Stand age-related effects of mangrove on archaeal methanogenesis in sediments: Community assembly and co-occurrence patterns

by Lingfang Ni, Jiaping Wu, Hongyue Dang, Carlos M.Duarte, Kai Feng, Ye Deng, Daoqiong Zheng, Dongdong Zhang
Year: 2024 DOI: https://doi.org/10.1016/j.scitotenv.2024.176596

Abstract

Mangrove sediment is a key source of methane emissions; however, archaea community structure dynamics and methanogenesis activities during long-term mangrove restoration remain unclear. In this study, microcosm incubations revealed a substantial reduction in microbial-mediated methane production potential from mangrove sediments with increasing stand age; methane production rates decreased from 0.42 ng g−1 d−1 in 6-year-old stands to 0.23 ng g−1 d−1 in 64-year-old stands. High-throughput sequencing revealed a reduction in community diversity because of specific microorganism colonization and species loss, notably a decline in the relative abundance of Bathyarchaeia in sediments of 64-year-old stands. In addition, mangrove sediments, especially those in older stands (20- and 64-year-old), had more complex and stable co-occurrence microbial networks than mudflats. Furthermore, archaea community assembly in older stands was dominated by stochastic processes wherein dispersal limitation was prominent, and that in younger stands (6- and 12-year-old) was driven by deterministic processes. The proportion of dispersal limitation of Bathyarchaeia and traditional methanogens in sediment decreased with an increase in stand age. Quantitative polymerase chain reaction analysis confirmed a decrease in Bathyarchaeia (from 3.50 to 0.54 copies g−1) and mcrA gene (from 3.83 to 0.25 copies g−1) abundance in mangrove sediments with an increase in stand age. These findings demonstrate the critical role of Bathyarchaeia in methanogenesis; the decline in microbial interactions and abundance, and the reduced proportion of dispersal limitation of Bathyarchaeia and traditional methanogens collectively contributed to the mitigation of microbial-mediated methane production potential in older mangrove stands.