Investigation on the aerobic methanotrophic community and the dominant taxon Methylomarinum in seagrass ecosystem.

Background: Methanotrophs are a key biological methane sink, and aerobic methanotrophs critically reduce wetland methane emissions under global climate change. However, despite their ecological significance, investigations on aerobic methanotrophs within seagrass ecosystems remain scant. In this study, microcosmic culture experiments were used to assess aerobic methane oxidation (AMO) potential and its drivers across a vertical gradient of seagrass sediments. Moreover, the methanotrophic community structure was characterized by amplicon sequencing, and the dominant methanotroph's metagenome-assembled genome (MAG) and metabolic pathway was investigated.

Results: Sediments of Halophila ovalis exhibited notable vertical differences in both physicochemical properties and methane oxidation rates. Furthermore, ammonium nitrogen (NH₄⁺-N) decreased with sediment depth, and was suggested by structural equation modeling (SEM) to significantly contribute to the vertical methane oxidation variability. Microbial community structure analysis revealed that type I methanotrophs were stimulated by methane addition and significantly impacted the oxidation of elevated methane, with Methylomarinum being the dominant taxon. Through metagenomic analysis, we assembled a phylogenetically novel methanotroph, Candidatus Methylomarinum sp. MAG81, which is distantly related to the extant Methylomarinum vadi IT-4. We conducted a comparative analysis of the two genomes and discovered that MAG81 not only possesses the capability for methane oxidation but also has the ability to participate in methanol oxidation via Xox-MDH. Furthermore, MAG81 also harbors nitrogen metabolism genes, particularly those involved in nitrogen fixation (nifHDK). This genetic characteristic suggests a potential role for MAG81 in facilitating the carbon and nitrogen cycles within seagrass ecosystems.

Conclusions: In summary, our study revealed that the vertical variation of NH₄⁺-N significantly affected methane oxidation and that type I methanotrophs, especially the genus Methylomarinum played an important role in oxidizing methane in seagrass sediments, shedding new insights into the methane abatement in the seagrass ecosystem, which is essential for climate change mitigation.