Abstract

Recent studies employing novel analytical tools provide detailed, microscopic portraits of archaea/sulfate-reducing bacteria aggregates in sediments from methane seep and vent sites. One of the most striking features of these aggregates is that lipid and cell carbon are highly depleted in <sup>13</sup>C (δ<sup>13</sup>C &lt; −60‰). Biogenic methane, with δ<sup>13</sup>C values of −50 to −110 permil, is a logical candidate for carbon source of these aggregates. Accordingly, it is widely assumed that the archaea oxidize and assimilate methane, and that methane-derived carbon is transferred to the sulfate-reducing bacteria (SRB) symbionts as CO<sub>2</sub> or as a partially oxidized intermediate. However, methane is not the only possible source of <sup>13</sup>C-depleted carbon in archaea/SRB aggregates. ΣCO<sub>2</sub> in sediments at seep and vent sites tends to be isotopically “light” due to decomposition of organic matter derived from chemoautotrophic organisms. In addition, CO<sub>2</sub> is depleted in <sup>13</sup>C by ∼10 permil compared to ΣCO<sub>2</sub> owing to the equilibrium isotope effect. Assimilation of this “light” CO<sub>2</sub> by methanogenic archaea and autotrophic SRB, combined with enzymatic isotope effects, could also yield lipid and biomass that are highly depleted in <sup>13</sup>C. We derive general equations based on isotope mass-balance and calibrated with laboratory and field data to predict the isotopic composition of archaeal cell carbon and lipids derived from autotrophic methanogenesis and anaerobic methane oxidation. The calculations show that observed δ<sup>13</sup>C values for archaeal biomass and lipids at methane seep and vent sites are readily accounted for by isotope fractionation during methane production from CO<sub>2</sub>, and that biomass produced during anaerobic methane oxidation is only slightly depleted in <sup>13</sup>C relative to methane unless the enzymatic isotope effect associated with the anabolic arm of the assimilation-dissimilation branch point is considerably larger than the isotope effect associated with the catabolic arm. We also apply an isotope diffusion-reaction model to demonstrate that micro-gradients in δ<sup>13</sup>C-CO<sub>2</sub> cannot be maintained within archaea/SRB aggregates. However, <sup>13</sup>C-depleted carbon in SRB members of the aggregate is readily explained by autotrophic sulfate-reduction with bulk porewater CO<sub>2</sub> as carbon source. These results illustrate that <sup>13</sup>C-depleted biomass and lipids observed in sediments from methane seep and vent sites may be derived from CO<sub>2</sub>-reducing archaea and autotrophic sulfate-reducing bacteria. The inference of anaerobic methanotrophy based on <sup>13</sup>C depletion in archaeal and sulfate-reducing bacterial cell carbon and/or lipids should be considered tentative unless corroborated by independent, concordant evidence of net methane consumption.

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