1990).
In this paper, we report (i) the characterization of a novel species of the genus Desulfovibrio, strain AM13T, and (ii) the isolation of sulfate reducers that are phylogenetically and genotypically similar to D. profundus, which originated from deep sediment layers in the Japan Sea (Bale et al., 1997). The isolation of D. profundus-like micro-organisms from deep-sea hydrothermal vents (chimney rocks) suggests that this species is ecologically significant within deep-sea environments, being distributed not only in deep marine sediments (Bale et al., 1997), but also at the surface of these sediments (this report). Similarly to the D. profundus-like micro-organisms isolated during this work, the sulfate-reducing strain AM13T was also isolated from a deep-sea hydrothermal chimney sample, but it differs greatly phylogenetically from D. profundus (similarity 87·8 %). Phenotypic and genotypic differences are also observed between D. profundus and strain AM13T. They include the G+C content of the DNA and the range of temperature for growth (Table 1).
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). There are also other phenotypic differences between the two bacteria (Table 1
); in particular, the inability of strain AM13T to oxidize sugars. Genomic differences were also observed when performing DNA–DNA hybridization, since a low value of DNA relatedness (23·8 %) was found between strain AM13T and D. zosterae, thus confirming that strain AM13T is a novel species of the genus Desulfovibrio (Wayne et al., 1987). An important physiological feature of this novel species is that it is barophilic, having a higher growth rate at a hydrostatic pressure of 260 atm, which corresponds to the pressure from its extracted environment, than at atmospheric pressure. This provides evidence that the novel species, like D. profundus, originates from deep environments. Because of the significant phenotypic, genotypic and phylogenetic differences between D. zosterae and strain AM13T, the latter can be assigned to a novel species of the genus Desulfovibrio, for which the name Desulfovibrio hydrothermalis sp. nov. is proposed.
Description of Desulfovibrio hydrothermalis sp. nov.
Desulfovibrio hydrothermalis (hy.dro.ther.ma'lis. N.L. adj. hydrothermalis from a hydrothermal area).
Cells are motile, Gram-negative, vibrio-shaped or sigmoid (0·5–1x1–2 µm). The temperature range for growth is 20–40 °C, the optimum being 35 °C. The optimum pH for growth is 7·8. In the presence of sulfate, hydrogen plus acetate (carbon source), formate plus acetate (carbon source), lactate, fumarate, malate, pyruvate, ethanol, glycerol and choline serve as growth substrates. Fermentative growth occurs on pyruvate. Sulfate, thiosulfate and sulfite, but not elemental sulfur or nitrate, are utilized as electron acceptors. Oxidation of lactate with sulfate is incomplete, with acetate, CO2 and H2S as the end products of metabolism. The G+C content of the DNA is 47±0·5 mol% as determined by HPLC. The GenBank accession number for the 16S rRNA gene sequence of strain AM13T is AF458778. Isolated from a hydrothermal chimney at a depth of 2600 m at 13° N from the East-Pacific Rise. The type strain is strain AM13T (=DSM 14728T =CIP 107303T).
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ACKNOWLEDGEMENTS |
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) and 260 atm (
).