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High rates of anaerobic oxidation of methane, ethane and propane coupled to thiosulphate reduction

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Abstract

Anaerobic methane oxidation coupled to sulphate reduction and the use of ethane and propane as electron donors by sulphate-reducing bacteria represent new opportunities for the treatment of streams contaminated with sulphur oxyanions. However, growth of microbial sulphate-reducing populations with methane, propane or butane is extremely slow, which hampers research and development of bioprocesses based on these conversions. Thermodynamic calculations indicate that the growth rate with possible alternative terminal electron acceptors such as thiosulphate and elemental sulphur may be higher, which would facilitate future research. Here, we investigate the use of these electron acceptors for oxidation of methane, ethane and propane, with marine sediment as inoculum. Mixed marine sediments originating from Aarhus Bay (Denmark) and Eckernförde Bay (Germany) were cultivated anaerobically at a pH between 7.2 and 7.8 and a temperature of 15 °C in the presence of methane, ethane and propane and various sulphur electron acceptors. The sulphide production rates in the conditions with methane, ethane and propane with sulphate were respectively 2.3, 2.2 and 1.8 μmol S L−1 day−1. For sulphur, no reduction was demonstrated. For thiosulphate, the sulphide production rates were up to 50 times higher compared to those of sulphate, with 86.2, 90.7 and 108.1 μmol S L−1 day−1 for methane, ethane and propane respectively. This sulphide production was partly due to disproportionation, 50 % for ethane but only 7 and 14 % for methane and propane respectively. The oxidation of the alkanes in the presence of thiosulphate was confirmed by carbon dioxide production. This is, to our knowledge, the first report of thiosulphate use as electron acceptor with ethane and propane as electron donors. Additionally, these results indicate that thiosulphate is a promising electron acceptor to increase start-up rates for sulphate-reducing bioprocesses coupled to short-chain alkane oxidation.

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References

  • Alperin MJ, Reeburgh WS, Whiticar MJ (1988) Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation. Glob Biogeochem Cycles 2:279–288

    Article  CAS  Google Scholar 

  • Barnes RO, Goldberg ED (1976) Methane production and consumption in anoxic marine sediments. Geology 4:297–300

    Article  CAS  Google Scholar 

  • Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626

    Article  CAS  Google Scholar 

  • Dale AW, Aguilera DR, Regnier P, Fossing H, Knab NJ, Jørgensen BB (2008) Seasonal dynamics of the depth and rate of anaerobic oxidation of methane in Aarhus Bay (Denmark) sediment. J Mar Res 66(1):127–155

    Article  CAS  Google Scholar 

  • Deusner C, Meyer V, Ferdelman TG (2010) High-pressure systems for gas-phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane. Biotechnol Bioeng 105(3):524–533

    Article  CAS  Google Scholar 

  • Finster K, Liesack W, Thamdrup B (1998) Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol 64(1):119–125

    CAS  Google Scholar 

  • Girguis PR, Cozen AE, DeLong EF (2005) Growth and population dynamics of anaerobic methane-oxidizing archaea and sulphate-reducing bacteria in a continuous flow bioreactor. Appl Environ Microbiol 71:3725–3733

    Article  CAS  Google Scholar 

  • Habicht KS, Canfield DE, Rethmeier J (1998) Sulfur isotope fractionation during bacterial reduction and disproportionation of thiosulfate and sulfite. Geochim Cosmochim Acta 62:2585–2595

    Article  CAS  Google Scholar 

  • Hinrichs KU, Summons RE, Orphan V, Sylva SP, Hayesa JM (2000) Molecular and isotopic analysis of anaerobic methane-oxidizing communities in marine sediments. Org Geochem 31(12):1685–1701

    Article  CAS  Google Scholar 

  • Holmkvist L, Ferdelman TG, Jørgensen BB (2011) A cryptic sulfur cycle driven by iron in the methane zone of marine sediment (Aarhus Bay, Denmark). Geochim Cosmochim Acta 75(12):3581–3599

    Article  CAS  Google Scholar 

  • Jaekel U, Musat N, Adam B, Kuypers M, Grundmann O, Musat F (2013) Anaerobic degradation of propane and butane by sulfate-reducing bacteria enriched from marine hydrocarbon cold seeps. ISME J 7(5):885–895

    Article  CAS  Google Scholar 

  • Jørgensen BB (1990) A thiosulfate shunt in the sulfur cycle of marine sediments. Science 249(4965):152–154

    Article  Google Scholar 

  • Jørgensen BB, Bak F (1991) Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). Appl Environ Microbiol 57(3):847–856

    Google Scholar 

  • Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449(7164):898–901

    Article  CAS  Google Scholar 

  • Krüger M, Treude T, Wolters H, Nauhaus K, Boetius A (2005) Microbial methane turnover in different marine habitats. Palaeogeogr Palaeoclimatol Palaeoecol 227:6–17

    Article  Google Scholar 

  • Krüger M, Wolters H, Gehre M, Joye SB, Richnow H-H (2008) Tracing the slow growth of anaerobic methane-oxidizing communities by (15)N-labelling techniques. FEMS Microbiol Ecol 63(3):401–411

    Article  Google Scholar 

  • Lindeboom REF, Ferrer I, Weijma J, van Lier JB (2013) Effect of substrate and cation requirement on anaerobic volatile fatty acid conversion rates at elevated biogas pressure. Bioresour Technol 150:60–66

    Article  CAS  Google Scholar 

  • Meulepas RJW, Jagersma CG, Gieteling J, Buisman CJN, Stams AJM, Lens PNL (2009a) Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors. Biotechnol Bioeng 104(3):458–470

    Article  CAS  Google Scholar 

  • Meulepas RJW, Jagersma CG, Khadem AF, Buisman CJN, Stams AJM, Lens PNL (2009b) Effect on environmental conditions on sulfate reduction with methane as electron donor by an Eckernförde bay enrichment. Environ Sci Technol 43(17):6553–6559

    Article  CAS  Google Scholar 

  • Nauhaus K, Albrecht M, Elvert M, Boetius A, Widdel F (2007) In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ Microbiol 9(1):187–196

    Article  CAS  Google Scholar 

  • Reeburgh WS (1976) Methane consumption in Cariaco Trench waters and sediments. Earth Planet Sci Lett 28(3):337–344

    Article  CAS  Google Scholar 

  • Reeburgh W (1980) Anaerobic methane oxidation: rate depth distributions in Skan bay sediments. Earth Planet Sci Lett 47:345–352

    Article  CAS  Google Scholar 

  • Savage KN, Krumholz LR, Gieg LM, Parisi VA, Suflita JM, Allen JC, Philp RP, Elshahed MS (2010) Biodegradation of low-molecular-weight alkanes under mesophilic, sulfate-reducing conditions: metabolic intermediates and community patterns. FEMS Microbiol Ecol 72(3):485–495

    Article  CAS  Google Scholar 

  • Steinbusch KJJ, Hamelers HVM, Buisman CJN (2008) Alcohol production through volatile fatty acids reduction with hydrogen as electron donor by mixed cultures. Water Res 42(15):4059–4066

    Article  CAS  Google Scholar 

  • Treude T, Orphan V, Knittel K, Gieseke A, House CH, Boetius A (2007) Consumption of methane and CO2 by methanotrophic microbial mats from gas seeps of the anoxic black sea. Appl Environ Microbiol 73(7):2271–2283

    Article  CAS  Google Scholar 

  • Valentine DL, Reeburgh WS (2000) New perspectives on anaerobic methane oxidation. Environ Microbiol 2(5):477–484

    Article  CAS  Google Scholar 

  • Weijma J, Veeken A, Dijkman H, Huisman J, Lens P (2006) Heavy metal removal with biogenic sulphide: advancing to full-scale. In: Cervantes F, Pavlostathis S, van Haandel A (eds) Advanced biological treatment processes for industrial wastewaters: principles and applications. IWA, London, pp 321–331

    Google Scholar 

  • Widdel F, Musat F, Knittel K, Galushko A (2007) Anaerobic degradation of hydrocarbons with sulphate as electron acceptor. Sulphate-reducing bacteria. Cambridge University Press, Cambridge, UK, pp 265–303

    Google Scholar 

  • Zhang Y, Henriet J-P, Bursens J, Boon N (2010) Stimulation of in vitro anaerobic oxidation of methane rate in a continuous high-pressure bioreactor. Bioresour Technol 101(9):3132–3138

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research is supported by the Dutch Technology Foundation STW, which is part of the Netherlands Organisation for Scientific Research (NWO), and which is partly funded by the Ministry of Economic Affairs. It was also financially supported by the WIMEK/SENSE research school. Additionally, we would like to thank Gusti Diansyah and Brian van Ringelestijn for their collaboration on the measurements. Anna Lichtschlag and Tina Treude from the MPI-Bremen are acknowledged for providing access to the Eckernförde Bay sediment. We thank the crew of the LITTORINA from the Leibniz-Institut für Meereswissenschaften for the sediment sampling. We thank Hans Røy, Kasper Kjeldsen, Mark Lever and the captain and crew of the RV Tyra for the successful sampling on May 23rd 2011. The authors are grateful to the staff at The Center for Geomicrobiology from Aarhus University for their hospitality and help with analysis.

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Correspondence to Jan Weijma.

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Suarez-Zuluaga, D.A., Weijma, J., Timmers, P.H.A. et al. High rates of anaerobic oxidation of methane, ethane and propane coupled to thiosulphate reduction. Environ Sci Pollut Res 22, 3697–3704 (2015). https://doi.org/10.1007/s11356-014-3606-0

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