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nba
1,2
1 Laboratory of Microbiology, Wageningen University, Dreijenplein 10, 6703 HB Wageningen, The Netherlands
2 Department of Environmental Engineering, Istanbul Technical University, 34469 Maslak, Istanbul, Turkey
3 Department of Marine Biogeochemistry and Toxicology, Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg (Texel), The Netherlands
Correspondence
Melike Balk
Melike.Balk{at}wur.nl
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain HB1T is DQ146482.
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Canfield et al., 1993; Thamdrup & Canfield, 1996; Rysgaard et al., 1998; Kostka et al., 1999; Glud et al., 2000; Rabus et al., 2006). Bacterial sulfate-reducers fall into different branches, the Deltaproteobacteria, with more than 25 genera, the Gram-positive bacteria, including genera such as Desulfotomaculum (Campbell & Postgate, 1965) and Thermodesulfobium (Mori et al., 2003), and Gram-negative sulfate-reducers such as the genera Thermodesulfobacterium (Zeikus et al., 1983) and Thermodesulfatator (Moussard et al., 2004) within the class Thermodesulfobacteria and Thermodesulfovibrio (Henry et al., 1994) within the class ‘Nitrospira’.
Although the Deltaproteobacteria is not a large assemblage of genera, its members show considerable morphological and physiological diversity (Rabus et al., 2006). Members of the family Desulfobacteraceae in the order Desulfobacterales are widely distributed in freshwater, marine, hypersaline and oil- or hydrocarbon-polluted sediments (Bak & Widdel, 1986; Brysch et al., 1987; Szewzyk & Pfennig, 1987; Gogotova & Vainstein, 1989; Schnell et al., 1989; Rees & Patel, 2001; Cravo-Laureau et al., 2004; Kjeldsen et al., 2007). These bacteria are anaerobic, mesophilic, Gram-negative, oval to coccoid, slightly curved or rod-shaped and grow optimally at 20–35 °C. A wide variety of substrates including alcohols, fatty acids and aromatic and aliphatic compounds can be utilized by this group of organisms (Kuever et al., 2005). Members of the family Desulfobacteraceae play an important role in the degradation of volatile fatty acids in anaerobic bioreactors treating sulfate-rich wastewaters, such as those from paper mills, tanneries or the food oil industry (Oude Elferink et al., 1994; Colleran et al., 1995; Roest et al., 2005). Acetate and butyrate are important intermediates in the anaerobic degradation of wastewaters. Some bacteria in the family Desulfobacteraceae are able to oxidize butyrate either incompletely to acetate or completely to carbon dioxide with concomitant reduction of sulfate to sulfide (Stieb & Schink, 1989; Platen et al., 1990; Brandt et al., 1999).
The microbial community of an upflow anaerobic sludge blanket (UASB) reactor treating paper-mill wastewater (Industriewater, Eerbeek, The Netherlands) was investigated. In this reactor, both sulfate reduction and methanogenesis have been found to be important (Oude Elferink et al., 1998). In a previous study, the dominant micro-organisms present in the anaerobic paper-mill wastewater treatment system were assessed by molecular techniques (Roest et al. 2005). As it was not clear from these earlier molecular studies which bacteria were involved in butyrate degradation with sulfate, in the present study, particular attention was paid to bacteria that are able to degrade butyrate with sulfate. Here, we report the taxonomic characterization of strain HB1T, which was isolated from granular sludge of the full-scale mesophilic UASB reactor at Eerbeek. Detailed characteristics of the granular sludge were described previously by Oude Elferink et al. (1998). About 10 ml granular sludge was disintegrated by a Potter homogenizer (Tamson). Serial dilutions of the homogenized sample were prepared in a bicarbonate-buffered anaerobic medium containing sodium butyrate and sodium sulfate. Bacterial growth was evident at a dilution of 10–8 of the incubation at 37 °C within 30 days.
Dilution series were made in a basal bicarbonate-buffered medium containing 10 mM sodium butyrate with 20 mM sodium sulfate. The basal liquid culture medium contained (g l–1 unless indicated): NaCl (7), NaHCO3 (4), Na2SO4 (2.8), MgCl2 . 6H2O (1.2), KCl (0.5), NH4Cl (0.3), KH2PO4 (0.2), CaCl2 (0.15), Na2S . 7–9H2O (0.3), yeast extract (0.02), selenite/tungstate solution (1 ml l–1) (Widdel & Bak, 1992) and a trace element solution (1 ml l–1) containing (mg l–1 unless indicated): FeCl2 . 4H2O (1500), CoCl2 . 2H2O (190), MnCl2 . 4H2O (100), ZnCl2 (70), H3BO3 (62), Na2MoO4 . 2H2O (36), NiCl2 . 6H2O (24), CuCl2 . 2H2O (17), EDTA (500) and 37 % HCl (7 ml l–1). In addition, vitamins were added from a concentrated stock solution according to Stams et al. (1983). The cultures were grown routinely in 117 ml serum vials with butyl rubber stoppers and aluminium crimp seals. The vials contained 50 ml basal medium and a gas phase of 1.7 bar N2/CO2 or H2/CO2 (80/20 %, v/v). Concentrated stock solutions of substrates were prepared anoxically, sterilized by filtration and added to the medium to final concentrations of 5–20 mM. Besides the substrates, vitamins, CaCl2, NaHCO3 and Na2S . 7–9H2O were added from stock solutions after sterilization of the medium. The pH of the medium was 7. Unless stated otherwise, all cultivations were carried out at 30 °C.
For isolation, the enriched culture was incubated in the presence of butyrate by using the soft-agar dilution method. This procedure was applied in 117 ml serum vials. Colonies, which were visible after 1 month of incubation, were picked with a sterile needle and subcultured in liquid medium containing butyrate and sulfate. The colonies were about 1 mm in diameter, lens-shaped and brownish. Serial agar and liquid dilutions were repeated until a pure culture was obtained.
Microscope observations were performed with a Leica DC250 photomicroscope. Cells of strain HB1T were oval to rod-shaped, 1–1.3 µm wide and 2.6–3.5 µm long, depending on the growth phase (Fig. 1). The cells stained Gram-negative (Murray et al., 1994). The cells were non-spore-forming and occurred singly, in pairs or in long chains.
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Temperature limits for growth were determined by culture incubation from 10 to 65 °C in the basal medium. The pH limits for growth were determined in the same medium adjusted to pH values between 5 and 9 by changing the CO2 content of the gas phase. The dependence of growth on NaCl concentration was determined in basal medium containing NaCl at concentrations ranging from 0 to 40 g l–1. Under optimal conditions, the doubling time of the isolate in media with butyrate and sulfate was about 130 h (µmax=0.0037 h–1) and the final cell density (OD600) was about 0.38.
Strain HB1T was mesophilic. Growth occurred between 15 and 37 °C, with an optimum growth temperature of 28–30 °C. Growth was possible at pH 6.5–8.0, with an optimum at pH 7.0. Growth was observed in 0–15 g NaCl l–1, with an optimum around 5 g NaCl l–1.
The G+C content of the DNA was determined by using standard HPLC analysis (Mesbah et al., 1989) at the Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH (Braunschweig, Germany). Genomic DNA was isolated according to the procedure of Cashion et al. (1977).
Organic compounds were measured by HPLC as described previously by Stams et al., (1993). Gases and alcohols were measured by gas chromatography (Balk et al., 2003; Henstra & Stams, 2004) and thiosulfate, nitrate and sulfate were analysed by an HPLC system equipped with an Ionpac AS9-SC column and an ED 40 electrochemical detector (Dionex) (Scholten & Stams, 1995). Sulfide was analysed by the method of Trüper & Schlegel (1964).
Strain HB1T used the following substrates as electron donors and carbon sources (tested at 20 mM, unless indicated): H2/acetate (1.7 bar/2 mM), formate, ethanol (5 mM), propionate, 1-propanol (5 mM), 1-butanol (5 mM), 2,3-butandiol (5 mM), fumarate, succinate, butyrate (10 mM), crotonate, catechol (0.5 mM), phenol (1 mM), benzoate (3 mM), 4-hydroxybenzoate (3 mM), palmitate (5 mM) and stearate (2 mM). Growth on ethanol, propionate, crotonate and benzoate was much faster than on butyrate. Growth on pyruvate and crotonate was possible without an electron acceptor. The strain was not able to grow on H2/CO2, methanol, acetone, lactate, malate, glucose or fructose. Slight growth was observed on acetate in the presence of sulfate. A maximum 2 mM acetate was utilized by strain HB1T during 3 weeks of incubation and acetate was not fully oxidized, even after longer incubations. Aromatic compounds including catechol, phenol, benzoate and 4-hydroxybenzoate were oxidized completely by strain HB1T.
Sulfate (20 mM) and thiosulfate (20 mM) were used as electron acceptors, but nitrate (10 mM), sulfite (5 mM) and elemental sulfur (0.5 g l–1) were not. Thiosulfate and sulfite were not disproportionated.
Butyrate was oxidized completely by strain HB1T. After 28 days of incubation in the presence of sulfate, no acetate was detected, and the molar ratio of the butyrate oxidized (7.2 mmol) to sulfide formed (16.0 mmol) of 1 : 2.23 was close to the expected theoretical values for the complete oxidation of butyrate according to the following reaction:
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. PCR was performed with the bacterial primers 7f and 1510r (Lane, 1991) by using the Taq DNA polymerase kit (Life Technologies) to amplify the bacterial 16S rRNA gene. PCR products were purified with the QIAquick PCR purification kit (Qiagen) according to the manufacturer's instructions. Sequencing of the complete 16S rRNA gene was performed at Westburg Genomics (http://genomics.westburg.nl). A total of 1535 nucleotides of the 16S rRNA gene were sequenced. The sequences were checked for reading errors with the alignment programs of the ARB package (Ludwig et al. 2004), and a rooted neighbour-joining tree was constructed using Escherichia coli ATCC 11775T as an outgroup (Fig. 2). Online similarity analysis of the 16S rRNA gene sequences was performed with the BLAST program at the GenBank and EMBL databases. The closest phylogenetic relatives of strain HB1T were Desulfococcus multivorans DSM 2059T, Desulfococcus biacutus DSM 5651T (sequence similarity of 91 % to both) and Desulfobacterium indolicum DSM 3383T (90 %) (Fig. 2).
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). After saponification of the residue, β-hydroxy fatty acids were also present in the range of C14 : 0 to C18 : 0, of which C16 : 0 was the most abundant. The C35 lipid bacteriohopanetetrol was also present in small amounts (approx. 1 % of total lipids).
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), but the lipid profile of Desulfococcus multivorans differs from that of strain HB1T by the predominance of anteiso-C17 : 0. The predominant fatty acids of strain HB1T were iso-C15 : 0 and anteiso-C15 : 0. This is not the case for Desulfobacterium species grown on benzoate (Kohring et al., 1994). Bacteriohopanetetrol derivatives have recently been identified in sulfate reducers (Blumenberg et al. 2006); the presence of this lipid in strain HB1T fits this pattern.
Based on morphological and physiological differences from members of the class Deltaproteobacteria, it is proposed that strain HB1T represents a novel species in a new genus. Characteristics that differentiate strain HB1T from phylogenetically related species are given in Table 2; other detailed characteristics determined are given in the species description below.
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). Therefore, we propose that isolate HB1T should be classified as representing a novel species in a new genus, Desulfatirhabdium butyrativorans gen. nov., sp. nov., within the family Desulfobacteraceae, class Deltaproteobacteria.
Description of Desulfatirhabdium gen. nov.
Desulfatirhabdium (De.sul.fa'ti.rhab'di.um. L. pref. de- from; N.L. masc. n. sulfas -atis sulfate; Gr. neut. n. rhabdium a little rod; N.L. neut. n. Desulfatirhabdium a sulfate-reducing small rod).
Cells are anaerobic, Gram-negative, non-spore-forming and oval to rod-shaped. Thiosulfate and sulfate are reduced to sulfide. Volatile fatty acids are oxidized completely. Predominant cellular fatty acids are iso-C15 : 0, anteiso-C15 : 0, C16 : 0 and C14 : 0. Phylogenetically, the genus belongs to the family Desulfobacteraceae in the class Deltaproteobacteria. The type species is Desulfatirhabdium butyrativorans.
Description of Desulfatirhabdium butyrativorans sp. nov.
Desulfatirhabdium butyrativorans (bu.ty.ra.ti.vo'rans. N.L. n. butyras -atis butyrate; L. part. adj. vorans devouring; N.L. part. adj. butyrativorans butyrate-devouring).
Displays the following properties in addition to those described for the genus. Cells are 1–1.3x2.6–3.5 µm. Colonies are brownish, lens-shaped in the agar after about 1 month of incubation. Growth occurs at 15–37 °C (optimum 28–30 °C) and pH 6.5–8.0 (optimum pH 7.0). Growth occurs at NaCl concentrations of 0–15 g NaCl l–1, with an optimum at 5 g NaCl l–1. Sulfate and thiosulfate are used as electron acceptors. In the presence of an electron acceptor, growth occurs on H2/acetate (1.7 bar/2 mM), formate (20 mM), ethanol (5 mM), pyruvate (20 mM), propionate (20 mM), propanol (5 mM), 1-butanol (5 mM), 2,3-butandiol (5 mM), fumarate (20 mM), succinate (20 mM), 1-butyrate (10 mM), crotonate (20 mM), catechol (0.5 mM), phenol (1 mM), benzoate (3 mM), 4-hydroxybenzoate (3 mM), palmitate (5 mM) and stearate (2 mM). Only slight growth is observed on acetate. Fermentative growth occurs on pyruvate and crotonate. Not able to grow on H2/CO2, methanol, acetone, lactate, malate, glucose or fructose. β-Hydroxy fatty acids are present in the range of C14 : 0 to C18 : 0, of which C16 : 0 was the most abundant. The DNA G+C content of the type strain is 55.1 mol%.
The type strain, HB1T (=DSM 18734T =JCM 14470T), was isolated from a UASB reactor treating paper-mill wastewater operated at 37 °C with butyrate as the energy source.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTMAIN TEXTREFERENCES |
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