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Abstract. The recently discovered cryptic methane cycle in the sulfate-reducing zone of marine and wetland sediment couples methylotrophic methanogenesis to anaerobic oxidation of methane (AOM). Here we present evidence of cryptic methane cycling activity within the upper regions of the sulfate-reducing zone, along a depth transect within the Santa Barbara Basin, off the coast of California, USA. The top 0–20 cm of sediment from each station was subjected to geochemical analyses and radiotracer incubations using 35S–SO42-, 14C–mono-methylamine, and 14C–CH4 to find evidence of cryptic methane cycling. Methane concentrations were consistently low (3 to 16 µM) across the depth transect, despite AOM rates increasing with decreasing water depth (from max 0.05 nmol cm−3 d−1 at the deepest station to max 1.8 nmol cm−3 d−1 at the shallowest station). Porewater sulfate concentrations remained high (23 to 29 mM), despite the detection of sulfate reduction activity from 35S–SO42- incubations with rates up to 134 nmol cm−3 d−1. Metabolomic analysis showed that substrates for methanogenesis (i.e., acetate, methanol and methylamines) were mostly below the detection limit in the porewater, but some samples from the 1–2 cm depth section showed non-quantifiable evidence of these substrates, indicating their rapid turnover. Estimated methanogenesis from mono-methylamine ranged from 0.2 to 0.5 nmol cm−3 d−1. Discrepancies between the rate constants (k) of methanogenesis (from 14C–mono-methylamine) and AOM (from either 14C–mono-methylamine-derived 14C–CH4 or from directly injected 14C–CH4) suggest the activity of a separate, concurrent metabolic process directly metabolizing mono-methylamine to inorganic carbon. We conclude that the results presented in this work show strong evidence of cryptic methane cycling occurring within the top 20 cm of sediment in the Santa Barbara Basin. The rapid cycling of carbon between methanogenesis and methanotropy likely prevents major build-up of methane in the sulfate-reducing zone. Furthermore, our data suggest that methylamine is utilized by both methanogenic archaea capable of methylotrophic methanogenesis and non-methanogenic microbial groups. We hypothesize that sulfate reduction is responsible for the additional methylamine turnover, but further investigation is needed to elucidate this metabolic activity.
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Nitrous oxide inhibition of methanogenesis represents an underappreciated greenhouse gas emission feedback
Methane (CH4) and nitrous oxide (N2O) are major greenhouse gases that are predominantly generated by microbial activities in anoxic environments. N2O inhibition of methanogenesis has been reported, but comprehensive efforts to obtain kinetic information are lacking. Using the model methanogen Methanosarcina barkeri strain Fusaro and digester sludge-derived methanogenic enrichment cultures, we conducted growth yield and kinetic measurements and showed that micromolar concentrations of N2O suppress the growth of methanogens and CH4 production from major methanogenic substrate classes. Acetoclastic methanogenesis, estimated to account for two-thirds of the annual 1 billion metric tons of biogenic CH4, was most sensitive to N2O, with inhibitory constants (KI) in the range of 18–25 μM, followed by hydrogenotrophic (KI, 60–90 μM) and methylotrophic (KI, 110–130 μM) methanogenesis. Dissolved N2O concentrations exceeding these KI values are not uncommon in managed (i.e. fertilized soils and wastewater treatment plants) and unmanaged ecosystems. Future greenhouse gas emissions remain uncertain, particularly from critical zone environments (e.g. thawing permafrost) with large amounts of stored nitrogenous and carbonaceous materials that are experiencing unprecedented warming. Incorporating relevant feedback effects, such as the significant N2O inhibition on methanogenesis, can refine climate models and improve predictive capabilities.
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- Award ID(s):
- 1831599
- PAR ID:
- 10563296
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 18
- Issue:
- 1
- ISSN:
- 1751-7362
- Page Range / eLocation ID:
- wrae027
- Subject(s) / Keyword(s):
- nitrous oxide, methane, greenhouse gas emissions, inhibition, feedback loop, climate change
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/ismejo/wrae027
