Organic carbon oxidation state shapes fermentative methanogenic microbiomes and controls greenhouse gas fluxes

Organic compounds with a negative nominal oxidation state of carbon (NOSC) are thermodynamically recalcitrant in anaerobic ecosystems, but few studies have measured the influence of NOSC on carbon degradation rates, gaseous product yields, or microbiome composition. We amended anaerobic rice paddy sediment microcosms with water-soluble monomeric organic carbon compounds varying in NOSC. Consistent with thermodynamic and stoichiometric predictions, negative NOSC compounds are catabolized more slowly but produce more methane per mole of carbon. Negative NOSC microbiomes have higher alpha diversity, more syntrophs and methanogens, and fewer fermentative bacteria. Strikingly, fermentative bacterial taxa display genomically encoded NOSC catabolic preferences both in the lab and field. Negative NOSC-preferring fermenters have longer predicted doubling times, consistent with the thermodynamic recalcitrance of their preferred substrates. We propose that microbial NOSC catabolic preferences may reflect the thermodynamic niche of microorganisms and we anticipate that extending research on microbial catabolic preferences to a greater variety of organic carbon substrates and diverse microbiomes will improve our understanding of microbial carbon cycling and trait evolution.