Authors
Weikang Sui, Longhui Deng, Bing-Zheng Wu, Guang-Chao Zhuang, Zian Tong, Ningyuan Lu, Danyue Huang, Zheng Xiong, Peng Guo, Xianbiao Lin, Yanwei Wang, Liang Dong, Fengping Wang
Published in
mBio. Pages e0144626. Jul 31, 2026. Epub Jul 31, 2026.
Abstract
Methane oxidation coupled to sulfate reduction is the dominant process restricting methane release from cold seeps. Methane oxidation can also be coupled to nitrate/nitrite reduction, thereby linking the cycles of CH4, CO2, and N2O. However, how this coupling shifts during seep development and its impact on N2O production remains poorly understood. Here, we integrated geochemical profiling, 14C-based labeling, and omics-based analyses to quantify the process rates, identify the key microbial mediators, and assess the net N2O production across the developmental stages of cold seeps in the South China Sea. In an early-stage, polychaete-dominated seep, the depth-integrated, potential nitrate/nitrite-coupled methane oxidation rate reached 21.9 ± 3.0 mmol C/m2/day, accounting for 36%-73% of the total methane oxidation. By contrast, in a typical epifauna-prevalent mature seep, this contribution diminished to ~1% (0.62 ± 0.16 mmol C/m2/day), while sulfate-dependent methane oxidation became dominant. Omics data identified the predominant methane-oxidizing bacteria Methyloprofundus and QPIN01 (relative abundances of 7%-24%) as the potential mediators of nitrate/nitrite-coupled methane oxidation in the early-stage seep sediments. Consistent with the absence of N2O-reduction gene nosZ in these lineages, simultaneous nitrate and methane amendments significantly stimulated net N2O production by 14%-46% in the early-stage seep sediments. This increase correlated strongly with the potential nitrate/nitrite-coupled methane oxidation rate and was estimated to offset 41% ± 9% of the climate benefit gained through methane oxidation. These findings revealed the previously unrecognized successional dynamics of dominant methane oxidation pathways and necessitate the incorporation of nitrate/nitrite-coupled methane oxidation into assessments of greenhouse-gas release from these globally distributed ecosystems.IMPORTANCECold seep biota are widely regarded as a critical "biofilter" that restricts seafloor methane emission, mainly through coupled methane and sulfur cycling. This study refines this prevailing view by demonstrating a major shift in the dominant methane oxidation pathway during seep ecosystem development. Contrasting to the dominance of sulfate-coupled methane oxidation in mature seep systems, the early-stage seep is dominated by nitrate/nitrite-coupled methane oxidation, a process primarily mediated by methane-oxidizing bacteria. Crucially, these organisms possess a truncated denitrification pathway that leads to the production of nitrous oxide (N2O), a greenhouse gas with nearly 10 times the warming potential of methane. The resulting net N2O production thereby substantially offsets the climate benefit achieved by methane consumption. This study highlights the dual role of cold seep microbiota in regulating climate-active gases, underscoring that accurate assessment of their environmental impact requires a holistic understanding of temporal changes in coupled carbon and nitrogen cycles.
PMID:
42536394
Bibliographic data and abstract were imported from PubMed on 31 Jul 2026.
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