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Three Strains of Sulfate-Reducing Bacteria Utilizing H2 As the Electron

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Three Strains of Sulfate-Reducing Bacteria Utilizing H2 As the Electron J. Gen. Appl. MicrobioI., 42, 109-120 (1996) PHYSIOLOGICAL PROPERTIES OF A SULFATE-REDUCING BACTERIUM ISOLATED FROM MUNICIPAL SEWAGE SLUDGE AND ITS POSSIBLE ROLE AS A SYNTROPHIC ACIDOGEN IN THE ECOSYSTEM MANABU NAKAMOTO, ATSUKO UEKI, AND KATSUJI UEKI* Department of Bioproduction, Faculty of Agriculture, Yamagata University, Tsuruoka 997, Japan (Received August 10, 1995; Accepted December 22, 1995) Three strains of sulfate-reducing bacteria utilizing H2 as the electron donor of sulfate reduction were isolated from anaerobic digester slurry of municipal sewage sludge. The isolates were Gram-negative, non-spore- forming, motile, curved rods with a single polar flagellum. Cytochrome c3 and desulfoviridin were present. The DNA base compositions (mol% G + C) were 59.6±0.7. The isolates used H2, formate, lactate, pyruvate, fumarate, malate, alcohols and amino acids as the electron donor for sulfate reduction. Alcohols were oxidized to corresponding mono- carboxylates, and other organic compounds were to acetate. Sulfate, sulfite and thiosulfate, but not nitrate, were used as the electron acceptor and reduced to sulfide. The isolates grew with pyruvate, fumarate, or malate as the energy source in the absence of oxidized sulfur compounds. Pyruvate was oxidized to acetate with the production of formate and H2. Fumarate and malate were oxidized to acetate, and the oxidation was coupled with the reduction of fumarate or malate to succinate. From the morphological and physiological properties, the isolates were considered to belong to a Desulfovibrio sp. In association with Methanobacterium formicicum as a hydrogen-consuming partner, one of the isolates could also grow in the absence of oxidized sulfur compounds by utilizing organic substrates other than pyruvate, malate and fumarate. In the coculture of the isolate and the methanogen, all the organic compounds other than malate and fumarate, which could serve as the electron donor for sulfate reduction in the pure culture of isolates, were syntrophically oxidized with the production of methane. These results indicate that the isolates of sulfate-reducing bacteria can play a role as a syntrophic * Address reprint requests to: Dr . Katsuji Ueki, Department of Bioproduction, Faculty of Agriculture, Yamagata University, 1-23 Wakaba-machi, Tsuruoka 997, Japan. 109 110 NAKAMOTO, UEKI, and UEKI VOL. 42 degrader of a wide range of organic compounds in the methanogenic sewage sludge devoid of sulfate. Sulfate-reducing bacteria, as well as methanogens, can play a role as the terminal hydrogen-scavenger in the anaerobic degradation process of organic matter. There are many reports on the competition between sulfate reduction and methanogenesis for the utilization of electron donors in various anaerobic environ- ments, and sulfate reduction is generally thought to dominate methanogenesis due to the differences in kinetic and thermodynamic properties (1, 6, 7, 10,11). As reported previously (15,17-20), however, sulfate reduction does not appar- ently compete with methanogenesis in nutritionally rich environments such as the anaerobic digester slurry of municipal sewage sludge or cattle waste, even when sulfate reduction was markedly enhanced by adding sulfate to the slurry. Sulfate- reducing bacteria can be generally enumerated at relatively high densities (>i0 5 cells/ml) in such environments even practically devoid of sulfate (18,20). Besides, it is known that some strains of sulfate-reducing bacteria can grow as the syntrophic degrader of lactate and ethanol (2, 4, 5), or propanediols and glycerol (9) in coculture with the hydrogenotrophic methanogen in the absence of oxidized sulfur compounds. These facts may provide insight into the ecological role of sulfate- reducing bacteria as the syntrophic acidogen in various methanogenic environments devoid of sulfate. In the present study, three strains of sulfate-reducing bacteria utilizing H2 as the electron donor for sulfate reduction were isolated from anaerobic digester slurry of municipal sewage sludge and characterized. The ability of the sulfate- reducing bacteria to grow as the syntroph in a binary coculture with a hydrogen- utilizing methanogen, Met hanobacterium formicicum, was examined, and a possible role of the sulfate-reducing bacteria as the syntrophic acidogen in the methanogenic digester slurry was discussed. MATERIALS AND METHODS Organisms. Three strains (HS-l, HS-2, HS-3) of sulfate-reducing bacteria were isolated from anaerobic digester slurry of municipal sewage sludge sampled from an anaerobic digester in the Wastewater Treatment Center of Tsuruoka City in Japan. Desulfovibrio vulgaris NCIMB 8303 and Desulfovibrio desulfuricans NCIMB 8307 were obtained from the National Collection of Industrial and Marine Bacteria (Scotland, U.K.), and Methanobacterium formicicum DSM 1535 was from the Deutsche Sammlung von Mikroorganismen GmbH (Braunschweig, Germany). Media and culture conditions. All procedures for cultivation of bacteria were carried out under strictly anoxic conditions. Cultures (ca. 10 ml) were grown at 30°C under 02-free atmosphere in test tubes (18>< 180 mm) sealed with butylrubber double stoppers. 1996 Syntrophic Role of Sulfate-reducing Bacteria 111 For the cultivation of sulfate-reducing bacteria, the basal medium (16) con- taining (per liter) 0.5 g KH2PO4, 1.0 g NH4C1, 1.0 g Na2SO4, 2.0 g MgSO4.7H2O, 0.1 g CaC12.2H2O, 0.5 g yeast extract (Difco Lab., Detroit, MI, U.S.A.), 10 ml trace element solution, 1 ml vitamin solution, 0.5 g cysteine-HCI, and 1 mg resazur- in-Na was amended with various organic compounds or H2 as the electron donor. The pH was adjusted to 7.2-7.4. Sulfate-reducing bacteria were usually main- tained on the medium with Na-lactate (20 mM) or H2 as the electron donor under 02-free N2 or H2/N2 (40/60, v/v) atmosphere, respectively. In experiments for substrate utilization, cultures (0.5 ml) grown with H2 as the electron donor for sulfate reduction were inoculated to fresh media (10 ml) amended with organic compounds as the electron donor and incubated at 30°C on a reciprocal shaker, unless otherwise stated. Sulfate-reducing bacteria were isolated from the anaerobic digester slurry of municipal sewage sludge by the anaerobic roll tube method. The medium for sulfate-reducing bacteria was used with H2 as the electron donor, except that cysteine-HC1 was omitted and 0.1 g Na-thioglycollate, 0.1 g ascorbic acid, 2.5 g Na2S204, and 2.5g FeSO4(NH4)2SOe6H2O (per liter) were added (16). Black colonies formed on roll tubes inoculated with 0.3 ml of 105 dilutions of the digester slurry were picked up and purified by repeating the colony isolation by the roll tube method. For the cultivation of M formicicum DSM 1535, the basal medium (DSM 119, modified) containing (per liter) 0.5 g KH2PO4, 0.6 g NH4C1, 0.4 g NaCI, 0.2 g MgC12.6H2O, 0.05 g CaCl2.2H2O, 5 mg FeCl2.4H2O, 1.0 g yeast extract (Difco Lab.), 1.0g Trypticase (BBL, Cockeysville, MD, U.S.A.), 10 ml trace element solution, 1 ml vitamin solution, 0.3 g cysteine-HCI, 0.3 g Na2S, and 1 mg resazurin- Na was used. The medium with H2 or Na-formate (40 mM) as the energy source was used under H2/C02 (80/20, v/v) or N2/C02 (80/20, v/v) atmosphere, respective- ly. The pH was adjusted to 7.0. For the coculture of strain HS-1 plus M formicicum, the media (chlorides were substituted for sulfates) amended with various organic compounds (20 mM) as the electron donor were used under N2/C02 (80/20, v/v) atmosphere. Strain HS-1 and M formicicum were separately grown with H2, and then the cultures (each 0.1 ml) were inoculated to a fresh coculture medium (10 ml). The growth was followed by measuring the optical density at 660 nm with a spectrophotometer (Hitachi U-100) . Analytical methods. DNA base composition and pigments were determined in cells grown to the early stationary phase with lactate as the electron donor for sulfate reduction. DNA was extracted as described by Marmur (8) and hyrolyzed with nuclease P, using the DNA-GC Kit (Yamasa Shoyu Co., Ltd., Choshi, Japan). The mol% G+C was determined by HPLC (Shimadzu LC-6A) equipped with YMC-Pack ODS-AQ column (YMC Inc., Kyoto, Japan). Cytochrome c3 was determined in whole cells by measuring redox difference spectra (Na2S204-reduced minus air-oxidized) with a spectrophotometer (Hitachi 112 NAKAMOTO, UEKI, and UEKI VOL. 42 150-20). Desulfoviridin was partially purified and determined according to Seki et al. (12). Gases, alcohols and fatty acids were determined by gas chromatography as described previously (19). Gas samples were taken from the headspace of culture tubes through the stopper with a pressure lock syringe (Precision Sampling Co., Baton Rouge, U.S.A.) and injected into a gas chromatograph (Hitachi 163). Culture fluids sampled for the analysis of fatty acids and alcohols were deprotein- ized and injected to a gas chromatograph (Hitachi 263). Sulfate was measured with an ion chromatograph (Dionex 2000i). A mobile phase composed of 1.8 mM Na2C03 and 1.7 mM NaHC03 was used at a flow rate of 1 ml/min. RESULTS Properties of isolates of H2-utilizing sulfate-reducing bacteria Morphological and physiological properties of three isolates designated as strains HS-1, HS-2 and HS-3 are presented in Table 1. For comparison, properties of type strains of D. vulgaris (NCIMB 8303) and D. desulfuricans (NCIMB 8307) are also presented. Morphology: Three isolates were Gram-negative, non-spore-forming, curved rods motile with a single polar flagellum. The cells were usually single, and 0.5-0.6 um in diameter and 2.2-2.8 gymin length. DNA base compositions and pigments: The G + C contents (mol%) of the isolates were 59.6+0.7%. The redox difference spectra of isolates exhibited a pattern characteristic of cytochrome c3 with maxima at 420, 523 and 553 nm, and the partially purified preparation of desulfoviridin showed the characteristic ab- sorption band at about 630 nm.
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