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Thiobaca Trueperi Gen. Nov., Sp. Nov., a Phototrophic Purple Sulfur Bacterium Isolated from Freshwater Lake Sediment

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Thiobaca Trueperi Gen. Nov., Sp. Nov., a Phototrophic Purple Sulfur Bacterium Isolated from Freshwater Lake Sediment International Journal of Systematic and Evolutionary Microbiology (2002), 52, 671–678 DOI: 10.1099/ijs.0.01739-0 Thiobaca trueperi gen. nov., sp. nov., a phototrophic purple sulfur bacterium isolated from freshwater lake sediment 1 University of Canberra and Gavin N. Rees,1 Christopher G. Harfoot,2 Peter H. Janssen,3 CRCFE/Murray-Darling 3 4 5 Freshwater Research Liesbeth Schoenborn, Jan Kuever and Heinrich Lu$ nsdorf Centre, PO Box 921, Albury, NSW 2640, Australia Author for correspondence: Gavin Rees. Tel: j61 2 6058 2356. Fax: j61 2 6043 1626. e-mail: gavin.rees!csiro.au 2 Department of Biological Sciences, University of Waikato, Hamilton, New Zealand Two strains of a novel species of phototrophic micro-organism were isolated from the sediments of a shallow, freshwater, eutrophic lake. Both strains grew 3 Department of Microbiology and photolithoheterotrophically with sulfide as an electron donor, transiently Immunology, University of accumulating intracellular sulfur globules. Photolithoautotrophic growth was Melbourne, Parkville, not observed. One strain was designated BCHT (the type strain) and was Victoria 3010, Australia studied in most detail. Cells contained bacteriochlorophyll a, and the dominant 4 Max-Planck-Institute for carotenoid was lycopene. Cell suspensions were brown. The photosynthetic Marine Microbiology, Celsiusstraße 1, D-28359 membranes had a vesicular arrangement. Acetate, propionate, pyruvate, Bremen, Germany succinate and fumarate were each used as electron donors and carbon sources 5 GBF–Gesellschaft fu$ r in the presence of sulfide and bicarbonate. In the presence of light, growth did Biotechnologische not occur with hydrogen, thiosulfate or iron(II). The optimum temperature for Forschung mbH, growth was between 25 and 30 SC, the maximum being 36 SC. The GMC content Mascheroder Weg 1, T D-38124, Braunschweig, of the genomic DNA of strain BCH was 63 mol%. Analysis of the 16S RNA Germany genes showed that both strains belonged to the γ-subclass of the Proteobacteria but were phylogenetically distinct from any described phototrophic organisms within the Chromatiaceae. On the basis of phylogenetic and physiological differences from other phototrophic micro- organisms, strain BCHT is described as a novel species of a new genus, Thiobaca trueperi gen. nov., sp. nov. Keywords: Thiobaca trueperi, phototrophic bacteria, freshwater lakes INTRODUCTION freshwater systems (Imhoff & Tru$ per, 1992). These phototrophs tend not to form dense, coloured blooms, Many investigations into the presence of phototrophic but numerous studies have demonstrated their pres- bacteria in aquatic ecosystems have been stimulated by ence in a wide variety of freshwater ecosystems. In this conspicuous coloured accumulations occurring in ano- study, we examined sediments of a freshwater lake that xic waters or surface mud (Pfennig & Tru$ per, 1992; undergoes summer stratification. The lake has ex- Pfennig, 1987). If sulfide is produced at depth in tensive growth of macrophytes, leading to a high aquatic environments, populations of purple and green carbon loading in the lake, resulting in apparently high phototrophic bacteria can grow by using the sulfide as rates of methane formation in the sediments. Since an electron donor for photosynthesis; this often leads previous observations indicated the methanogenic to prolific communities of phototrophic organisms nature of the study site, we examined the presence of (Sorokin, 1970; Takahashi & Ichimura, 1970; Over- phototrophic bacteria growing with relatively low mann et al., 1996). Other phototrophic bacteria that levels of sulfide. Enrichment cultures led to the do not use sulfide, but instead use a range of reduced purification of brown-coloured organisms that were organic compounds as electron donors, also occur in shown subsequently to be related to purple sulfur ................................................................................................................................................. bacteria. Phylogenetic and physiological studies show- The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA sequences of ed that the organisms differed significantly from any strains BCHT (l DSM 13587T l ATCC BAA-132T) and OCH-PHB (l DSM described in the literature, and we conclude that the 13588 l ATCC BAA-133) are respectively AJ404006 and AJ404007. strains represent a novel species of a new genus. We 01739 # 2002 IUMS Printed in Great Britain 671 G. N. Rees and others propose the name Thiobaca trueperi gen. nov., sp. conditions were yeast extract-\ammonium chloride-free nov., to encompass these novel strains. medium with argon in the headspace and ammonium- containing medium with argon in the headspace. METHODS Whole-cell spectra were obtained as described by Pfennig & Tru$ per (1992). For acetone extracts, cells were collected Source of organisms. Normans Lagoon is a eutrophic oxbow on glass-fibre filters and extracted overnight in the dark at lake that is between 2 and 4 m deep and is situated adjacent 4 mC. Scans were obtained using a Cary 3 (Varian) spectro- to the River Murray, Albury, Australia. The lake has areas photometer. Photosynthetic pigments were analysed by of open water surrounding beds of the emergent macrophyte HPLC as described previously (Dilling et al., 1995). Eleocharis sphacelata. Beds of Brasenia schreberi are associ- Phase-contrast micrographs were prepared by immobilizing ated with the edges of the lake, and portions of the surface cells on agar-coated slides and examining the slides with a often show growth of the aquatic fern Azolla. The lake is Zeiss Axioskop microscope. Nile blue A (Ostle & Holt, fringed, in part, by river red gums (Eucalyptus camaldu- 1982) was used to determine whether cells contained lipid lensis). Sediment was collected from the open-water regions, inclusions. For electron microscopy studies, exponential- and enrichment cultures were made by adding 0 5 ml wet n phase cells of strain BCHT were chemically fixed with 2 5% sediment to 10 ml basal medium (see below) that contained n (v\v) glutaraldehyde in the carbonate-buffered growth acetate (5 mM), malate (5 mM) and sulfide (0 5mM). n medium (pH 7 0) at ambient temperature for 5 days. Fixed Enrichment cultures were subcultured several times and n cells were immobilized in 2% (w\v) Noble agar (Difco). pure cultures were obtained by application of the agar-shake $ Cubes (1 mm ) of immobilized cells were cut and then dilution method (Pfennig, 1978). washed three times for 10 min each at room temperature Growth conditions. Basal medium (Biebl & Pfennig, 1981) with 100 mM cacodylate buffer (pH 7 3). Post-fixation with " n was used throughout this study and contained (g l− distilled 1%(w\v) OsO%\100 mM cacodylate buffer (pH 7n3), further water): KH#PO% (0n5), MgSO%;7H#O(0n2), NaCl (0n4), preparation steps and electron microscope analysis were NH%Cl (0n4), CaCl#;2H#O(0n05) and yeast extract (0n2, done according to Yakimov et al. (1998). Oxoid). Basal medium was prepared and dispensed into DNA base composition and phylogenetic analyses. The Hungate tubes or 30 ml serum bottles, with N# as the headspace gas, as described by Rees et al. (1995). Bi- GjC content (mol%) of the genomic DNA was determined et al carbonate was added to culture vessels after autoclaving to by HPLC as described by Janssen . (1996). The 16S give a final concentration of 30 mM. Sodium sulfide was rRNA genes of the novel strains were sequenced and the sequence data used to infer evolutionary relationships added to give a final concentration of either 0n5or1n5 mM, depending on the desired growth conditions. The final pH of between these strains and other bacteria, as described by Janssen & O’Farrell (1999). Evolutionary analyses were the medium was between 7n2 and 7n4. Additional carbon sources were added to the medium from sterile anoxic stock carried out using software implemented in the Australian solutions. Organic compounds were prepared as anoxic Genomic Information Service () system (Littlejohn et solutions, which were generally sterilized by autoclaving. al., 1996). The 16S rRNA gene sequences were compared Sodium pyruvate, carbohydrates, sodium thiosulfate and with known 16S rRNA gene sequences by carrying out a analysis (Altschul et al., 1990) in the GenBank sodium sulfite were filter-sterilized through 0n2 µm pore-size membrane filters. A vitamin solution (Widdel & Bak, 1992) database (Benson et al., 2000), allowing the identification of close relatives. The gene sequences from the two novel containing vitamin B"# was added to sterile medium to give −" strains and selected reference sequences (identified by the a final concentration of 50 µg vitamin B"# l . Cultures were analyses and by comparisons of the inferred phylo- routinely incubated at 25 mC, with illumination provided by tungsten lamps giving a light intensity of 120–140 lux. genies determined in other studies; Guyoneaud et al., 1998; Imhoff et al., 1998) were aligned using the program. Cellular and physiological characterization. All physiological The alignment was then checked manually and edited, using tests were carried out in basal medium. When growth with the secondary structure of the Escherichia coli 16S rRNA organic compounds was not unequivocal, strains were (Neefs et al., 1993) as a template. Regions for which subcultured into medium containing the same substrate. homology could not be determined were eliminated from the Photoautotrophy and vitamin requirements were examined entire dataset; these were helices 10 and 11, the terminal by subculturing strains
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