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Desulfocella Halophila Gen. Nov., Sp. Nov., a Halophilic, Fatty-Acid-Oxidizing, Sulfate- Reducing Bacterium Isolated from Sediments of the Great Salt Lake

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Desulfocella Halophila Gen. Nov., Sp. Nov., a Halophilic, Fatty-Acid-Oxidizing, Sulfate- Reducing Bacterium Isolated from Sediments of the Great Salt Lake International Journal of Systematic Bacteriology (1 999), 49, 193-200 Printed in Great Britain Desulfocella halophila gen. nov., sp. nov., a halophilic, fatty-acid-oxidizing, sulfate- reducing bacterium isolated from sediments of the Great Salt Lake Kristian K. Brandt,lF2 Bharat K. C. Patel' and Kjeld Ingvorsenl Author for correspondence: Kjeld Ingvorsen. Tel: +45 89 42 32 45. Fax: +45 86 12 71 91 e-mail : Kjeld.Ingvorsen@ biology .aau.dk 1 Department of Microbial A new halophilic sulfate-reducing bacterium, strain GSL-ButZT, was isolated Ecology, Institute of from surface sediment of the Southern arm of the Great Salt Lake, UT, USA. The B iologica I Sciences, University of Aarhus, Ny organism grew with a number of straight-chain fatty acids (C4-C,J, 2- Munkegade, Building 540, methylbutyrate, L-alanine and pyruvate as electron donors. Butyrate was DK-8000 Aarhus C, oxidized incompletely to acetate. Sulfate, but not sulfite or thiosulfate, served Denmark as an electron acceptor. Growth was observed between 2 and 19% (w/v) NaCl * Faculty of Science and with an optimum at 4-5% (w/v) NaCl. The optimal temperature and pH for Tech no1ogy, G riffit h University, Nathan, growth were around 34 "C and pH 6.5-7.3, respectively. The generation time Brisbane 41 11, Australia under optimal conditions in defined medium was around 28 h, compared to 20 h in complex medium containing yeast extract. The G+C content was 35-0 mol%. 16s rRNA gene sequence analysis revealed that strain GSL-ButZT belongs to the family Desulfobacteriaceaewithin the delta-subclass of the Proteobacteria and suggested that strain GSL-ButZTrepresents a member of a new genus. The name Desulfocella halophila gen. nov., sp. nov. is proposed for this organism. The type strain of D. halophila is strain GSL-ButZT(= DSM 11763T = ATCC 7004263. Keywords : Desulfocella halophila, halophilic sulfate-reducing bacteria, long-chain fatty acids, taxonomy INTRODUCTION of the acetate-oxidizing Desulfobac ter halo tolerans (Brandt & Ingvorsen, 1997), all these strains share the The occurrence of dissimilatory sulfate-reduction in ability to oxidize lactate, molecular hydrogen and hypersaline environments has been known for several other substrates typically metabolized by members of decades (ZoBell, 1958). More recent studies indicate the genus Desulfovibrio. Other types of SRB capable of that bacterial sulfate reduction is the most important growing on higher fatty acids and benzoate have been anaerobic mineralization process in hypersaline mi- reported from hypersaline oilfields (Cord-Ruwisch et crobial mats and sediments (Canfield & Des Marais, al., 1987). However, these species were not sufficiently 1993; Caumette et al., 1994; Jsrgensen & Cohen, described to allow for a taxonomic affiliation with 1977 ; Skyring, 1987). However, not until recently have existing SRB. Hence nothing is known about the the first dissimilatory sulfate-reducing bacteria (SRB) physiology and phylogeny of long-chain fatty acid- from a wide range of hypersaline habitats been isolated oxidizing SRB in hypersaline environments. and phylogenetically described (Brandt & Ingvorsen, 1997; Caumette et al., 1991 ; Krekeler et al., 1997; Nga As a part of our investigations on the ecology and et al., 1996; Ollivier et al., 1991 ; Tardy-Jacquenod et diversity of SRB in hypersaline environments, here we al., 1996,1998; Zhilina et al., 1997). With the exception provide the characterization of a new butyrate- and higher fatty-acid-oxidizing, sulfate-reducing bac- terium isolated from the Great Salt Lake, UT, USA. Abbreviation: SRB, sulfate-reducing bacteria. Phylogenetic analysis as well as other characteristics The GenBank accession number for the 165 rDNA sequence of strain GSL- suggest that this strain, designated GSL-BU~~~,is a B~t2~is AF022936. representative of a new genus and a new species for 00842 0 1999 IUMS 193 K. K. Brandt, B. K. C. Pate1 and K. Ingvorsen Fig. 7. Transmission electron micrographs of Desulfocella halophila strain GSL-ButZT after negative staining. (a) Dividing cell showing the polar flagellum; bar, 0.5 pm. (b) The polar region showing polar appendages; bar, 0.2 pm. which we propose the name Desulfocella halophila gen. (1992). The fatty acid analysis was performed by Professor nov., sp. nov. Dr Reiner M. Kroppenstedt at DSMZ (Braunschweig, Germany) and the fatty acid nomenclature of Vainshtein et al. (1992) was used. METHODS G + C content of genomic DNA and characterization of Source of strains. Strain GSL-BU~~~and physiologically pigments. The G+C content of genomic DNA was de- similar strains were isolated from surface sediment collected termined at the Identification Service of the DSMZ from the Southern arm of the Great Salt Lake at 8-10m (Braunschweig, Germany) by Dr Jutta Burghardt. Genomic depth (station AS2; Utah Geological Survey station code). DNA from strain GSL-BU~~~was isolated and purified according to Visuvanathan et al. (1989) and the G+C Isolation and media. Strains of SRB were initially enriched in content was determined by HPLC analysis (Mesbah et al., Medium E (Brandt & Ingvorsen, 1997) containing 100 g 1989; Tamaoka & Komagata, 1984). The presence of NaCl 1-1 and a mixture of acetate (10 mM), propionate desulfoviridin was investigated in cell extracts as described (10 mM) and butyrate (5 mM). A modified defined medium, previously by Widdel & Pfennig (1 98 1). Medium I (Brandt & Ingvorsen, 1997), containing 100 g NaCl 1-1 and butyrate (15 mM) as the sole electron donor 165 rRNA gene sequencing and phylogenetic analysis. was employed for all subsequent enrichments/isolations. Genomic DNA from strain GSL-BU~~~was isolated by the Pure cultures were obtained by repeated use of deep agar method of Porteuous et al. (1994). A primer pair, designated dilution series (Widdel & Bak, 1992). If not stated otherwise, Fdl(5’ CAGAGTTTGATCCTGGCTCAG 3’) and Rdl(5’ growth experiments were performed in Medium I (50 g NaCl AAGGAGGTGATCCAGCC 3’) was used for PCR ampli- 1-l) with butyrate and sulfate as growth substrates (27 or fication of the 16s rRNA gene. The PCR product was 30 “C, pH 6.9-7’3). purified by using QIAEX (QIAGEN) as described by the manufacturer. The purified PCR product was subsequently Morphology. Gram staining was performed as described by Dussault (1955). Exponentially growing cells were negatively sequenced at Griffith University with an Applied Biosystems stained with 1 % (w/v) uranyl acetate and subsequently model 373A automated DNA sequencer by using a Prism dideoxy terminator cycle sequencing kit and by following viewed with a JEOL 1200EX transmission electron micro- scope. the recommended protocol of the manufacturer (Applied Biosystems). The primers used for sequencing were Fd 1, F 1 Analytical techniques. Hydrogen sulfide was analysed (5’ CTCCTACGGGAGGCAGCAG 37, F3 (5’ AAACTC- spectrophotometrically (Cord-Ruwisch, 1985). Fatty acids AAAGGAATTGACGG 37, F4 (5’ TGTACACACCGC- were quantified by HPLC analysis using an Aminex HPX- CCGT 37, R1 (5’ CTGCTGCCTCCCGTAG 3’), R2 (5’ 87H ion exclusion column (Bio-Rad) and UV detection as GTATTACCGCGGCTGCTG 3’), R4 (5’ CCGTCAATT- previously described (Brandt & Ingvorsen, 1997). CCTTTGAGTTT 39, R5 (5’ GGGGTTGCGCTCGTTG 37, R6 (5’ TACGGTTACCTTGTTACGAC 3’) and Rdl. Lipid analysis and fatty acid nomenclature. Strain GSL- B~t2~was cultivated in the standard medium of Vainshtein The 16s rRNA gene sequence was manually aligned against et al. (1992) supplemented with 50 g NaCl 1-1 and 20 mM representative sequences from the delta-subclass of the butyrate. Cells were harvested by centrifugation (1 6 000 g), Proteobacteria using the alignment editor ae2 (Maidak et al., freeze-dried and analysed according to Vainshtein et al. 1997). Painvise evolutionary distances were calculated ac- 194 International Journal of Systematic Bacteriology 49 Desulfocella halophila gen. nov., sp. nov. Table 7- Morphological and physiological characteristics of Desulfocella halophila strain GSL-BU~~~as compared to the closest relatives among the dissimilatory sulfate-reducing bacteria ND, Not done. Final concentrations (mM) of the electron donors/acceptors tested are given in parentheses. The sulfate concentration of the medium was 40.6 mM. Saturated unbranched fatty acids were added at concentrations recommended by Widdel & Bak (1992). The following electron donors were not utilized by strain GSL-BU~~~:L-arginine (7.9, L-asparagine (9, betaine (lo), 1-butanol (lo), capric acid (lo), citrate (lo), L-cysteine (lo), fructose (lo), glucose (lo), glutamate (lo), glycerol (lo), glycine (lo), L-isoleucine (9,L-leucine (9,L-methionine (9,L-serine (lo), thioglycolate (2.5), L-threonine (7.9, L-tryptophan (2) or xylose (10). Fe(II1)-citrate (20), nitrate (lo), elemental sulfur or fumarate (10) were not used as electron acceptors by strain GSL-BU~~~.Symbols used: + , good growth; + (auto), autotrophic growth; (+), slow growth; -, no growth. Desulfocella 'Desulfobotulus Desulfococcus Desulfosarcina Desulfohacterium halophila sapovorans '* multivorans" variabilis* autotrophicumt Cell shape Vibrio Vibrio Spherical Oval (form Oval rod aggregates) Width (pm) O.W.7 1.5 1.5-2.2 1-1.5 1-1.5 Length (pm) 2-4 3-55 - 15-25 1.5-2.5 Vitamin requirement None None 4-Aminobenzoate, None 4-Aminobenzoate, biotin, thiamin biotin, nicotinate Motility : + (polar + (polar - +/- (polar + (polar flagellum) flagellum) flagellum) flagellum) Electron donors : - H2 +(auto) +(auto) Formate (1 0) +(auto) + (auto) + (auto) Acetate (10) (+I (+) (+I Propionate (1 0) - + + (+I Fatty acids (C-atoms) 4-6, 8, 12, 16 616 4-14 4-1 6 Isobutyrate (10) - + - + 2-Methylbutyrate (10) + + (+I + 3-Methylbutyrate (10) - + (+I lactate (10) + + + Ethanol (20) + + + Pyruvate (10) + + + Benzoate (2) + + Succinate (10) - + + Fumarate (1 0) + + Malate (10) - - + L-Alanine (10) + ND ND ND ND Oxidation of energy Incomplete Incomplete Complete Complete Complete substrate Electron acceptors : Sulfate + + + + Sulfite (2-5) - + + + Thiosulfate (5-10) - + + Shortest doubling time (h) 15 - - on butyrate + sulfate Optimum temperature 34 34 35 33 25-28 ("C) Optimum salinity (% 0.147 0.7-2.0 1-3 2 NaCl, w/v) Optimum pH 7.0 7.7 7.3 7.4 6.7 Desulfoviridin - - + - - G + C content of DNA 35 53 57 51 48 (mol YO) * Widdel (1980).
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