Abstract
Slurries of anoxic paddy soil were either freshly prepared or were partially depleted in endogenous electron donors by prolonged incubation under anaerobic conditions. Endogenous NO −3 was reduced within 4 h, followed by reduction of Fe3+ and SO 2−4 , and later by production of CH4. Addition of NO −3 slightly inhibited the production of Fe2+ in the depleted but not in the fresh paddy soil. Inhibition was overcome by the addition of H2, acetate, or a mixture of fatty acids (and other compounds), indicating that these compounds served as electron donors for the bacteria reducing NO −3 and/or ferric iron. Addition on NO −3 also inhibited the reduction of SO 2−4 in the depleted paddy soil. This inhibition was only overcome by H2, but not by acetate or a mixture of compounds, indicating that H2 was the predominant electron donor for the bacteria involved in NO −3 and/or SO 2−4 reduction. SO 2−4 reduction was also inhibited by exogenous Fe3+, but only in the depleted paddy soil. This inhibition was overcome by either H2, acetate, or a mixture of compounds, suggesting that they served as electron donors for reduction of Fe3+ and/or SO 2+4 . CH4 production was inhibited by NO −3 both in depleted and in fresh paddy soil. Fe3+ and SO 2−4 also inhibited methanogenesis, but the inhibition was stronger in the depleted than in the fresh paddy soil. Inhibition of CH4 production was paralleled by a decrease in the steady state concentration of H2 to a level which provided a free enthalpy of less than ΔG=−17 kJ mol-1 CH4 compared to more than ΔG=−32 kJ mol-1 CH4 in the control. The results indicate that in the presence of exogenous fe3+ or SO 2+4 , methanogenic bacteria were outcompeted for H2 by bacteria reducing Fe3+ or SO 2+4 .
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References
Bak F, Scheff G, Jansen KH (1991) A rapid and sensitive ion chromatographic technique for the determination of sulfate and sulfate reduction rates in freshwater lake sediments. FEMS Microbiol Ecol 85:23–30
Beauchamp EG, Trevors JT, Paul JW (1989) Carbon sources for bacterial denitrification. Adv Soil Sci 10:113–142
Chao TT: Zhou L (1983) Extraction techniques for selective dissolution of amorphous iron oxides from soils and sediments. Soil Sci Soc AM J 47:225–232
Conrad R, Schink B, Phelps TJ (1986) Thermodynamics of H2-producing and H2-consuming metabolic reactions in diverse methanogenic environments under in-situ conditions. FEMS Microbiol Ecol 38:353–360
Conrad R, Lupton FS, Zeikus JG (1987a) Hydrogen metabolism and sulfate-dependent inhibition of methanogenesis in a eutrophic lake sediment (Lake Mendota). FEMS Microbiol Ecol 45:107–115
Conrad R, Schütz H, Babbel M (1987b) Temperature limitation of hydrogen turnover and methanogenesis in anoxic paddy soil. FEMS Microbiol Ecol 45:281–289
Cord-Ruwisch R, Seitz JH, Conrad R (1988) The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor. Arch Microbiol 149:350–357
Dolfing J, Tiedje JM (1991) Kinetics of 2 complementary hydrogen sink reactions in a defined 3-chlorobenzoate degrading methanogenic co-culture. FEMS Microbiol Ecol 86:25–32
Fischer WR (1983) Theoretische Betrachtungen zur reduktiven Auflösung von Eisen(III)-oxiden. Z Pflanzenernaehr Bodenkd 146:611–622
Isa Z, Grusenmeyer S, Verstraete W (1986) Sulfate reduction relative to methane production in high-rate anaerobic digestion: microbiological aspects. Appl Environ Microbiol 51:580–587
King GM (1984) Utilization of hydrogen, acetate, and “noncompetitive” substrates by methanogenic bacteria in marine sediments. Geomicrobiol J 3:275–306
Komatsu Y, Takagi M, Yamaguchi M (1978) Participation of iron in denitrification in waterlogged soil. Soil Biol Biochem 10:21–26
Kristjansson JK, Schönheit P, Thauer RK (1982) Different Ks values for hydrogen of methanogenic bacteria and sulfate reducing bacteria: an explanation for the apparent inhibition of methanogenesis by sulfate. Arch Microbiol 131:278–282
Lovley DR (1985) Minimum threshold for hydrogen metabolism in methanogenic bacteria. Appl Environ Microbiol 49:1530–1531
Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287
Lovely DR, Phillips EJP (1987) Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction sediments. Appl Environ Microbiol 53:2636–2641
Lovley DR, Goodwin S (1988) Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments. Geochim Cosmochim Acta 52:2993–3003
Lovley DR, Dwyer DF, Klug MJ (1982) Kinetic analysis of competition betbeen sulfate reducers and methanogens for hydrogen in sediments. Appl Environ Microbiol 43:1373–1379
Lovley DR, Phillips EJP, Lonergan DJ (1989) Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl Environ Microbiol 55:700–706
Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S (1993) Geobacter metallireducens gen nov sp nov, a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344
Mayer HP, Conrad R (1990) Factors influencing the population of methanogenic bacteria and the initiation of methane production upon flooding of paddy soil. FEMS Microbiol Ecol 73:103–112
Mountfort DO, Asher RA, Mays EL, Tiedje JM (1980) Carbon and electron flow in mud and sandflat intertidal sediments at Delaware Inlet, Nelson, New Zealand. Appl Environ Microbiol 39:686–694
Munch JC, Pttow JCG (1977) Modelluntersuchungen zum Mechanismus der bakteriellen Eisenreduktion in hydromorphen Böden. Z Pflanzenernaehr Bodenkd 140:549–562
Munch JC, Ottow JCG (1980) Preferential reduction of amorphous to crystalline iron oxides by bacterial activity. Soil Sci 129:15–21
Munch JC, Ottow JCG (1982) Einfluß von Zellkontakt und Eisen(III)-Oxidform auf die bakterielle Eisenreduktion. Z Pflanzenernaehr Bodenkd 145:66–77
Ottow JCG (1970) Selection, characterization and iron-reducing capacity of nitrate reductaseless (nit-) mutants of iron-reducing bacteria. Z Allg Mikrobiol 10:55–62
Patrick WH Jr, Reddy CN (1978) Chemical changes in rice soils. In: International Rice Research Institute (ed) Soils and rice. IRRI, Los Baños, pp 361–379
Ponnamperuma FN (1972) The chemistry of submerged soils. Adv Agron 24:29–96
Qatibi AI, Bories A, Garcia HL (1990) Effects of sulfate on lactate and C2-volatile, C3-volatile fatty acid anaerobic degradation by a mixed microbial culture. Antonic van Leeuwenhoek J Microbiol Serol 58:241–248
Robinson JA, Tiedje JM (1984) Competition between sulfate-reducting and methanogenic bacteria for H2 under resting growing conditions. Arch Microbiol 137:26–32
Rothfuss F, Conrad R (1993) Vertical profiles of CH4 concentrations, dissolved substrates and processes involved in CH4 production in a flooded Italian rice field. Biogeochemistry 18:137–152
Schink B (1992) Syntrophism among prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, vol 1, 2nd edn. Springer, New York, pp 276–299
Schütz H, Holzapfel-Pschorn A, Conrad R, Rennenberg H, Seiler W (1989) A 3-year continuous record on the influence of daytime, season and fertilizer treatment on methane emission rates from an Italian rice paddy. J Geophys Res 94:16405–16416
Schwertmann U, Cornell RM (1991) Iron oxides in the laboratory. VCH, Weinheim
Seitz HJ, Schink B, Pfennig N, Conrad R (1990) Energetics of syntrophic ethanol oxidation in defined chemostat cocultures. 1. Energy requirement for H2 production and H2 oxidation. Arch Microbiol 155:82–88
Soerensen J (1982) Reduction of ferric iron in anaerobic, marine sediment and interaction with reduction of nitrate and sulfate. Appl Environ Microbiol 43:319–324
Stookey LL (1970) Ferrozin. A new spectrophotometric reagent for iron. Anal Chem 42:779–781
Thauer RK, Morris JG (1984) Metabolism of chemotrophic anaerobes: old views and new aspects. In: Kelly DP, Carr NG (eds) The microbe 1984. Part II: Prokaryotes and eukaryotes. Cambridge University Press, Cambridge, pp 123–168
Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180
Tugel JB, Hines ME, Jones GE (1986) Microbial iron reduction by enrichment cultures isolated from estuarine sediments. Appl Environ Microbiol 52:1167–1172
VanSchreven DA (1968) Mineralization of the carbon and nitrogen of plant material added to soil and of the soil humus during drying incubation following periodic drying and rewetting of the soil. Plant Soil 28:226–245
Ward DM, Winfrey MR (1985) Interactions between methanogenic and sulfate-reducing bacteria in sediments. Adv Aquat Microbiol 3:141–179
Westermann P, Ahring BK (1987) Dynamics of methane production, sulfate reduction, and denitrification in a permanently waterlogged alder swamp. Appl Environ Microbiol 53:2554–2559
Winfrey MR, Zeikus JG (1977) Effect of sulfate on carbon and electron flow during microbial methanogenesis in freshwater sediments. Appl Environ Microbiol 33:275–281
Zehnder AJB, Stumm W (1988) Geochemistry and biogeochemistry of anaerobic habitats. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 1–38
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Achtnich, C., Bak, F. & Conrad, R. Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19, 65–72 (1995). https://doi.org/10.1007/BF00336349
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DOI: https://doi.org/10.1007/BF00336349