Life in the Absence of Oxygen: Alternative Electron Acceptors for Anaerobic Microorganisms in a Petroleum Environment

Anaerobic microorganisms derive energy by transferring electrons from an external source or donor to an external electron sink or terminal acceptor and often have the capacity to reduce 2 or more terminal electron acceptors. The well-known type of microbial respiration, in which oxygen serves as an electron acceptor for the oxidation of organic carbon and/or hydrogen, has been studied elsewhere in detail. Anaerobic microorganisms are widely distributed in oil-producing vents, hydrothermal vents, volcanic hot springs, non-volcanic geothermally heated subsurface aquifers, and soil. In this study, anaerobic, thermophilic, and fermenting microorganisms in a petroleum sample from the Adıyaman region of Turkey were examined for their ability to use different electron acceptors. The temperature range for growth of the enrichment culture (TP1) was between 40 and 65 °C and the optimum pH ranged from 4.5 to 8.0. TP1 had the ability to use a wide variety of mono-, di-, and polysaccharides to form acetate, lactate, ethanol, H2, and CO2. No sulfate-reducing or methanogenic microorganisms were found. As an electron acceptor, TP1 reduces thiosulfate, elemental sulfur, sulfite, Fe(III), anthraquinone-2,6-disulfonate (AQDS), arsenake, and MnO2, but not sulfate, nitrate, (per)chlorate, or selenate. Herein, we show that the enrichment culture from the petroleum environment was able to reduce multiple electron acceptors. The utilization of these electron acceptors by TP1 also indicated their presence in this area. The results presented suggest that TP1 may occupy a niche as an environmental opportunist by taking advantage of diverse electron acceptors.

Life in the Absence of Oxygen: Alternative Electron Acceptors for Anaerobic Microorganisms in a Petroleum Environment

Anaerobic microorganisms derive energy by transferring electrons from an external source or donor to an external electron sink or terminal acceptor and often have the capacity to reduce 2 or more terminal electron acceptors. The well-known type of microbial respiration, in which oxygen serves as an electron acceptor for the oxidation of organic carbon and/or hydrogen, has been studied elsewhere in detail. Anaerobic microorganisms are widely distributed in oil-producing vents, hydrothermal vents, volcanic hot springs, non-volcanic geothermally heated subsurface aquifers, and soil. In this study, anaerobic, thermophilic, and fermenting microorganisms in a petroleum sample from the Adıyaman region of Turkey were examined for their ability to use different electron acceptors. The temperature range for growth of the enrichment culture (TP1) was between 40 and 65 °C and the optimum pH ranged from 4.5 to 8.0. TP1 had the ability to use a wide variety of mono-, di-, and polysaccharides to form acetate, lactate, ethanol, H2, and CO2. No sulfate-reducing or methanogenic microorganisms were found. As an electron acceptor, TP1 reduces thiosulfate, elemental sulfur, sulfite, Fe(III), anthraquinone-2,6-disulfonate (AQDS), arsenake, and MnO2, but not sulfate, nitrate, (per)chlorate, or selenate. Herein, we show that the enrichment culture from the petroleum environment was able to reduce multiple electron acceptors. The utilization of these electron acceptors by TP1 also indicated their presence in this area. The results presented suggest that TP1 may occupy a niche as an environmental opportunist by taking advantage of diverse electron acceptors.

___

  • Magot M. Similar bacteria in remote oil fields. Nature 379: 681, 1996.
  • Ravot G, Ollivier B, Magot M et al. Thiosulfate reduction, an important physiological feature shared by members of the order Thermotogales. Appl Environ Microbiol 61: 2053-2055, 1995.
  • Jeanthon C, Reysenbach AL, L’Haridon S et al. Thermotoga subterranea sp. nov., a new thermophilic bacterium isolated from a continental oil reservoir. Arch Microbiol 164: 91-97, 1995.
  • Fardeau ML, Ollivier B, Patel BKC et al. Thermotoga hypogea sp. nov., a xylanolytic, thermophilic bacterium from an oil-producing well. Int J Syst Evol Microbiol 47: 1013-1019, 1997.
  • Orphan VJ, Taylor LT, Hafenbradl D et al. Culture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66: 700-711, 2000.
  • Stetter KO, Hoffmann A, Huber R. Microorganisms Adapted to High Temperature Environments. In: Guerrrero R, Pedros-Alio C. eds. Trends in Microbiology Ecology. Spanish Society for Microbiology, 1993: pp. 25-28.
  • Pedersen K. Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiol Lett 185: 9-16, 2000.
  • Kasting JF, Siefert JL. Life and the Evolution of Earth’s Atmosphere. Science 296: 1066, 2002.
  • Reysenbach AL, Shock E. Merging Genomes with Geochemistry in Hydrothermal Ecosyst Sci 296: 1077, 2002.
  • Balk M, Weijma J, Friedrich MW et al. Methanol conversion by novel thermophilic homoacetogenic bacterium Moorella mulderi sp. nov. isolated from a bioreactor. Arch Microbiol 179: 315- 320, 2003. Henstra AM, Stams AJ. Novel physiological features of Carboxydothermus hydrogenoformans and Thermoterrabacterium ferrireducens. Appl Environ Microbiol 70: 7236-40, 2004.
  • Scholten JC, Stams AJM. The effect of sulfate and nitrate on methane formation in a freshwater sediment. Antonie van Leeuwenhoek 68: 309-315, 1995.
  • Trüper HG, Schlegel HG. Sulphur metabolism in Thiorhodaceae. I. Quantitative measurements on growing cells of Chromatium okenii. Antonie Van Leeuwenhoek 30: 225-238, 1964.
  • Amend JP, Shock EL. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev 25: 175-243, 2001.
  • Morikawa M, Kanemoto T, Imanaka T. Biological oxidation of alkane to alkene under anaerobic conditions. J Ferm Bioeng 82: 309-311, 1996.
  • Stetter KO, Huber R. The role of hyperthermophilic prokaryotes in oil fields, in: Bell M, Brylinsky M, Johnson-Green P. eds. Microbial Biosystems: New Frontiers, Proceedings of the 8th International Symposium on Microbial Ecology, Halifax, Canada; 2000: pp 369-375.
  • Barth T, Riis M. Interactions between organic acid anions in formation waters and reservoir mineral phases. Org Geochem 19: 455-482, 1992.
  • Roling WF, Head IM, Larter SR. The microbiology of hydrocarbon degradation in subsurface petroleum reservoirs: perspectives and prospects. Res Microbiol 154: 321-8, 2003.
  • Odom JM, Singleton R. The Sulfate-Reducing Bacteria: Contemporary Perspectives. New York: Springer Verlag, 1993.
  • Lovley DR, Chapelle FH. Deep subsurface processes. Rev Geophys 33: 365-381, 1995.
  • Lovley DR, Coates JD. Novel forms of anaerobic respiration of environmental relevance. Curr Opin Microbiol 3: 252-6, 2000.
  • Lovley DR, Phillips EJ. Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl Environ Microbiol 53: 2636- 2641, 1987.
  • Lovley DR, Coates JD. Bioremediation of metal contamination. Curr Opin Biotechnol 8: 285-9, 1997.
  • Canfield DE. The geochemistry of river particulates from the continental USA: major elements. Geochim Cosmochim Acta 61: 3349-65, 1997.
  • Cornell RM, Schwertmann U. The Iron Oxides–Structure, Properties, Reactions, Occurrence and Uses. VCH, Weinheim, 1996. Thamdrup B, Rossello-Mora R, Amann R. Microbial manganese and sulfate reduction in Black Sea shelf sediments. Appl Environ Microbiol 66: 2888-97, 2000. Nazina TN, Ivanova AE, Golubeva OV. Occurrence of sulfate. a n d iron-reducing bacteria in stratal waters of the Romashkinskoe oil filed. Microbiology (English Translation of Mikrobiologiya) 64: 203-208, 1995.
  • Hernandez ME, Newman DK. Extracellular electron transfer. Cell Mol Life Sci 58: 1562-71, 2001. Stolz JF, Oremland RS. Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23: 615-27, 1999.
  • Newman DK, Kennedy EK, Coates JD. Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol 168: 380-8, 1997.
  • Ohlendorf HM, Hoffman DJ, Saiki MK et al. Embryonic mortality and abnormalities of aquatic birds: apparent impacts of selenium from irrigation drainwater. Sci Tot Env 52: 49-63, 1986.
  • Pacyna JM. Atmospheric emissions of arsenic, cadmium, lead and mercury from high temperature processes in power generation and industry. In: Hutchinson TC, Meema KM. eds. Lead, mercury, cadmium and arsenic in the environment. Wiley, New York; 1987: pp 69-87.
  • Bowen HJM. Environmental chemistry of the elements. Academic Press, New York, 1979. Widdel F, Rabus R. Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12: 259-276, 2001.
  • Zengler K, Richnow HH, Rosello-Mora R et al. Methane formation from lon-chain alkanes by anaerobic microorganisms. Nature 401: 266-269, 1999.
  • Newman DK, Banfield JF. Geomicrobiology: How molecular-scale interactions underpin biogeochemical systems. Science 296: 1071-7, 2002.
Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK