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1 Division of Biological Sciences, Program in Microbial Ecology, University of Montana, Missoula, MT 59812-4824, USA
2 Institut für Chemie und Biologie des Meeres, Universität Oldenburg, D-26111 Oldenburg, Germany
3 Department of Geology, University of Montana, Missoula, MT 59812, USA
4 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
5 Section Microbiology, Department Biology I, Ludwig-Maximilians-Universität München, Maria-Ward-Str. 1a, D-80638 München, Germany
Correspondence
R. F. Rosenzweig
Frank.Rosenzweig{at}mso.umt.edu
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A transmission electron micrograph of cells of strain STP12T, a graph showing lactate oxidation and growth and a summary of the metal-tolerance profiles of strain STP12T and related strains are available as supplementary material in IJSEM Online.
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), Desulfosporosinus auripigmenti (Stackebrandt et al., 2003) and Desulfosporosinus meridiei (Robertson et al., 2001). Isolates from locales separated by thousands of kilometres exist for some of these species (e.g. DSM 8344; Vainshtein et al., 1994). Culture- and non-culture-based studies have revealed the existence of Desulfosporosinus-like organisms in environmental settings as diverse as permafrost (Vainshtein et al., 1994), pristine aquifers (Detmers et al., 2004), municipal drinking water (Bade, 2000) and rice plant roots (Scheid et al., 2004).
Multiple lines of evidence suggest that members of the genus also commonly inhabit industrially impacted soils and sediments. D. auripigmenti was isolated from an arsenic-contaminated watershed, and is one of a limited number of bacteria known to respire arsenate (Newman et al., 1997). Recently, another arsenic-reducing Desulfosporosinus strain was isolated from arsenic-contaminated sediments; this organism has the capacity to metabolize a wide variety of aromatic compounds (Liu et al., 2004). Kusel et al. (2001) reported the isolation of Desulfosporosinus-like organisms from a coal-mining-impacted lake, while Robertson et al. (2000) isolated eight Desulfosporosinus strains from a hydrocarbon-contaminated soil. Two of these were later described as D. meridiei (Robertson et al., 2001) and their activity was linked to toluene mineralization (Robertson et al., 2000; Franzmann et al., 2002). Desulfosporosinus-like strains have repeatedly been seen to dominate subsurface bacterial communities associated with radionuclide-contaminated sediment. This observation is consistent across widely dispersed habitats in the United States that include the Midnight Mine, WA (Suzuki et al., 2002), the DOE Field Research Center in Oak Ridge, TN (Shelobolina et al., 2003), and uranium mine tailings in Shiprock, NM (Nevin et al., 2003). Significantly, enrichment of Desulfosporosinus-like microbes has been associated with stimulated removal of solution-phase uranium (Nevin et al., 2003). In such contexts, uranium precipitation may occur secondarily to sulfidogenesis or as a primary result of dissimilatory U(VI) reduction (Suzuki et al., 2002, 2003, 2004).
Herein, we report the isolation and characterization of a novel Desulfosporosinus strain from a pristine environment, sediments of Lake Stechlin, Germany. Strain STP12T was found by 16S rRNA gene sequence comparison to have similarity values of 96.4–96.7 % relative to other members of the genus; DNA–DNA hybridization experiments revealed only 32 % reassociation with the type strain of the type species, D. orientis DSM 765T. We describe genetic and phenotypic attributes of STP12T investigated in parallel with the three Desulfosporosinus species with validly published names. We contend that ribosomal gene sequence differences and hybridization data, considered along with strain-specific differences in cytochromes, cell-wall chemotaxonomy and riboprint patterns, support recognition of STP12T as representing a distinct and novel species within the genus Desulfosporosinus.
Strain STP12T was isolated from the highest positive tubes of a most-probable number (MPN) series inoculated with sediment from Lake Stechlin a pristine, dimictic, oligotrophic freshwater lake located 100 km north of Berlin (Germany) (Sass et al., 1997). The culture medium used was that described by Widdel & Pfennig (1977), modified by Widdel (1980). Medium was reduced by addition of 0.1 ml freshly prepared sodium dithionate stock solution (3 % w/v). Na2SO4 (10 mM) and sodium lactate (10 mM) were added separately from sterile anaerobic stocks. Anaerobic techniques were used in all medium preparation and culture manipulations. Physiological attributes of strain STP12T were evaluated in parallel with those of other members of the genus Desulfosporosinus. D. meridiei DSM 13257T (Robertson et al., 2001), D. orientis DSM 765T (Campbell & Postgate, 1965) and D. auripigmenti DSM 13351T (Newman et al., 1997; Stackebrandt et al., 2003) were obtained from the DSMZ. Bacteria were initially cultivated on the appropriate recommended DSMZ medium. Because all strains grew on Widdel & Pfennig (1977) medium as modified by Widdel (1980), this medium was used for all comparative experiments. Unless otherwise indicated, all physiological experiments were performed in triplicate at 30 °C, lasting until cultures reached stationary phase. Uninoculated media and/or autoclaved cells served as negative controls.
Gram staining was performed using the Fisher Gram stain set protocol (Magee et al., 1975). Spore formation was tested by culturing strains in media containing 10 mM sulfate and 10 mM lactate through late-stationary phase and then assessing presence of spores by phase-contrast light microscopy and transmission electron microscopy (TEM). Cultures deemed positive for spore formation were incubated at 85 °C for 30 min and then transferred to fresh medium and monitored for outgrowth.
Samples for negative staining and electron microscopy were pipetted onto a nickel grid coated with 0.25 % Formvar solution in ethylene dichloride and stained for 30–60 s with 2 % uranyl acetate. Thereafter, the grid was mounted on a grid holder and viewed using a 1K/1K AMT camera attached to a Hitachi H-7100 transmission electron microscope. Samples for TEM were prepared by fixing cells with Karnovsky's fixative and washing three times with 0.1 M sodium cacodylate buffer. Samples were pelleted by centrifugation, embedded in 1 % agarose (with 0.01 % azide), post-fixed with 1 % buffered osmium tetroxide and then dehydrated in a graded ethanol series followed by propylene oxide. Bacterial samples were infiltrated in a polybed 812 resin and polymerized at 60 °C for 2 days. Sections (70 nm) were collected on 100-mesh copper–rhodium grids, post-stained with 2 % uranyl acetate followed by Reynold's lead citrate (Bozzola & Russell, 1999) and then viewed using a 1K/1K AMT camera attached to a Hitachi H-7100 transmission electron microscope.
To test for the oxidation of lactate coupled with sulfate reduction, mid-exponential phase cells were used to inoculate (5 % inoculum) fresh medium amended with 10 mM lactate and 5 mM sulfate. Negative controls consisted of (i) live cells in fresh medium without lactate, (ii) autoclaved cells added to complete medium (Madigan et al., 1997) and (iii) live cells filtered through a 0.2 µm sterile filter, with the filtrate added to complete medium. Culture tubes were subsampled periodically to estimate cell number and concentrations of H2S, lactate and acetate. Culture densities were estimated spectrophotometrically at 420 nm. Direct cell counting was used to confirm growth on selenate, manganese oxide and Fe(III). Cells were stained with 10 µg 4',6-diamidino-2-phenylindole ml–1 (DAPI; Sigma) and then cells were counted by epifluorescence microscopy using a Zeiss Axioskop. Growth yield was defined as bacterial dry mass obtained from a given amount of substrate, as described by Cypionka & Pfennig (1986).
Oxygen sensitivity was tested by transferring late-exponential phase cells grown on sodium lactate (10 mM) and sodium sulfate (5 mM) into sterile flasks and shaking them under air at 30 °C for 24 h, whereupon they were reintroduced into anoxic medium containing 10 mM lactate and 5 mM sulfate. Growth was monitored as described below. Production of sulfide was assayed by testing for black FeS precipitate upon addition of 0.05 % Fe(NH4)2(SO4)2.
Temperature and pH optima were estimated by culturing cells in basal medium amended with 10 mM sodium lactate and 5 mM sodium sulfate. To determine temperature optima, cells were grown at pH 7.0 at 4, 10, 15, 21, 28, 30, 32, 37, 42 and 45 °C. To determine pH optima, the bicarbonate buffer was replaced with 20 mM (each) HEPES, PIPES, MES and Tris base and the initial medium pH was set using 1 M HCl or 1 M NaOH. Population growth at pH 6.0, 6.5, 7.0 and 7.5 was estimated by following the change in optical density; growth rates were calculated using the linear portion of a semi-logarithmic plot of optical density against time.
Desulfosporosinus strains were evaluated for their ability to grow using the electron donors listed in Table 1. Anaerobic stock solutions (1 M) were prepared for each donor and aliquots were added to defined medium to yield the concentrations indicated. Each donor was tested using sulfate (5 mM) as the terminal electron acceptor. Triplicate experiments were initiated by the addition of 10 % mid-exponential-phase inocula to fresh medium. Change in cell density and sulfide production was monitored as described below. Organisms were considered positive for utilization of an electron donor if 2.5 to 3 doublings occurred after the third passage with simultaneous production of sulfide, as indicated by formation of black precipitate when amended with 0.05 % Fe(NH4)2(SO4)2. Inoculated medium lacking substrate served as a negative control.
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using sodium lactate (10 mM) as a carbon source and electron donor. Anaerobic stock solutions (1 M) were prepared for each electron acceptor and aliquots were added to defined medium to yield the indicated concentrations. Experiments were initiated by the addition of 10 % mid-exponential-phase inocula to fresh medium. Change in cell density and sulfide production was monitored as described herein. Organisms were considered positive for utilization of a given electron acceptor if 2.5 to 3 doublings occurred after the third passage. Inoculated medium lacking electron acceptor served as negative control. Reduction of sulfate, sulfite, sulfur and thiosulfate was tested by adding 0.5 % Fe(NH4)2(SO4)2 to culture tubes. If black FeS precipitate formed, cultures were scored positive for reduction of oxidized sulfur compounds. MnO2 reduction was inferred by a colour change from black MnO2 to white MnCO3, while formation of red elemental selenium precipitate was indicative of Se(VI) reduction. The change in colour from yellow to white due to the formation of siderite (FeCO3) indicated reduction of ferric pyrophosphate [Fe4(P2O7)3] to ferrous iron (Coleman et al., 1993).
To test for sulfur disproportionation, strains were grown in modified Pfennig medium to mid-exponential phase and then inoculated into fresh medium containing 10 mM thiosulfate, bisulfite or elemental sulfur. Growth and sulfur disproportionation were inferred by measuring the change in optical density and by testing for sulfide through addition of 0.05 % Fe(NH4)2(SO4)2 at the end of each experiment. Oxidase and catalase tests were performed as described by Cappuccino & Sherman (1999).
Metal(loid) tolerance was assayed by inoculating medium containing lactate (10 mM) and Na2SO4 (10 mM) along with either Na2HAsO4.7H2O, CdSO4, K2CrO4 or ZnSO4. The amount of metal added was pre-determined using the geochemical equilibrium-modelling program MINTEQA2 (Allison et al., 1991). Prior to inoculation in metal-amended medium, cells were washed in order to remove all previously produced sulfide. Isolates were considered metal-tolerant if the medium turned black due to formation of FeS precipitate following addition of 0.05 % Fe(NH4)2(SO4)2 and cell density increased by more than threefold.
Sulfide (as hydrogen sulfide, H2S) concentration was estimated by spectrophotometric assay of methylene blue as described by Cline (1969). Reduced arsenic [as arsenite, As (III)] was quantified spectrophotometrically at 865 nm using the procedure originally described by Johnson & Pilson (1972), later modified by Niggemyer et al. (2001). Disappearance of lactate and accumulation of acetate in lactate oxidation measurements was determined using ion chromatography. Culture samples were filtered using 0.2 µm filters before injection onto an ICE-AS6 column connected to a Dionex DX500 chromatography system. Heptafluorobutyric acid (0.4 mM) was the eluent and 5 mM tetrabutyl ammonium hydroxide was used to regenerate the column (Dionex Column manual).
Cells were tested for desulfoviridin using a modification of the method described by Postgate (1959); Desulfovibrio desulfuricans ATCC 27774 was used as a positive control and Escherichia coli K-12 as a negative control. For determination of cytochromes and sulfite reductases, 2 l freshly grown culture was gassed with CO2 for 15 min to remove H2S and then centrifuged and the cell pellet was washed with 150 ml KCl. Cell-free extracts were obtained by treatment of cell pellets with a French press and subsequent centrifugation (12 100 g; 30 min). Cytochromes and sulfite reductases were analysed by recording redox difference and carbon monoxide difference spectra using a Lambda 2S spectrophotometer (Perkin Elmer). Separation and identification of b-type and c-type cytochromes were performed as described by Widdel (1980).
Cell-wall preparations were obtained by boiling cells in 20 % (w/v) aqueous trichloroacetic acid solution for 20 min. Diaminopimelic acid isomers were detected in cell-wall hydrolysates (4 M HCl, 100 °C, 16 h) by TLC on cellulose sheets (Merck) using the solvent system of Rhuland et al. (1955). Isoprenoid quinones were analysed as described previously (Groth et al., 1996). Cellular fatty acid patterns were determined from cells grown to stationary phase in DSMZ medium 641 (http://www.dsmz.de/media). Fatty acid methyl esters were obtained from 40 mg (wet weight) of cells by saponification, methylation and extraction as previously described (Kämpfer & Kroppenstedt, 1996; Kroppenstedt, 1985; Miller, 1982). Fatty acid methyl ester mixtures were separated by an automated gas chromatographic system (model 5890 Series II and 7673 autosampler; Agilent) controlled by MIS software (Microbial ID). Peaks were automatically integrated and fatty acid names and percentages were determined using the Microbial Identification standard software package (Sasser, 1990).
Universal primers (E. coli positions 8-27F and 1541R) were used to obtain nearly full-length bacterial 16S rRNA gene fragments from genomic DNA obtained from pure culture isolates of strain STP12T (as described by Rainey et al., 1996). The resulting PCR product was purified using the Prep-A-gene DNA purification kit (Bio-Rad). Sequencing was done on an Applied Biosystems model 373A automated DNA sequencer using the ABI PRISM dye terminator cycle sequencing kit with AmpliTaq FS (Applied Biosystems) according to the manufacturer's instructions. The almost-complete 16S rRNA gene sequence of the novel strain was aligned with sequences included in the ARB database or those obtained from the EMBL nucleotide sequence database (http://www.ebi.ac.uk) using tools implemented in the ARB package. The resulting alignment was inspected visually and potential errors were corrected manually. Evolutionary distances were calculated based on the algorithms of Jukes & Cantor (1969), using neighbour-joining and parsimony methods of tree reconstruction as implemented in the ARB program package. The databases of 16S rRNA gene sequences used in this study, as well as the phylogenetic programs, are available at http://www.arb-home.de
Genomic DNA for the determination of DNA base composition and DNA–DNA hybridization studies was isolated using a French pressure cell and purified by chromatography on hydroxyapatite as described by Cashion et al. (1977). The G+C content was determined by reversed-phase HPLC of nucleosides according to Mesbah et al. (1989). DNA–DNA hybridization studies were carried out according to the method of De Ley et al. (1970) as modified by Huß et al. (1983), using a Gilford System model 2600 spectrophotometer equipped with a Gilford model 2527-R thermoprogrammer and plotter. Renaturation rates were computed with the TRANSFER.BAS program (Jahnke, 1992). Ribotyping of cultures was performed as described previously using the Qualicon RiboPrinter system (DuPont) with PvuII or EcoRI as restriction enzymes (Bruce, 1996).
Morphology and physiology
Like other representatives of the genera Desulfosporosinus and Desulfotomaculum, cells of strain STP12T possessed a Gram-negative cell wall. Cells were curved rods which ranged in length from 2.3 to 3.8 µm and in width from 0.55 to 0.7 µm and which were capable of forming conspicuous endospores (see Supplementary Fig. S1 in IJSEM Online). Flagellation was variable; peritrichous flagella were occasionally observed.
Strain STP12T coupled oxidation of lactate to reduction of sulfate, conserving energy for growth (data not shown), and belonged to physiological group I of the sulfate-reducing bacteria. Such bacteria do not oxidize acetyl CoA to CO2, and therefore excrete acetate. All strains tested utilized lactate and sulfate in a 2 : 1 ratio. No increase in cell number, depletion of lactate or reduction of sulfate was detected in autoclaved controls. The ratios determined and shown in Supplementary Fig. S2 (available in IJSEM Online) indicate a lactate to sulfate ratio of 2 : 1 only at the beginning of the experiment. Above sulfide concentrations of 4 mM, sulfate reduction ceased and lactate seems to be exclusively fermented to acetate. This sulfide sensitivity was already reported for Desulfotomaculum (including Desulfosporosinus) species by Klemps et al. (1985).
Strain STP12T coupled growth to sulfate respiration over the range 4–32 °C, with µmax of 0.08 h–1 at 30 °C. All temperature experiments were conducted at pH 7.0. pH optima were determined at 30 °C as STP12T attained its µmax at that temperature. Sulfidogenic growth of STP12T was confined to the pH range 6.5–7.5, although in other experiments using different media this strain has been observed to grow above pH 8.0 (J. Overmann, unpublished results).
Heat-treated cultures of STP12T incubated in fresh medium increased in cell density and accumulated sulfide. Bacteria were also capable of growth after 24 h of exposure to atmospheric oxygen. These observations can be attributed to the ability of the cells to form high-temperature- and oxygen-resistant endospores.
Electron acceptor and donor preferences for all four strains are summarized in Table 1. All Desulfosporosinus strains tested utilized oxidized inorganic sulfur compounds. Yield of strain STP12T was similar on all three oxidized inorganic sulfur compounds (sulfate, sulfite and thiosulfate) (OD420
0.28). However, unlike certain other Desulfosporosinus strains, STP12T was incapable of using elemental sulfur, fumarate, nitrate or arsenate as electron acceptors. Strain STP12T and D. meridiei DSM 13257T had similar electron donor utilization profiles; STP12T was distinct in that it was able to couple growth to sulfate respiration using glycerol as both electron donor and carbon source. All four Desulfosporosinus strains tested grew on formate, butyrate, pyruvate, lactate, ethanol and yeast extract.
Yield of strain STP12T was 5.5 g dry mass per mol lactate when grown at 25 °C. STP12T also grew autotrophically as a homoacetogen with H2 and CO2. Cell density did not increase and sulfide did not accumulate when cells were cultured on acetate, propionate, fumarate, succinate, malate, glucose or benzoate. STP12T grew fermentatively on either lactate or pyruvate in the absence of sulfate.
The novel isolate failed to disproportionate sulfur presented in the form of thiosulfate, bisulfite or elemental sulfur. Lack of growth and sulfide production were inferred by the absence of change in OD420 and the absence of black FeS precipitate following addition of 0.05 % Fe(NH4)2(SO4)2 at the end of each experiment. The novel sulfate reducer STP12T was both catalase- and oxidase-negative.
Under circumneutral, low Eh conditions, the production of H2S by sulfate reducers immobilizes solution-phase metal(loid)s as insoluble precipitates. Sulfate reducers have therefore been proposed as agents for accelerated bioremediation of metal-contaminated soils and sediments. With a view towards evaluating their potential in these contexts, we tested the tolerance of STP12T and its congeners to arsenic, cadmium, zinc and chromium. Results for the four strains are summarized in Supplementary Table S1 available in IJSEM Online. Activity and growth were inferred from the presence of sulfide and change over time in DAPI cell counts. No bacteria tested grew in the presence of Cr, even at the lowest concentration tested (0.4 mM). On the other hand, no strain tested failed to grow in the presence of 2 mM As(V). Among Desulfosporosinus strains, only strain STP12T failed to grow in the presence of 10 mM As(V). Electron acceptor assays, however, clearly demonstrated that only D. auripigmenti DSM 13351T had the capacity for dissimilatory As(V) reduction (data not shown). The highest concentration tested for cadmium (10 µM) inhibited growth of all strains except D. auripigmenti DSM 13351T. Of all cultures tested, only STP12T failed to grow in the presence of 50 µM zinc, the highest concentration assayed. STP12T was inhibited even in the presence of 10 µM zinc.
Chemotaxonomy
Cellular fatty acid composition profiles for the novel strain and its three congeners are displayed in Table 2. Fatty acid 16 : 1cis9 (26.3 %) predominated in STP12T. The diagnostic amino acid of STP12T peptidoglycan was LL-diaminopimelic acid. Isoprenoid quinones MK-7 and MK-5 were present in the ratio of 64 : 36 (ratio of peak areas) in strain STP12T. STP12T demonstrated P582-type sulfite reductases having absorption maxima at 592 nm, and c-type cytochromes (
max 553 nm), although traces of b-type cytochromes were also observed in cell-free extracts.
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). These patterns have been shown to discriminate among closely related bacterial strains (Scott et al., 2003). The ribotype pattern of strain STP12T was distinct from the type strains of the other described Desulfosporosinus species (data not shown). The DNA G+C content of strain STP12T was 42.7 mol%.
Fig. 1 depicts phylogenetic relationships for the novel strain. Sequence similarity values based on the comparison of almost-complete 16S rRNA gene sequences indicate that strain STP12T is 96.5 % similar to D. meridiei DSM 13257T, 96.4 % similar to D. orientis DSM 765T and 96.7 % similar to D. auripigmenti DSM 13351T.
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Description of Desulfosporosinus lacus sp. nov.
Desulfosporosinus lacus (la'cus. L. n. lacus -us a lake; L. gen. n. lacus of a lake).
Cells are rod-shaped, stain Gram-negative and have peritrichous flagella. Individual cell dimensions vary from 0.55 to 0.7 µm in width and 2.3 to 3.8 µm in length. They produce heat-resistant endospores that are oval and subterminal and which sometimes cause the cells to swell. Utilizes sulfate, sulfite, thiosulfate and Fe(III) as terminal electron acceptors in the presence of lactate. Arsenate, fumarate, nitrate, sulfur, selenate and Mn(IV) are not used as electron acceptors. In the presence of sulfate, H2/CO2, H2/CO2 plus acetate, formate, butyrate, pyruvate, lactate, ethanol, methanol, yeast extract and glycerol are utilized as electron donors and carbon sources. Cannot use acetate, propionate, benzoate, fumarate, succinate, malate or glucose as electron donors or carbon sources. Cells are capable of fermentative growth using pyruvate and lactate as energy sources in the absence of any electron acceptor. The temperature and pH ranges for growth are 4–32 °C and pH 6.5–7.5. Possesses a P582-type sulfite reductase and c-type cytochromes with traces of b-type cytochromes. The diagnostic diamino acid of the peptidoglycan is LL-diaminopimelic acid. The predominant whole-cell fatty acids are 16 : 1cis9, 16 : 0, 18 : 1cis11, 16 : 1cis7. The major isoprenoid quinones are MK-7 and MK-5. The DNA G+C content of the type strain is 42.7 mol%.
The type strain, STP12T (=DSM 15449T=JCM 12239T), was isolated from sediment of Lake Stechlin (northern Germany).
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ACKNOWLEDGEMENTS |
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