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.

微生物群落对于维持红树林湿地的生态系统功能至关重要，然而其对环境变化的长期响应机制仍未得到充分解析。本研究针对中国深圳福田红树林国家级自然保护区内的微生物多样性、功能特性及演化动态，开展了为期7年（2017—2023年）的多组学调查。该区域自2007年以来先后经历了生态退化与分阶段修复治理过程。通过对81份宏基因组（metagenome）样本的分析，本研究成功重建了8474个微生物宏基因组组装基因组（metagenome-assembled genomes, MAGs），涵盖13个古菌门、70个细菌门，其中多达95%的物种为新鉴定物种。微生物群落组成主要受沉积物深度与季节变化的调控。整合72份宏转录组（metatranscriptome）数据的分析结果显示，与碳、氮、硫循环相关的基因表达呈现显著的时间动态变化，其中在修复后期阶段，参与有机碳氧化、硫酸盐还原、反硝化及固氮过程的基因转录水平显著上调。演化分析表明，微生物类群普遍经历了纯化选择，环境波动与基因组大小是决定选择压力的关键因素。此外，本研究在热原体门（Thermoplasmatota）中提议建立一个全新的候选纲——"Candidatus Shennongiarchaeia"，该类群具备厌氧、兼性异养的代谢特性，并具有合成生物活性化合物的潜力。上述研究结果表明，修复后的红树林湿地微生物群落会发生结构与功能层面的重塑，具体表现为厌氧类群的富集、关键代谢通路的上调以及环境驱动的选择压力作用。本项长期研究深化了学界对红树林生态系统中微生物群落韧性与适应性的认知，同时可为未来滨海湿地的保护与修复策略提供理论参考。