The role of oxygen in stimulating methane production in wetlands

Abstract

Methane (CH4), a potent greenhouse gas, is the second most important greenhouse gas contributor to climate change after carbon dioxide (CO2). The biological emissions of CH4 from wetlands are a major uncertainty in CH4 budgets. Microbial methanogenesis by Archaea is an anaerobic process accounting for most biological CH4 production in nature, yet recent observations indicate that large emissions can originate from oxygenated or frequently oxygenated wetland soil layers. To determine how oxygen (O2) can stimulate CH4 emissions, we used incubations of Sphagnum peat to demonstrate that the temporary exposure of peat to O2 can increase CH4 yields up to 2000‐fold during subsequent anoxic conditions relative to peat without O2 exposure. Geochemical (including ion cyclotron resonance mass spectrometry, X‐ray absorbance spectroscopy) and microbiome (16S rDNA amplicons, metagenomics) analyses of peat showed that higher CH4 yields of redox‐oscillated peat were due to functional shifts in the peat microbiome arising during redox oscillation that enhanced peat carbon (C) degradation. Novosphingobium species with O2‐dependent aromatic oxygenase genes increased greatly in relative abundance during the oxygenation period in redox‐oscillated peat compared to anoxic controls. Acidobacteria species were particularly important for anaerobic processing of peat C, including in the production of methanogenic substrates H2 and CO2. Higher CO2 production during the anoxic phase of redox‐oscillated peat stimulated hydrogenotrophic CH4 production by Methanobacterium species. The persistence of reduced iron (Fe(II)) during prolonged oxygenation in redox‐oscillated peat may further enhance C degradation through abiotic mechanisms (e.g., Fenton reactions). The results indicate that specific functional shifts in the peat microbiome underlie O2 enhancement of CH4 production in acidic, Sphagnum‐rich wetland soils. They also imply that understanding microbial dynamics spanning temporal and spatial redox transitions in peatlands is critical for constraining CH4 budgets; predicting feedbacks between climate change, hydrologic variability, and wetland CH4 emissions; and guiding wetland C management strategies.

Genome-Resolved Metagenomics Informs the Functional Ecology of Uncultured Acidobacteria in Redox Oscillated Sphagnum Peat

“…Acidic, sphagnum-dominated peatlands are among the preferred habitats for many Acidobacteria lineages ( 16 – 22 ), and this could be attributed to their vast hydrolytic capabilities, which are associated with the degradation of complex plant-derived polysaccharides ( 18 , 22 ). Peat organic matter (OM) is predominantly composed of condensed aromatics and plant-derived polymers, such as cellulose, pectin, and hemicellulose, the degradation of which is the primary step toward the anaerobic decomposition of peat OM ( 23 – 26 ). Various hydrolytic extracellular enzymes produced by microorganisms are the key catalytic agents mediating these degradation pathways ( 24 ).…”

“…Various hydrolytic extracellular enzymes produced by microorganisms are the key catalytic agents mediating these degradation pathways ( 24 ). Their activities, however, may be inhibited by phenolic compounds that are typically abundant in peat systems ( 27 , 28 ), leading to a mechanistic control on the growth and activity of microbial decomposers, although the evidence for this “enzyme latch” theory is variable ( 26 , 29 ).…”

Metagenomic evidence of suppressed methanogenic pathways along soil profile after wetland conversion to cropland

“…Thus, we can suspect that substrate would be the limiting factor to CH 4 production in wetlands, proving the high CH 4 cost of sequestering carbon in the wetland (Hemes et al, 2018 ). However, the aerobic of cropland soil would alleviate the substrate limitation because the temporary exposure of soil to oxygen could stimulate carbon degradation (Wilmoth et al, 2021 ). This biogeochemical compromise between high CH 4 emission in wetland and high carbon loss in cropland would also be impressive and worth quantitative estimating in the cultivation and restoration process.…”

Spatial distribution and biogeochemistry of redox active species in arctic sedimentary porewaters and seeps

“…11,12 Conversely, enzymatic activity by aerobic microbes or abiotic reactions involving oxygen and Fe(II)-mediated (Fenton) pathways may promote organic matter mineralization, enhancing methanogenesis. 1,[13][14][15] Currently, little is known about the spatial distribution and abundances of important redox active species in sediment porewaters from Arctic lacustrine systems due to the logistical challenges of conducting measurements in these remote and extreme environments. Previous studies in the Arctic that measured the spatial distribution and abundance of redoxactive species have indicated great heterogeneity of TEA distribution and methane generation between lakes and within lakes that make it difficult to understand carbon cycling on larger scales.…”

“…11,12 Conversely, enzymatic activity by aerobic microbes or abiotic reactions involving oxygen and Fe( ii )-mediated (Fenton) pathways may promote organic matter mineralization, enhancing methanogenesis. 1,13–15…”