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    Carbon and hydrogen isotope fractionation during methanogenesis: A laboratory study using coal and formation water Rita Susilawati, Suzanne D. Golding, Kim A. Baublys, Joan S. Esterle, Stephanie K. Hamilton PII: DOI: Reference:

S0166-5162(16)30189-6 doi: 10.1016/j.coal.2016.05.003 COGEL 2635

To appear in:

International Journal of Coal Geology

Received date: Revised date: Accepted date:

16 October 2015 9 May 2016 10 May 2016

Please cite this article as: Susilawati, Rita, Golding, Suzanne D., Baublys, Kim A., Esterle, Joan S., Hamilton, Stephanie K., Carbon and hydrogen isotope fractionation during methanogenesis: A laboratory study using coal and formation water, International Journal of Coal Geology (2016), doi: 10.1016/j.coal.2016.05.003

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ACCEPTED MANUSCRIPT CARBON AND HYDROGEN ISOTOPE FRACTIONATION DURING METHANOGENESIS: A LABORATORY STUDY USING COAL AND FORMATION WATER

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Rita Susilawatia,b*, Suzanne D. Goldinga, Kim A. Baublysa, Joan S. Esterlea and Stephanie K.

School of Earth Sciences, The University of Queensland, St Lucia, Queensland 4072 Australia; b Geological Agency of Indonesia, Jl. Sukarno Hatta no 444, Bandung, West Java 40254, Indonesia.

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Hamiltona

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ABSTRACT

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Carbon and hydrogen isotope compositions of CH4 generated via methanogenesis in cultures of South Sumatra Basin (SSB) coalbed methane (CBM) formation waters grown on coal, acetate and H2+CO2 were investigated. CH4 production and molecular analysis confirmed the presence of active microbial communities that are able to convert coal into CH4 using both acetoclastic and hydrogenotrophic pathways. The representative bacterial sequences were dominated by Bacteroidetes, Firmicutes and Deltaproteobacteria, while Methanosaeta and Methanosarcina were the most prevalent archaeal methanogens present in the cultures. CH4 produced in this study’s culturing experiments has δ13C values in the range of –50 ‰ to –20 ‰, with most values falling outside the current understanding of the carbon isotopic boundaries for biogenic CH4 (–110 ‰ to –30 ‰). However, the corresponding apparent carbon isotopic α factor (αc = 1.02±0.006), and isotopic effect (εc = –20.1 ‰ ±15.3) showed that CH4 in SSB cultures was predominantly produced by acetoclastic methanogenesis, which is consistent with the results of molecular DNA analysis. In addition, the calculated contribution of CO2 reduction from the δ13C values of coaltreated cultures was overall < 50 %, further confirming the high contribution of the acetoclastic pathway to CH4 production in the SSB cultures. The outcome of this experimental study also suggests that δ2HCH4 values may not provide a reliable basis for distinguishing methanogenic pathways, while apparent carbon isotopic fractionation factor (αc) and isotope effect (εc) are considered more useful indicators of the methanogenic pathway. The high δ13C-CH4 values (>–30 ‰) and the dominance of Methanosaeta over Methanosarcina indicate that methanogens within the SSB cultures were operating at low substrate concentrations. An unusually positive δ13C-CH4 suggests a substrate depletion effect, which is thought to be related to a decrease in the relative abundance of key bacterial coal degraders with formation water inoculum storage time. Closer observation of δ13C-CH4 values during the growth of cultures within a single experiment also showed a 13C-enrichment trend over time. At log phase of growth, the CH4 produced was 13C-depleted when compared to the stationary phase that also indicates substrate depletion effects. Finally, the δ13CCH4 values encountered in this study (as high as –20 ‰) highlight the possible positive extension of δ13CCH4 values of acetoclastic methanogenesis from those currently reported in the literature for natural and experimental samples (as high as –30 ‰). Keywords: Biogenic gas, coal, culture experiment, isotopic composition

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INTRODUCTION Archaeal methanogens are the only known microorganisms capable of forming CH4. These

strictly anaerobic microbes are restricted to utilizing simple compounds that contain no more

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than two carbon atoms. As such, complex organic compounds in anoxic environments (e.g., marine sediments, rice paddies, subsurface shales and coalbeds) are degraded by associations of

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microbes consisting of hydrolytic, fermentative and acetogenic bacteria and methanogenic

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archaea (Schink, 2006; Strąpoć et al., 2011; Winter and Knoll, 1989; Zinder, 1993). This association is often termed a methanogenic consortium. Methanogenesis is the final step in the

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decomposition of organic matter by methanogenic consortia. Because of their vital ecological role in the Earth’s carbon cycling, methanogens have gained attention in the literature,

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particularly in the environmental and bioenergy areas (Conrad et al., 2011; Demirel and Scherer, 2008; Milkov, 2011; Miller, 2004; Wawrik et al., 2012). Methanogen substrates, in general, can be grouped into competitive and non-competitive

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substrates. The first category relates to substrates that are also utilized by other groups of

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microbes. These substrates include acetate, formate and H2+CO2. Depending on the environment, bacteria can successfully out-compete methanogens for competitive substrates

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(e.g., sulfur reducing bacteria in a sulfate-rich zone) (Whiticar, 1999). Non-competitive substrates are substrates that are available for methanogens but less attractive to other microbes (Whiticar, 1999). Included in this group are methanol and methylated amines. When utilizing substrates to produce CH4, methanogens mainly use two primary pathways, acetate fermentation (Equation (1)) and CO2 reduction (Equation (2)) (Strąpoć et al., 2011; Whiticar, 1999; Zinder, 1993). Studies have documented that CO2 reduction is the dominant pathway in the marine environment, while acetate fermentation is the major pathway in freshwater environments (Schoell, 1980; Whiticar et al., 1986). However, in coalbed environments, it has been recognized that the CO2 reduction pathway predominates, even when the waters are quite fresh (Golding et al., 2013). CH3COOH → CO2 + CH4

(1)

CO2 + 4H2 → 2H2O + CH4

(2)

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ACCEPTED MANUSCRIPT Stable isotopes are a valuable tool for the identification of CH4 gas origin and generation pathways (Flores et al., 2008; Hamilton et al., 2014; Kinnon et al., 2010; Strąpoć et al., 2007). The method has been used to evaluate CH4 dynamics both in ecosystems and laboratory

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engineered systems. Organic matter degradation by microbial activity in an anoxic environment produces CH4 depleted in 13C relative to CH4 produced thermogenically (Faiz and Hendry, 2006;

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Golding et al., 2013; Whiticar, 1999). This is because microbes preferentially utilize the lighter

generally

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isotope of C (12C) that has lower bond energies, and therefore biogenically derived CH4 is C-depleted. Isotope fractionation is maximized under conditions where the

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methanogenic substrate is in abundant supply, and depends on several factors including temperature, microbial growth phase, the hydrogen supply, the methanogen species, and the

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methanogenic pathways involved (Botz et al., 1996; Conrad, 2005; Penning et al., 2005). Moreover, isotopic fractionation of biogenic CH4 may increase throughout the culture’s exponential growth phase before stabilizing during the stationary phase (Valentine et al., 2004).

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The current understanding of the isotopic composition of biogenic CH4 is in the range of –

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110 ‰ to ‒50 ‰ and ‒400 ‰ to ‒150 ‰, for δ13C-CH4 and δ2H-CH4, respectively (Conrad, 2005; Golding et al., 2013; Whiticar, 1999; Whiticar et al., 1986). In addition, CH4 produced 13

C-depleted relative to that produced from acetate (Chanton et al.,

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from H2+CO2 is typically

2004; Conrad et al., 2011; Whiticar, 1999). Hydrogenotrophic methanogenesis derived CH4 typically has δ13C-CH4 between –110 ‰ and ‒60 ‰, while acetoclastic methanogenesis produced CH4 has δ13C between ‒60 ‰ and ‒45 ‰ (Conrad et al., 2011; Whiticar, 1999). Small isotopic fractionation factor α values ( 0 ‰ (Table 9). Similarly, for the H2+CO2-

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treated culture, the use of αmc = 1.072 also gave unreasonably low ƒmc values, while calculation using αmc = 1.041 gave ƒmc values ranging from 0.99 to 1, suggesting a high contribution from the CO2 reduction pathway to CH4 generation in this culture as expected. The somewhat different fractionation factors for hydrogenotrophic methanogenesis in the coal-treated cultures and the H2+CO2-treated culture were likely caused by differences in H2 concentration. As previously mentioned in the methods section, a high concentration of H2 (80 %) was injected into the H2+CO2-treated culture. A previous study showed that under high H2 concentration (unlimited substrate), the hydrogenotrophic methanogens fractionated carbon isotopes less than when H2 concentration was low (Valentine et al., 2004). That may explain why the H2+CO2treated culture had a lower αc value (1.041) compared to the coal-treated culture (1.072). In addition, studies have noted that such differences in fractionation factors for the same pathway may be related to differences in microbial community structures and culture conditions. In the case of our SSB cultures, when different carbon sources were present, their carbon isotopic compositions and differing bioavailability also possibly influenced the isotopic fractionation factor of the samples.

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Table 9. Estimation of CO2 reduction contribution (ƒ mc) for CH4 from SSB H2+CO2 and acetate treated cultures Major source of carbon

ɛma = 10

ɛma = 6.1

ɛma = 0

ɛma = 10

ɛma = 6.1

ɛma = 0

SSB4

H2+CO2

-0.42

-0.18

-1.80

0.99

0.99

1.00

SSB3

Acetate

0.00

-0.15

0.17

-0.01

0.15

0.31

SSB4

Acetate

-0.01

-0.14

0.15

-0.02

0.13

0.28

SSB5

Acetate

-0.01

-0.14

0.16

-0.01

0.14

0.29

1.041

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1.072

CONCLUSIONS

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ƒmc calculated using Eqns 7,8 and 9, with 2 variables of αmc (1.072 and 1.041) and 2 variables of ɛma. Isotopic values are expressed in per mil (‰) notation. Highlighted areas show the most likely contribution of the CO2 reduction pathway. For detailed explanation see text.

Three different experiments were conducted that aimed to determine the isotopic

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composition of microbial CH4 and CO2 produced from cultures of SSB formation waters grown on coal, H2+CO2 and acetate. Overall, the results showed the following: (1) The δ13C-CH4 values in our experiment (–50 ‰ to –20 ‰) mostly fell outside the field currently considered as representative of biogenic CH4. This study hypothesizes two possible causes for the positive δ13C-CH4 values found in SSB cultures; the increasing importance of acetate as a methanogenic substrate and a substrate depletion effect. Substrate depletion possibly occurred due to a decrease in the relative abundance of bacterial coal degraders with formation water inoculum storage time. (2) In these experiments, an apparent carbon isotopic fractionation factor (αc) and isotope effect (εc) were found to be more useful indicators of methanogenic pathways than the absolute δ13C-CH4 values. Overall, the apparent α and ε values calculated in this study suggest the dominance of acetoclastic methanogenesis over hydrogenotrophic methanogenesis, which is consistent with pathway contribution calculation and microbial community data. The values are

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ACCEPTED MANUSCRIPT also in agreement with carbon isotopic fractionation values for acetoclastic methanogenesis reported in the literature. (3) Three cases are thought to have affected the carbon isotopic systematics of SSB coal-

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treated cultures: a) acetate fermentation in cultures that experienced a substrate limitation that

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was not severe enough to exclude isotope fractionation; b) acetate fermentation in cultures that experienced substrate depletion strong enough to exclude isotope fractionation; and c) acetate

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fermentation in cultures that have very severe substrate depletion, which may result in a slightly positive value of ɛma.

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(4) These experimental outcomes support the concept that CO2 reduction can result in CH4 with more negative δ2H values comparable to that found in acetate. Overall, the measurement of

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δ2H suggests that δ2H-CH4 is independent of the methanogenic pathway and may not provide a reliable basis for distinguishing the methanogenic pathway in SSB cultures. In addition, relatively positive δ13C-CH4 values encountered in this study suggest a positive extension of

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δ13C-CH4 values of acetoclastic methanogenesis from those currently reported in the literature. Altogether this study produced results that contribute to knowledge of the isotopic

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composition of CH4 produced from methanogenesis in cultures utilizing coal. The results are also potentially applicable to natural systems and may assist in interpreting the isotopic compositions of field gases.

ACKNOWLEDGEMENTS

Funding for this research came from an Australian Awards Scholarship 2010. PT Medco CBM Sekayu, Lemigas and PT Bukit Asam are gratefully acknowledged for access to sites and samples. TSOP Spackman award was used to partly fund laboratory consumables. The Australian Centre for Ecogenomics at The University of Queensland provided access to its PC2 and quarantine laboratory. The authors thank Sam Papendick, Soleh Basuki Rahmat, Eko Budi Tjahyono and Erlina Lena Ria for field assistance during sampling, as well as Steven Robbins and Paul Evans from the Australian Centre for Ecogenomics for assistance in molecular phylogenetic analysis. The authors also thank Tennille Mares, Maria Mastalerz and Anna Martini as well as three other anonymous reviewers for their constructive review of this manuscript. 33

ACCEPTED MANUSCRIPT REFERENCES Alperin, M.J., Hoehler, T.M., 2009. Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 2. Isotopic constraints. American Journal of Science 309, 958-984.

RI

PT

Amijaya, H., Littke, R., 2006. Properties of thermally metamorphosed coal from Tanjung Enim Area, South Sumatra Basin, Indonesia with special reference to the coalification path of macerals. International Journal of Coal Geology 66, 271-295.

SC

Bainotti, A.E., Futagami, K., Nakashimada, Y., Chang, Y.J., Nagai, S., Nishio, N., 1997. pH Auxostat continuous culture of Acetobacterium sp. coupled with removal of acetate by Methanosaeta concilii. Biotechnology Letters 19, 989-993.

NU

Balabane, M., Galimov, E., Hermann, M., Létolle, R., 1987. Hydrogen and carbon isotope fractionation during experimental production of bacterial methane. Organic Geochemistry 11, 115-119.

MA

Barnhart, E.P., De León, K.B., Ramsay, B.D., Cunningham, A.B., Fields, M.W., 2013. Investigation of coal-associated bacterial and archaeal populations from a diffusive microbial sampler (DMS). International Journal of Coal Geology 115, 64-70.

TE

D

Baublys, K.A., Hamilton, S.K., Golding, S.D., Vink, S., Esterle, J., 2015. Microbial controls on the origin and evolution of coal seam gases and production waters of the Walloon Subgroup; Surat Basin, Australia. International Journal of Coal Geology 147-148, 85-104.

AC CE P

Beckmann, S., Lueders, T., Kruger, M., Netzer, F.v., Engelen, B., Cypionka, H., 2011. Acetogens and acetoclastic Methanosarcinales govern methane formation in abandoned coal mines. Applied and Environmental Microbiology 77, 3749-3756. Botz, R., Pokojski, H.-D., Schmitt, M., Thomm, M., 1996. Carbon isotope fractionation during bacterial methanogenesis by CO2 reduction. Organic Geochemistry 25, 255-262. Bragg, L., Stone, G., Imelfort, M., Hugenholtz, P., Tyson, G.W., 2012. Fast, accurate errorcorrection of amplicon pyrosequences using Acacia. Nature Methods 9, 425-426. Burke, R.A., 1993. Proceedings of the NATO advanced research workshop. Possible influence of hydrogen concentration on microbial methane stable hydrogen isotopic composition. Chemosphere 26, 55-67. Chanton, J., Chaser, L., Glasser, P., Siegel, D., 2004. Carbon and hydrogen isotopic effects in microbial methane from terrestrial environments. Stable Isotopes and Biosphere-Atmosphere Interactions, Physiological Ecology Series, 85-105. Chidthaisong, A., Chin, K.-J., Valentine, D.L., Tyler, S.C., 2002. A comparison of isotope fractionation of carbon and hydrogen from paddy field rice roots and soil bacterial enrichments during CO2/H2 methanogenesis. Geochimica et Cosmochimica Acta 66, 983-995.

34

ACCEPTED MANUSCRIPT Coleman, D.D., Risatti, J.B., Schoell, M., 1981. Fractionation of carbon and hydrogen isotopes by methane-oxidizing bacteria. Geochimica et Cosmochimica Acta 45, 1033-1037.

PT

Conrad, R., 2005. Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Organic Geochemistry 36, 739-752.

RI

Conrad, R., Klose, M., Claus, P., 2002. Pathway of CH4 formation in anoxic rice field soil and rice roots determined by 13C-stable isotope fractionation. Chemosphere 47, 797-806.

SC

Conrad, R., Noll, M., Claus, P., Klose, M., Bastos, W.R., Enrich-Prast, A., 2011. Stable carbon isotope discrimination and microbiology of methane formation in tropical anoxic lake sediments. Biogeosciences 8, 795-814.

NU

Coplen, T.B., 1996. New guidelines for reporting stable hydrogen, carbon, and oxygen isotoperatio data. Geochimica et Cosmochimica Acta 60, 3359-3360.

MA

Demirel, B., Scherer, P., 2008. The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Reviews in Environmental Science and Bio/Technology 7, 173-190.

TE

D

DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P., Andersen, G.L., 2006. Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Applied and Environmental Microbiology 72, 5069-5072.

AC CE P

Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. Faiz, M., Hendry, P., 2006. Significance of microbial activity in Australian coal bed methane reservoirs—a review. Bulletin of Canadian Petroleum Geology 54, 261-272. Fakoussa, M.R., Hofrichter, M., 1999. Biotechnology and microbiology of coal degradation. Applied Microbiology and Biotechnology 52, 25-40. Fey, A., Claus, P., Conrad, R., 2004. Temporal change of 13C-isotope signatures and methanogenic pathways in rice field soil incubated anoxically at different temperatures. Geochimica et Cosmochimica Acta 68, 293-306. Flores, R.M., Rice, C.A., Stricker, G.D., Warden, A., Ellis, M.S., 2008. Methanogenic pathways of coal-bed gas in the Powder River Basin, United States: The geologic factor. International Journal of Coal Geology 76, 52-75. Galand, P.E., Yrjälä, K., Conrad, R., 2010. Stable carbon isotope fractionation during methanogenesis in three boreal peatland ecosystems. Biogeosciences Discussions 7, 5497-5515. Gelwicks, J.T., Risatti, J.B., Hayes, J.M., 1994. Carbon isotope effects associated with aceticlastic methanogenesis. Applied and Environmental Microbiology 60, 467-472.

35

ACCEPTED MANUSCRIPT Goevert, D., Conrad, R., 2009. Effect of substrate concentration on carbon isotope fractionation during acetoclastic methanogenesis by Methanosarcina barkeri and M. acetivorans and in rice field soil. Applied and Environmental Microbiology 75, 2605-2612.

PT

Golding, S.D., Boreham, C.J., Esterle, J.S., 2013. Stable isotope geochemistry of coal bed and shale gas and related production waters: A review. International Jounral of Coal Geology 120, 24-40.

SC

RI

Hamilton, S.K., Golding, S.D., Baublys, K.A., Esterle, J.S., 2014. Stable isotopic and molecular composition of desorbed coal seam gases from the Walloon Subgroup, eastern Surat Basin, Australia. International Journal of Coal Geology 122, 21-36.

NU

Hayes, J.M., 1993. Factors controlling 13C contents of sedimentary organic compounds: Principles and evidence. Marine Geology 113, 111-125.

MA

Jetten, M.S.M., Stams, A.J.M., Zehnder, A.J.B., 1992. Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiology Reviews 8, 181-197.

TE

D

Jones, E.J.P., Voytek, M.A., Corum, M.D., Orem, W.H., 2010. Stimulation of methane generation from nonproductive coal by addition of nutrients or a microbial consortium. Applied and Environmental Microbiology 76, 7013-7022.

AC CE P

Kendall, M., Boone, D., 2006. The Order Methanosarcinales, in: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., Stackebrandt, E. (Eds.), The Prokaryotes. Springer New York, pp. 244-256. Kinnon, E.C.P., Golding, S.D., Boreham, C.J., Baublys, K.A., Esterle, J.S., 2010. Stable isotope and water quality analysis of coal bed methane production waters and gases from the Bowen Basin, Australia. International Journal of Coal Geology 82, 219-231. Krüger, M., Beckmann, S., Engelen, B., Thielemann, T., Cramer, B., Schippers, A., Cypionka, H., 2008. Microbial methane formation from hard coal and timber in an abandoned coal mine. Geomicrobiology Journal 25, 315-321. Krzycki, J.A., Kenealy, W.R., DeNiro, M.J., Zeikus, J.G., 1987. Stable carbon isotope fractionation by Methanosarcina barkeri during methanogenesis from acetate, methanol, or carbon dioxide-hydrogen. Applied and Environmental Microbiology 53, 2597-2599. Liu, Y., Whitman, W.B., 2008. Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Annals of the New York Academy of Sciences 1125, 171-189. Londry, K.L., Dawson, K.G., Grover, H.D., Summons, R.E., Bradley, A.S., 2008. Stable carbon isotope fractionation between substrates and products of Methanosarcina barkeri. Organic Geochemistry 39, 608-621.

36

ACCEPTED MANUSCRIPT Milkov, A.V., 2011. Worldwide distribution and significance of secondary microbial methane formed during petroleum biodegradation in conventional reservoirs. Organic Geochemistry 42, 184-207.

PT

Miller, J.B., 2004. The carbon isotopic composition of atmospheric methane and its constraint on the global methane budget. Stable Isotopes and Biosphere-Atmosphere Interactions: Processes and Biological Controls. Elsevier Academic Press California, 288-306.

SC

RI

Mondav, R., Woodcroft, B.J., Kim, E.H., McCalley, C.K., Hodgkins, S.B., Crill, P.M., Chanton, J., Hurst, G.B., VerBerkmoes, N.C., Saleska, S.R., Hugenholtz, P., Rich, V.I., Tyson, G.W., 2014. Discovery of a novel methanogen prevalent in thawing permafrost. Nature Communications 5, 3212.

NU

Moran, J.J., House, C.H., Freeman, K.H., Ferry, J.G., 2005. Trace methane oxidation studied in several Euryarchaeota under diverse conditions. Archaea 1, 303-309.

MA

Nakagawa, F., Yoshida, N., Sugimoto, A., Wada, E., Yoshioka, T., Ueda, S., Vijarnsorn, P., 2002. Stable isotope and radiocarbon compositions of methane emitted from tropical rice paddies and swamps in Southern Thailand. Biogeochemistry 61, 1-19.

TE

D

Paul, D., Skrzypek, G., Forizs, I., 2007. Normalization of measured stable isotopic compositions to isotope reference scales—a review. Rapid Communications in Mass Spectrometry 21, 30063014.

AC CE P

Penger, J., Conrad, R., Blaser, M., 2012. Stable carbon isotope fractionation by methylotrophic methanogenic archaea. Applied and Environmental Microbiology 78, 7596-7602. Penning, H., Claus, P., Casper, P., Conrad, R., 2006. Carbon isotope fractionation during acetoclastic methanogenesis by Methanosaeta concilii in culture and a lake sediment. Applied and Environmental Microbiology 72, 5648-5652. Penning, H., Plugge, C.M., Galand, P.E., Conrad, R., 2005. Variation of carbon isotope fractionation in hydrogenotrophic methanogenic microbial cultures and environmental samples at different energy status. Global Change Biology 11, 2103-2113. Schink, B., 1997. Energetics of syntrophic cooperation in methanogenic degradation. Microbiology and Molecular Biology Reviews 61, 262-280. Schink, B., 2006. Syntrophic associations in methanogenic degradation, in: Overmann, J. (Ed.), Molecular basis of symbiosis. Springer Berlin Heidelberg, pp. 1-19. Schoell, M., 1980. The hydrogen and carbon isotopic composition of methane from natural gases of various origins. Geochimica et Cosmochimica Acta 44, 649-661. Smith, K.S., Ingram-Smith, C., 2007. Methanosaeta, the forgotten methanogen? Trends in Microbiology 15, 150-155.

37

ACCEPTED MANUSCRIPT Stams, A.M., 1994. Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie Van Leeuwenhoek 66, 271-294.

PT

Stams, A.J.M., Plugge, C.M., 2009. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews Microbiology 7, 568-577.

RI

Strąpoć, D., Mastalerz, M., Dawson, K., Macalady, J., Callaghan, A.V., Wawrik, B., Turich, C., Ashby, M., 2011. Biogeochemistry of microbial coal-bed methane. Annual Review of Earth and Planetary Sciences 39, 617-656.

NU

SC

Strąpoć, D., Mastalerz, M., Eble, C., Schimmelmann, A., 2007. Characterization of the origin of coalbed gases in southeastern Illinois Basin by compound-specific carbon and hydrogen stable isotope ratios. Organic Geochemistry 38, 267-287.

MA

Sugimoto, A., Wada, E., 1993. Carbon isotopic composition of bacterial methane in a soil incubation experiment: Contributions of acetate and CO2/H2. Geochimica et Cosmochimica Acta 57, 4015-4027. Sugimoto, A., Wada, E., 1995. Hydrogen isotopic composition of bacterial methane: CO2/H2 reduction and acetate fermentation. Geochimica et Cosmochimica Acta 59, 1329-1337.

TE

D

Susilawati, R., Esterle, J.S., Golding, S.D., Mares, T.E., 2015a. Microbial methane potential for the South Sumatra Basin coal: formation water screening and coal substrate bioavailability. Energy Procedia 65, 282-291.

AC CE P

Susilawati, R., Evans, P.N., Esterle, J.S., Robbins, S.J., Tyson, G.W., Golding, S.D., Mares, T.E., 2015b. Temporal changes in microbial community composition during culture enrichment experiments with Indonesian coals. International Journal of Coal Geology 137, 66-76. Susilawati, R., Papendick, S.L., Gilcrease, P.C., Esterle, J.S., Golding, S.D., Mares, T.E., 2013. Preliminary investigation of biogenic gas production in Indonesian low rank coals and implications for a renewable energy source. Journal of Asian Earth Sciences 77, 234-242. Suzuki, M.T., Béjà, O., Taylor, L.T., DeLong, E.F., 2001. Phylogenetic analysis of ribosomal RNA operons from uncultivated coastal marine bacterioplankton. Environmental Microbiology 3, 323-331. Tyler, S.C., Bilek, R.S., Sass, R.L., Fisher, F.M., 1997. Methane oxidation and pathways of production in a Texas paddy field deduced from measurements of flux, δl3C, and δD of CH4. Global Biogeochemical Cycles 11, 323-348. Valentine, D.L., Chidthaisong, A., Rice, A., Reeburgh, W.S., Tyler, S.C., 2004. Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens. Geochimica et Cosmochimica Acta 68, 1571-1590. Vavilin, V.A., Qu, X., Mazéas, L., Lemunier, M., Duquennoi, C., He, P., Bouchez, T., 2008. Methanosarcina as the dominant aceticlastic methanogens during mesophilic anaerobic digestion of putrescible waste. Antonie van Leeuwenhoek 94, 593-605. 38

ACCEPTED MANUSCRIPT Waldron, S., Watson‐Craik, I.A., Hall, A.J., Fallick, A.E., 1998. The carbon and hydrogen stable isotope composition of bacteriogenic methane: A laboratory study using a landfill inoculum. Geomicrobiology Journal 15, 157-169.

RI

PT

Wawrik, B., Mendivelso, M., Parisi, V.A., Suflita, J.M., Davidova, I.A., Marks, C.R., Van Nostrand, J.D., Liang, Y., Zhou, J., Huizinga, B.J., Strąpoć, D., Callaghan, A.V., 2012. Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin. FEMS Microbiology Ecology 81, 26-42.

SC

Whiticar, M.J., 1999. Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chemical Geology 161, 291-314.

NU

Whiticar, M.J., Faber, E., Schoell, M., 1986. Biogenic methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation–Isotope evidence. Geochimica et Cosmochimica Acta 50, 693–709.

MA

Winter, J., Knoll, G., 1989. Methanogens—Synthrophic dependence on fermentative and acetogenic bacteria in different ecosystems. Advances in Space Research 9, 107-116.

TE

D

Zhu, J., Zheng, H., Ai, G., Zhang, G., Liu, D., Liu, X., Dong, X., 2012. The genome characteristics and predicted function of methyl-group oxidation pathway in the obligate aceticlastic methanogens, Methanosaeta spp. PLoS ONE 7, e36756.

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Zinder, S.H., 1993. Physiological ecology of methanogens, in: Ferry, J.G. (Ed.), Methanogenesis: Ecology, Physiology, Biochemistry & Genetics. Chapman & Hall, New York, pp. 128-206.

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Methanogenesis investigated in cultures of South Sumatra Basin CBM waters. Cultures grown on South Sumatra Basin coal, acetate and H2+CO2. Stable isotopic and molecular DNA evidence for substrate depletion effects. αc and εc were better indicators of methanogenic pathway than δ13C-CH4 and δ2H-CH4. Possible positive extension of δ13C-CH4 values of acetoclastic methanogenesis.

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