The aim of this research was to investigate the competition between methanogens and sulfate-reducing bacteria in hypersaline environments. Samples of photosynthetic microbial mats, both soft mats (salinities of 55–126 ppt) and gypsum-hosted endoevaporite mats (salinities of 77–320 ppt), were obtained from hypersaline environments in California, USA, Mexico and Chile. Methane production was determined from the increase in headspace methane concentration within incubation vials containing mat samples. At the end of the incubation period, the δ13C values of produced methane were measured. Soft microbial mat vials containing molybdate, a specific inhibitor of bacterial sulfate reduction, exhibited dramatically higher methane production rates and higher (enriched in 13C) methane δ13C values than the controls. This suggests that the inhibition of sulfate reduction allowed the methanogens at these sites to use the competitive substrates (H2 and/or acetate) made available. Further, the higher δ13C values of the produced methane suggest that substrates (both competitive and non-competitive) were used to near completion. At the endoevaporite sites, which have much higher salinities than the soft mat sites, methane production was not significantly different and the methane δ13C values either remained the same or decreased (depleted in 13C) with added molybdate. We suggest that substrate availability increased enough to allow for somewhat greater isotopic fractionation resulting in the lower methane δ13C values that were observed, but not enough to significantly increase measured production rates. Where no changes in either methane production rates or δ13C values occurred, we hypothesize that salinity itself was inhibiting sulfate reduction and thus controlling microbe populations and rates of metabolism.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Banat IM, Lindström EB, Nedwell DB, Balba MT (1981) Evidence for coexistence of two distinct functional groups of sulfate-reducing bacteria in salt marsh sediment. Appl Environ Microbiol 42:985–992
Beaudoin CS (2015) Use of stable carbon isotopes to assess anaerobic and aerobic methane oxidation in hypersaline ponds. Masters thesis, University of Missouri
Bull AT, Asenjo JA (2013) Microbiology of hyper-arid environments: recent insights from the Atacama Desert, Chile. Antonie Van Leeuwenhoek 103:1173–1179
Canfield DE, Des Marais DJ (1993) Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim Cosmochim Acta 16:3971–3984
Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752
Des Marais DJ (1995) The biogeochemistry of hypersaline microbial mats. Adv Microb Ecol 14:251–274
Des Marais DJ (2003) Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere. Bio Bull 204:160–167
Des Marais DJ, Cohen Y, Nguyen H, Cheatham M, Cheatham T, Munoz E (1989) Carbon isotopic trends in the hypersaline ponds and microbial mats at Guerrero Negro, Baja California Sur, Mexico: implications for Precambrian stromatolites. In: Cohen Y, Rosenberg E (eds) Microbial mats: physiological ecology of benthic microbial communities. American Society for Microbiology, Washington DC, pp 191–203
García-Maldonado JQ, Bebout BM, Celis LB, López-Cortés A (2012) Phylogenetic diversity of methyl-coenzyme M reductase (mcrA) gene and methanogenesis from trimethylamine in hypersaline environments. Int Microbiol 15:33–41
García-Maldonado JQ, Bebout BM, Everroad RC, López-Cortés A (2015) Evidence of novel phylogenetic lineages of methanogenic Archaea from hypersaline microbial mats. Microb Ecol 69:106–117
García-Maldonado JQ, Escobar-Zepeda A, Raggi L, Bebout BM, Sanchez-Flores A, López-Cortés A (2018) Bacterial and archaeal profiling of hypersaline microbial mats and endoevaporites, under natural conditions and methanogenic microcosm experiments. Extremophiles 22:903–916
Kelley CA, Prufert-Bebout LE, Bebout BM (2006) Changes in carbon cycling ascertained by stable isotopic analyses in a hypersaline microbial mat. J Geophys Res. https://doi.org/10.1029/2006JG000212
Kelley CA, Poole JA, Tazaz AM, Chanton JP, Bebout BM (2012) Substrate limitation for methanogenesis in hypersaline environments. Astrobiol 12:89–97
Kelley CA, Nicholson BE, Beaudoin CS, Detweiler AM, Bebout BM (2014) Trimethylamine and organic matter additions reverse substrate limitation effects on the δ13C values of methane produced in hypersaline microbial mats. Appl Environ Microbiol 80:7316–7323
Kelley CA, Chanton JP, Bebout BM (2015) Rates and pathways of methanogenesis in hypersaline environments as determined by 13C-labeling. Biogeochemistry 126:329–341
King GM (1991) Measurement of acetate concentrations in marine pore waters by using an enzymatic approach. Appl Environ Microbiol 57:3476–3481
King GM, Klug MJ, Lovley DR (1983) Metabolism of acetate, methanol, and methylated amines in intertidal sediments of Lowes Cove, Maine. Appl Environ Microbiol 45:1848–1853
McEwen AS, Ojha L, Dundas CM, Mattson SS, Byrne S, Wray JJ, Cull SC, Murchie SL, Thomas N, Gulick VC (2011) Seasonal flows on warm Martian slopes. Science 333:740–743
Nicholson B (2013) Effect of increasing trimethylamine and organic matter concentration on stable carbon isotopes of methane produced in hypersaline, substrate limited environments. Masters thesis, University of Missouri
Ojha L, Wilhelm MB, Murchie SL, McEwen AS, Wray JJ, Hanley J, Massé M, Chojnacki M (2015) Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat Geosci 8:829–832
Oremland RS, Capone DG (1988) Use of “specific” inhibitors in biogeochemistry and microbial ecology. Adv Microb Ecol 10:285–383
Oremland RS, Polcin S (1982) Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44:1270–1276
Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923
Osterloo MM, Hamilton VE, Banfield JL, Glotch TD, Baldridge AM, Christensen PR, Tornabene LL, Anderson FS (2008) Chloride-bearing materials in the southern highlands of Mars. Science 319:1651–1654
Rice AL, Gotoh AA, Ajie HO, Tyler SC (2001) High precision continuous-flow measurements of δ13C and δD of atmospheric CH4. Anal Chem 73:4104–4110
Sørensen KB, Canfield DE, Oren A (2004) Salinity responses of benthic microbial communities in a solar saltern (Eilat, Israel). Appl Environ Microbiol 70:1608–1616
Summons RE, Franzmann PE, Nichols PD (1998) Carbon isotopic fractionation associated with methylotrophic methanogenesis. Org Geochem 28:465–475
Tazaz AM, Bebout BM, Kelley CA, Poole J, Chanton JP (2013) Redefining the isotopic boundaries of biogenic methane: methane from endoevaporites. Icarus 224:268–275
Webster CR, Mahaffy PR, Atreya SK, Moores JE, Flesch GJ, Malespin C, McKay CP, Martinez G, Smith CL, Martin-Torres J, Gomez-Elvira J, Zorzano M-P, Wong MH, Trainer MG, Steele A, Archer D Jr, Sutter B, Coll PJ, Freissinet C, Meslin P-Y, Gough RV, House CH, Pavlov A, Eigenbrode JL, Glavin DP, Pearson JC, Keymeulen D, Christensen LE, Schwenzer SP, Navarro-Gonzalez R, Pla-García J, Rafkin SCR, Vicente-Retortillo Á, Kahanpää H, Viudez-Moreiras D, Smith MD, Harri A-M, Genzer M, Hassler DM, Lemmon M, Crisp J, Sander SP, Zurek RW, Vasavada AR (2018) Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 360:1093–1096
Welsh DT, Lindsay YE, Caumette P, Herbert RA, Hannan J (1996) Identification of trehalose and glycine betaine as compatible solutes in the moderately halophilic sulfate reducing bacterium, Desulfovibrio halophilus. FEMS Microbiol Lett 140:203–207
Whiticar MJ (1999) Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 161:291–314
Yung YL, Chen P, Nealson K, Atreya S, Beckett P, Blank JG, Ehlmann B, Eiler J, Etiope G, Ferry JG, Forget F, Gao P, Hu R, Kleinböhl A, Klusman R, Lefevre F, Miller C, Mischna M, Mumma M, Newman S, Oehler D, Okumura M, Oremland R, Orphan V, Popa R, Russell M, Shen L, Sherwood Lollar B, Staehle R, Stamenković V, Stolper D, Templeton A, Vandaele AC, Viscardy S, Webster CR, Wennberg PO, Wong ML, Worden J (2018) Methane on Mars and habitability: challenges and responses. Astrobiol 18:1221–1242
Thanks to Tyler Mauney and to our many colleagues in Mexico and Chile for help in the field and laboratory. We are also appreciative of the access to the field sites provided by Exportadora de Sal, S.A. de C.V and the U.S. Fish and Wildlife Service. Funding by the NASA Exobiology program is gratefully acknowledged. We are honored to be part of this special issue dedicated to Mark Hines, one of the most loving and supportive people, both personally and scientifically, that anyone could know. You are missed, Mark.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Kelley, C.A., Bebout, B.M., Chanton, J.P. et al. The Effect of Bacterial Sulfate Reduction Inhibition on the Production and Stable Isotopic Composition of Methane in Hypersaline Environments. Aquat Geochem 25, 237–251 (2019). https://doi.org/10.1007/s10498-019-09362-x
- Methane production
- Stable isotopes