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Desulfovirga Adipica Gen. Nov., Sp. Nov., an Adipate-Degrading, Gram-Negative, Sulfate-Reducing Bacterium

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Desulfovirga Adipica Gen. Nov., Sp. Nov., an Adipate-Degrading, Gram-Negative, Sulfate-Reducing Bacterium International Journal of Systematic and Evolutionary Microbiology (2000), 50, 639–644 Printed in Great Britain Desulfovirga adipica gen. nov., sp. nov., an adipate-degrading, Gram-negative, sulfate-reducing bacterium Kazuhiro Tanaka,1 Erko Stackebrandt,2 Shigehiro Tohyama3 and Tadashi Eguchi3 Author for correspondence: Kazuhiro Tanaka. Tel\Fax: j81 298 61 6083. e-mail: ktanaka!nibh.go.jp 1 Applied Microbiology A novel, mesophilic, Gram-negative bacterium was isolated from an anaerobic Department, National digestor for municipal wastewater. The bacterium degraded adipate in the Institute of Bioscience and Human-Technology, presence of sulfate, sulfite, thiosulfate and elemental sulfur. (E)-2- Higashi 1-1, Tsukuba, Hexenedioate accumulated transiently in the degradation of adipate. (E)-2- Ibaraki 305-8566, Japan Hexenedioate, (E)-3-hexenedioate, pyruvate, lactate, C1–C12 straight-chain fatty 2 Deutsche Sammlung von acids and C2–C10 straight-chain primary alcohols were also utilized as electron Mikroorganismen und donors. 3-Phenylpropionate was oxidized to benzoate. The GMC content of the Zellkulturen GmbH, Mascheroder Weg 1b, DNA was 60 mol%. 16S rDNA sequence analysis revealed that the new isolate D-38124 Braunschweig, clustered with species of the genus Syntrophobacter and Desulforhabdus Germany amnigenus. Strain TsuAS1T resembles Desulforhabdus amnigenus DSM 10338T 3 Department of Chemistry with respect to the ability to utilize acetate as an electron donor and the and Materials Science, inability to utilize propionate without sulfate in co-culture with Tokyo Institute of T T Technology, O-okayama, Methanospirillum hungatei DSM 864. Strains TsuAS1 and DSM 10338 form a Meguro-ku, Tokyo ‘non-syntrophic subcluster’ within the genus Syntrophobacter. Desulfovirga 152-8551, Japan adipica gen. nov., sp. nov. is proposed for the newly isolated bacterium, with strain TsuAS1T (l DSM 12016T) as the type strain. Keywords: adipic acid, sulfate reduction, anaerobic digestor, mesophilic bacterium, Desulfovirga adipica INTRODUCTION METHODS Source of the isolate and micro-organisms. Strain TsuAS1T Adipic acid is a natural product contained in the lichen was isolated from an anaerobic digestor of a municipal Cetraria islandica (Solberg, 1986) and in leaves of the wastewater treatment centre in Tsuchiura, Ibaraki, Japan, plant Limonia acidissima (Das & Thakur, 1989). This and was deposited in the Deutsche Sammlung von Mikro- acid is also synthesized industrially as a raw material to organismen und Zellkulturen, Braunschweig, Germany, as synthesize polymers such as ‘nylon 6,6’ and poly- strain DSM 12016T. Methanospirillum hungatei strain JF1 urethanes, and plasticizers such as di(2-ethylhexyl)- (DSM 864) was provided by Y. Kamagata (NIBH, Japan). adipate, all of which are important industrial products. Chemicals. (E)- and (Z)-2-hexenedioates were synthesized as This acid is known to be degraded aerobically, for follows. γ-Butyrolactone was treated with p-toluenesulfonic example by Pseudomonas aeruginosa, Acidovorax dela- acid in ethanol to give ethyl 4-hydroxybutyrate. Oxidation fieldii and ‘Pseudomonas saccharophila’ (Palleroni, of ethyl 4-hydroxybutyrate by DMSO-oxalyl chloride\ 1984). To the authors’ knowledge, however, its an- triethylamine afforded an intermediary aldehyde, which was aerobic degradation by a pure culture of a sulfate subjected to the Wittig reaction with (carbethoxymethylene)- reducer has not been documented. Here, we describe triphenylphosphorane in methanol to give a mixture of the isolation and characterization of a novel Gram- diethyl (E)- and (Z)-2-hexenedioates (about 2:1). After negative, mesophilic and sulfate-reducing strain chromatographic separation over silica gel, each isomer was capable of growing by completely oxidizing adipate. finally hydrolysed with lithium hydroxide, followed by acid treatment to give the desired (E)- and (Z)-2-hexenedioic acids. ................................................................................................................................................. The GenBank/DDBJ accession number for the 16S rDNA gene sequence of (E)-2-Hexenedioic acid: colourless powder; m.p. 179– " strain TsuAS1T is AJ237605. 180 mC; H NMR (500 MHz, DMSO-d')d2n37 (m, 4H), 5n76 01226 # 2000 IUMS 639 K. Tanaka and others (broad d, J 15 6 Hz, 1H), 6 80 (m, 1H), 12 13 (broad s, Light microscopy. Cells were observed with an Olympus BH- "$ l n n n 2H); C NMR (125 MHz, DMSO-d')d26n9, 32n1, 122n5, 2 phase-contrast microscope. Micrographs were taken after 147n4, 167n1, 173n6; IR (KBr), 2923, 1689, 1647, 1421, 1321, mounting cultures on glass slides coated with 2% agar −" 1214 cm . Elemental analysis. Calculated for C'H)O%:C, (Pfennig & Wagener, 1986). 50 00; H, 5 59. Found: C, 50 29; H, 5 77. (s, singlet; d, n n n n Electron microscopy. Cells on the grid were negatively stained doublet; m, multiplet) with 1% uranyl acetate. Photographs were taken using a (Z)-2-Hexenedioic acid: colourless powder; m.p. 78–80 C; JEM-1010 transmission electron microscope (JEOL) at " m H NMR (500 MHz, DMSO-d')d2n33(t, J l 7n4 Hz, 2H), 100 kV. 2 74 (dq, J 1 7 and 7 4 Hz, 2H), 5 72 (dt, J 11 5 and n l n n n l n Analysis of adipate and metabolic products. Determination 1 7 Hz, 1H), 6 19 (dt, J 11 5 and 7 4 Hz, 1H), 12 14 (broad n "$ n l n n n of adipate, (E)-2-hexenedioate and (Z)-2-hexenedioate was s, 2H); C NMR (125 MHz, DMSO-d )d242, 33 1, 121 3, ' n n n carried out as follows. Culture fluid (1 0 ml) was centrifuged 147 8, 167 2, 173 9; IR (KBr), 2939, 1701, 1649, 1604, 1450, n n n n " in a 1 5 ml polypropylene tube. Then, 0 45 ml supernatant 1419, 1389, 1300, 1261, 1226, 1160 cm− . Elemental analysis. n n was transferred to a new 1 5 ml polypropylene tube and Calculated for C H O :C,5000; H, 5 59. Found: C, 50 24; n ' ) % n n n acidified with 50 µl1MHPO , followed by analysis of the H, 5 77. (s, singlet; d, doublet; t, triplet; dt, double triplet;dq, $ % n acidified supernatant by HPLC using a 6 150 mm Shim- double quartet) i pack CLC-ODS column (Shimadzu) at 40 mC, 9 mM −" Hexanoic acid and heptanoic acid were purchased from H$PO%\2n5% (v\v) methanol as eluant at 1 ml min , and a Wako and Aldrich, respectively. UV detector at 210 nm. Benzoate was determined similarly, except 3 mM H PO \49% methanol was as eluant (Tanaka Culture conditions. Strain TsuAS1T was cultured using the $ % et al., 1991). Sulfide was determined spectrophotometrically Hungate technique (Bryant, 1972). A basal medium con- via a method yielding methylene blue (Cline, 1969). tained 2 mM Na#S, 1 µM resazurin, 30 mM NaHCO$, 1mMNH%Cl, 1 mM KH#PO%, 1 mM MgCl#, 1 mM CaCl#, Pigment analysis. Desulfoviridin was determined as de- 10 µM FeCl#,1µM CoCl#,1µM MnCl#,1µM ZnCl#, scribed by Postgate (1956). Cytochromes were identified by 100 nM H$BO$, 100 nM NiCl#, 100 nM Na#MoO%, 100 nM taking redox difference spectra of dithionite-reduced minus AlCl$,10nMNa#SeO$,10nMNa#WO%, 10 nM CuCl#, air-oxidized cell-free extracts with a Shimadzu UV-1600PC 100 nM biotin, 100 nM 4-aminobenzoic acid, 100 nM pan- spectrophotometer. tothenic acid, 100 nM pyridoxine, 100 nM nicotinic acid, Isolation of DNA and base composition. Cells were lysed by 100 nM thiamine, 100 nM lipoic acid, 100 nM folic acid, treatment with achromopeptidase and SDS (Ezaki et al., 100 nM riboflavin and 100 nM vitamin B , under an "# 1990). DNA was isolated from the resultant lysate (Marmur, atmosphere of N \CO (80:20, v\v). The medium was # # 1961) and base composition of DNA was determined using prepared using a Widdel flask (Widdel & Bak, 1992). The pH HPLC (Tamaoka & Komagata, 1984; Kamagata et al., of the basal medium was 6 9–7 1 unless otherwise stated. n n 1992). When pH dependence was studied, the N#\CO# ratio was varied in a range between 100:0 and 50:50. For sulfate 16S rDNA sequence determination. Genomic DNA extrac- reduction, 5 mM sodium sulfate was added unless otherwise tion, PCR-mediated amplification of the 16S rDNA and stated. A time course study was carried out using half-filled sequencing of the PCR products were performed as de- 130 ml serum bottles in duplicate. Substrate tests were scribed by Rainey et al. (1996). The sequence reaction carried out using half-filled 20 ml Pyrex tubes in duplicate mixtures were electrophoresed using a model 373A auto- for water-soluble substrates. Lipophilic substrates such as matic DNA sequencer (Applied Biosystems). decanoic acid (5 mM), undecanoic acid (5 mM), dodecanoic Phylogenetic analysis. The 16S rDNA sequence of strain acid (5 mM), tridecanoic acid (5 mM), 1-hexanol (10 mM), T 1-heptanol (5 mM), 1-octanol (5 mM), 1-nonanol (5 mM), TsuAS1 was aligned to the sequences of a general selection 1-decanol (5 mM), 1-undecanol (5 mM), 2-phenylethanol of different bacteria in the DSMZ identification database, δ (50 mM), 2-phenylpropanol (50 mM) and indole (10 mM) and analysed against members and relatives of the -subclass Proteobacteria et al were prepared in sterile stock solutions in decahydro- of the using the ae2 editor (Maidak ., naphthalene at the concentrations indicated. A test tube for 1997). Evolutionary distances were calculated by the method of Jukes & Cantor (1969). Phylogenetic dendrograms were the lipophilic substrate test was prepared to contain 2n0ml substrate solution and 19 2 ml basal medium in a 25 mm constructed according to the method of DeSoete (1983) and n the neighbour-joining method contained in the (o.d.)i150 mm order-made screw-capped tube plugged with a Teflon-coated butyl rubber stopper, which was then package (Felsenstein, 1993). inoculated with 0n8 ml preculture to give a final aqueous volume of 20n0 ml. In this case, one-tenth of the substrate RESULTS concentration in decahydronaphthalene is given in par- entheses in Results to make it easy to compare with results Enrichment and isolation with hydrophilic substrates.
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