Temporal and Spatial Dynamics of Microbial Community Composition and Functional Potential in Mangrove Wetlands over a Seven-Year Period

Microbial communities are essential to sustaining ecosystem functions in mangrove wetlands, yet their long-term responses to environmental changes remain poorly characterized. Here, we conducted a seven-year multiomics investigation (2017–2023) of microbial diversity, functionality, and evolutionary dynamics in the Futian Mangrove National Nature Reserve, Shenzhen, China. This region has experienced ecological degradation followed by phased restoration efforts since 2007. By analyzing 81 metagenomes, 8474 microbial metagenome-assembled genomes (MAGs) were successfully reconstructed, representing 13 archaeal phyla, 70 bacterial phyla, and up to 95% newly identified species. Community composition was primarily influenced by sediment depth and seasonal variations. Integrating 72 metatranscriptomes revealed marked temporal shifts in gene expression linked to carbon, nitrogen, and sulfur cycling, including enhanced transcription of genes involved in organic carbon oxidation, sulfate reduction, denitrification, and nitrogen fixation during later stages restoration. Evolutionary analyses demonstrated pervasive purifying selection across microbial lineages, with environmental fluctuations and genome size acting as key determinants of selective pressures. Additionally, a new class Candidatus Shennongiarchaeia within Thermoplasmatota was proposed, exhibited anaerobic, facultatively heterotrophic characteristics and bioactive compound synthesis potential. These findings demonstrate that microbial communities in restored mangrove wetlands undergo structural and functional reorganization, characterized by the enrichment of anaerobic lineages, upregulation of key metabolic pathways, and environmentally driven selective pressures. This long-term study deepens our understanding of microbial resilience and adaptation in mangrove ecosystems, with implications for future conservation and restoration strategies in coastal wetlands.