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Hydrogen and Carbon Isotope Systematics in Hydrogenotrophic Okumura et al. Progress in Earth and Planetary Science (2016) 3:14 Progress in Earth and DOI 10.1186/s40645-016-0088-3 Planetary Science RESEARCH ARTICLE Open Access Hydrogen and carbon isotope systematics in hydrogenotrophic methanogenesis under H2-limited and H2-enriched conditions: implications for the origin of methane and its isotopic diagnosis Tomoyo Okumura1,2, Shinsuke Kawagucci1,2,3*, Yayoi Saito2,4, Yohei Matsui2,3, Ken Takai1,2,3 and Hiroyuki Imachi2,3 Abstract Hydrogen and carbon isotope systematics of H2O–H2–CO2–CH4 in hydrogenotrophic methanogenesis and their relation to H2 availability were investigated. Two H2-syntrophic cocultures of fermentatively hydrogenogenic bacteria 2 and hydrogenotrophic methanogens under conditions of <10 Pa-H2 and two pure cultures of hydrogenotrophic 5 methanogens under conditions of ~10 Pa-H2 were tested. Carbon isotope fractionation between CH4 and CO2 during hydrogenotrophic methanogenesis was correlated with pH2, as indicated in previous studies. The hydrogen isotope ratio of CH4 produced during rapid growth of the thermophilic methanogen Methanothermococcus okinawensis under 5 high pH2 conditions (~10 Pa) was affected by the isotopic composition of H2, as concluded in a previous study of Methanothermobacter thermautotrophicus “δ ” .This DH2 effect is a possible cause of the diversity of previously reported values for hydrogen isotope fractionation between CH4 and H2OexaminedinH2-enriched culture experiments. δ δ Hydrogen isotope fractionation between CH4 and H2O, defined by (1000 + DCH4 )/(1000 + DH2O), during hydrogenotrophic methanogenesis of the H2-syntrophic cocultures was in the range 0.67–0.69. The hydrogen isotope fractionation of our H2-syntrophic dataset overlaps with those obtained not only from low-pH2 experiments reported so far but also from natural samples of “young” methane reservoirs (0.66–0.74). Conversely, such hydrogen isotope fractionation is not consistent with that of “aged” methane in geological samples (≥0.79), which has been regarded as methane produced via hydrogenotrophic methanogenesis from the carbon isotope fractionation. As a possible process inducing the inconsistency in hydrogen isotope signatures between experiments and geological samples, we hypothesize that the hydrogen isotope signature of CH4 imprinted at the time of methanogenesis, as in the experiments and natural young methane, may be altered by diagenetic hydrogen isotope exchange between extracellular CH4 and H2O through reversible reactions of the microbial methanogenic pathway in methanogenic region and/or geological methane reservoirs. Keywords: Methane, Hydrogenotrophic methanogenesis, Hydrogen isotope ratio, Carbon isotope ratio, H2 availability, Culture experiments * Correspondence: [email protected] 1Laboratory of Ocean-Earth Life Evolution Research (OELE), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan 2Department of Subsurface Geobiological Analysis and Research (D-SUGAR), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan Full list of author information is available at the end of the article © 2016 Okumura et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Okumura et al. Progress in Earth and Planetary Science (2016) 3:14 Page 2 of 19 Background Yoshioka et al. 2008; Hattori et al. 2012; Stolper et al. Methane is a greenhouse gas, a primary product of meth- 2015; Wang et al. 2015) and by observations on anogenic archaea, a useful fuel for human activity, and the methane-bearing environments (e.g., Nakai et al. 1974; simplest organic molecular. The geochemical origins of Whiticar et al. 1986; Burke 1993; Waldron et al. 1999). methane in environmental samples have been investigated Large variation of the CH4–H2O hydrogen isotope in terms of global warming (e.g., Patra et al. 2011), limits fractionation has been reported in previous studies of the deep biosphere (e.g., Inagaki et al. 2015), exploration (Additional file 1), and the possible relationship between and development of energy resources (e.g., Kvenvolden the fractionation and the H2 availability in the methano- 1988), and prebiotic chemical evolution on the early Earth genic environment has been discussed (Burke 1993; (e.g., McCollom 2013). The geochemical origin of methane Yoshioka et al. 2008; Hattori et al. 2012; Stolper et al. can be classified into four types in terms of the carbon 2015; Wang et al. 2015). On the other hand, Kawagucci source (inorganic vs. organic) and the generation process et al. (2014) recently demonstrated that the hydrogen (chemical vs. microbial): abiotic, thermogenic, aceticlastic isotope ratio of substrate H2 also affects the hydrogen and methylotrophic, and hydrogenotrophic methane (e.g., isotope ratio of the produced CH4 during the rapid Kawagucci et al. 2013a). Because hydrogenotrophic growth of a thermophilic methanogen, Methanothermo- methanogenesis is one of the most important energy bactor thermautotrophicus strain ΔH, in H2-enriched metabolisms in living ecosystems in the ancient Earth batch culture. If this “δDH2 effect” occurs ubiquitously in and habitable extraterrestrial environments (McCollom other hydrogenotrophic methanogens and under other 1999; Takai et al. 2004; Hsu et al. 2015), distinguishing growing conditions such as low H2 availability, it may be hydrogenotrophic methanogenesis from the other necessary to reconsider the geochemical implications of methanogenic processes is a key to discuss whether life the traditional interpretation based on the CH4–H2O is present or absent there. hydrogen isotope ratio fractionation. The stable isotope ratios of carbon (13C/12C) and In this study, we therefore investigated the hydrogen hydrogen (D/H) in methane have been used as geochem- and carbon isotope systematics of H2O–H2–CO2–CH4 ical tracers to deduce its origin (e.g., Schoell 1980; 1988; during the growth of different hydrogenotrophic metha- Whiticar et al. 1986; Whiticar 1999). Although the use- nogens under various growth conditions and the effect fulness of the stable isotope tracers for methane origins of H2 availability. We tested two different species of have been long debated (Martini et al. 1996; Waldron methanogens under syntrophic growth conditions with et al. 1999; Tang et al. 2000), the stable isotope diagnosis fermentatively hydrogenogenic bacteria that attained 2 becomes more accurate by enhancing the understanding very low H2 availability (corresponding to <10 Pa-H2 in of stable isotope systematics with respect to each of the the headspace gas) and two different species of hydroge- methanogenic processes in addition to subsequent alter- notrophic methanogens under H2-enriched growth condi- 5 ation of the imprinted isotope signature. For this pur- tions (~10 Pa-H2 in the headspace gas). This is the first pose, carbon isotope fractionation between CH4 and attempt to monitor both hydrogen and carbon isotope CO2 in hydrogenotrophic methanogenesis has been well systematics in low-pH2 cultures, although the hydrogen studied by laboratory incubations (e.g., Valentine et al. and carbon isotope systematics have been investigated 2004; Penning et al. 2005; Takai et al. 2008). The magni- separately (Penning et al. 2005; Yoshioka et al. 2008) tude of the carbon isotope fractionation is thought to (Additional file 1). Compilation of the hydrogen and car- depend on the thermodynamic state of the methano- bon isotope fractionations from the experimental results genic environment: a greater 13C-depletion in the pro- and environmental observations reveals three provinces in duced CH4 occurs at a lower H2 availability. This the dataset and provides new insights into stable isotope relationship has been explained by “differential revers- diagnosis of the origin and fate of environmental methane. ibility” in the multistep pathway of methanogenesis from H2 and CO2 (Valentine et al. 2004): higher reversibility Methods exhibits at a lower H2 availability. Organism details and medium compositions In contrast to the carbon isotopic characteristics, the Table 1 provides information on the four culture sets hydrogen isotope characteristics of hydrogenotrophic and the experimental conditions used in this study. To methanogenesis remain less understood. In general, the assess the growth of methanogens under low H2-avail- hydrogen isotope ratio of produced CH4 is related solely ability conditions at different temperatures, two species to that of H2O (e.g., Daniels et al. 1980). Based on this of butyrate-oxidizing hydrogenogenic fermentative bac- finding, numerous studies have examined the CH4–H2O teria were cocultured with two species of methanogens hydrogen isotope fractionation both in experiments as syntrophic consortia at 55 °C and 25 °C (thermophilic using various methanogen cultures (Balabane et al. 1987; and mesophilic cocultures). The partial pressure of H2 2 Sugimoto and Wada 1995; Valentine et al. 2004; for the cocultures was lower than 10 Pa-H2 during the Okumura et al. Progress in Earth and Planetary Science (2016) 3:14 Page 3 of 19 Table 1 Experimental and organismal information examined in
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