Stimulated Organic Carbon Cycling and Microbial Community Shift Driven by a Simulated Cold-Seep Eruption

Cold seeps are a major methane source in marine systems, and microbe-mediated anaerobic oxidation of methane (AOM) serves as an effective barrier for preventing methane emissions from sediment to water. However, how the periodic eruption of cold seeps drives the microbial community shift and further affects carbon cycling has been largely neglected, mainly due to the technical challenge of analyzing the in situ communities undergoing such geological events. Using a continuously running high-pressure bioreactor to simulate these events, we found that under the condition of simulated eruptions, the abundance of AOM-related species decreased, and some methane was oxidized to methyl compounds to feed heterotrophs. The methanogenic archaeon Methanolobus replaced ANME-2a as the dominant archaeal group; moreover, the levels of methylotrophic bacteria, such as Pseudomonas, Halomonas, and Methylobacter, quickly increased, while those of sulfate-reducing bacteria decreased. According to the genomic analysis, Methylobacter played an important role in incomplete methane oxidation during eruptions; this process was catalyzed by the genes pmoABC under anaerobic conditions when the methane pressure was high, possibly generating organic carbon. Additionally, the findings showed that methyl compounds can also be released to the environment during methanogenesis and AOM under eruption conditions when the methane pressure is high. IMPORTANCE In the ocean, almost all of the emission and consumption of deeply buried methane occurs in cold seeps; therefore, understanding the methane cycling in cold seeps is crucial to estimating the oceanic methane budget. Cold-seep eruptions often lead to the dramatic destruction of microbial ecosystems that drive methane cycling. Because of technical challenges, the direct monitoring of these communities as well as the activity shifts during eruptions has never been achieved. In this study, we took an alternative approach by simulating cold-seep eruptions and using genome-resolved metagenomics to interpret the dynamic changes in the microbial community. The results show that the periodical cold-seep eruptions intensify organic carbon cycling, undermine the direct oxidation of methane to carbon dioxide, and drive microbial community shifts. These results further suggest that a more sophisticated calculation of the methane budget in cold seeps that considers their eruption status is needed.