{"title":"Wetland restoration suppresses microbial carbon metabolism by altering keystone species interactions.","authors":"Huijie Zheng, Deyan Liu, Ye Li, Zengming Chen, Junjie Li, Yanhong Dong, Cong Yang, Yuncai Miao, Junji Yuan, Weixin Ding","doi":"10.3389/fmicb.2025.1570703","DOIUrl":null,"url":null,"abstract":"<p><p>Soil bacteria play a pivotal role in regulating multifaceted functions of terrestrial ecosystems. Unraveling the succession of bacterial communities and the feedback mechanism on soil organic carbon (SOC) dynamics help embed the ecology of microbiome into C cycling model. However, how wetland restoration drives soil bacterial community assembly and species association to regulate microbial C metabolism remains unclear. Here, we investigated soil bacterial diversity, community structure and co-occurrence network, enzyme activities and SOC decomposition in restored wetlands for one, three, and four years from paddy fields in Northeast China. Wetland restoration for three and four years increased taxonomic (richness) and phylogenetic diversities by 2.39-3.96% and 2.13-3.02%, respectively, and increased the relative contribution of nestedness to community dissimilarity, indicating increased richness changed soil bacterial community structure. However, wetland restoration for three and four years decreased the richness index of aerobic Firmicutes by 5.04-5.74% due to stronger anaerobic condition characterized by increased soil Fe<sup>2+</sup>/Fe<sup>3+</sup> from 0.20 to 0.64. Besides, wetland restoration for four years decreased network complexity (characterized by decreased node number by 2.51%, edge number by 9.62%, positive/negative edge number by 6.37%, average degree by 5.74% and degree centralization by 6.34%). Robustness index decreased with the increase of restoration duration, while vulnerability index increased with the increase of restoration duration, indicating that wetland restoration decreased network stability of soil bacterial communities. These results might be because stronger anaerobic condition induced the decrease of aerobic Bacilli richness index in keystone module, thereby reducing positive association within keystone module. Decreased positive species association within keystone module in turn weakened microbial C metabolism by decreasing hydrolase activities from 7.49 to 5.37 mmol kg SOC<sup>-1</sup> h<sup>-1</sup> and oxidase activities from 627 to 411 mmol kg SOC<sup>-1</sup> h<sup>-1</sup>, leading to the decrease of SOC decomposition rate from 1.39 to 1.08 g C kg SOC<sup>-1</sup> during wetland restoration. Overall, our results suggested that although wetland restoration after agricultural abandonment increased soil bacterial diversity, it decreased positive association within Bacilli-dominated keystone module under stronger anaerobic condition, which weakened microbial C metabolism and SOC decomposition.</p>","PeriodicalId":12466,"journal":{"name":"Frontiers in Microbiology","volume":"16 ","pages":"1570703"},"PeriodicalIF":4.0000,"publicationDate":"2025-04-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12075313/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.3389/fmicb.2025.1570703","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Soil bacteria play a pivotal role in regulating multifaceted functions of terrestrial ecosystems. Unraveling the succession of bacterial communities and the feedback mechanism on soil organic carbon (SOC) dynamics help embed the ecology of microbiome into C cycling model. However, how wetland restoration drives soil bacterial community assembly and species association to regulate microbial C metabolism remains unclear. Here, we investigated soil bacterial diversity, community structure and co-occurrence network, enzyme activities and SOC decomposition in restored wetlands for one, three, and four years from paddy fields in Northeast China. Wetland restoration for three and four years increased taxonomic (richness) and phylogenetic diversities by 2.39-3.96% and 2.13-3.02%, respectively, and increased the relative contribution of nestedness to community dissimilarity, indicating increased richness changed soil bacterial community structure. However, wetland restoration for three and four years decreased the richness index of aerobic Firmicutes by 5.04-5.74% due to stronger anaerobic condition characterized by increased soil Fe2+/Fe3+ from 0.20 to 0.64. Besides, wetland restoration for four years decreased network complexity (characterized by decreased node number by 2.51%, edge number by 9.62%, positive/negative edge number by 6.37%, average degree by 5.74% and degree centralization by 6.34%). Robustness index decreased with the increase of restoration duration, while vulnerability index increased with the increase of restoration duration, indicating that wetland restoration decreased network stability of soil bacterial communities. These results might be because stronger anaerobic condition induced the decrease of aerobic Bacilli richness index in keystone module, thereby reducing positive association within keystone module. Decreased positive species association within keystone module in turn weakened microbial C metabolism by decreasing hydrolase activities from 7.49 to 5.37 mmol kg SOC-1 h-1 and oxidase activities from 627 to 411 mmol kg SOC-1 h-1, leading to the decrease of SOC decomposition rate from 1.39 to 1.08 g C kg SOC-1 during wetland restoration. Overall, our results suggested that although wetland restoration after agricultural abandonment increased soil bacterial diversity, it decreased positive association within Bacilli-dominated keystone module under stronger anaerobic condition, which weakened microbial C metabolism and SOC decomposition.
土壤细菌在调节陆地生态系统的多方面功能中起着关键作用。揭示细菌群落演替和土壤有机碳动态反馈机制有助于将微生物生态嵌入到碳循环模型中。然而,湿地恢复如何驱动土壤细菌群落聚集和物种关联来调节微生物C代谢尚不清楚。以东北水田为研究对象,研究了1年、3年和4年恢复湿地土壤细菌多样性、群落结构和共生网络、酶活性和有机碳分解。湿地恢复3年和4年使土壤细菌的分类(丰富度)多样性和系统发育多样性分别增加2.39 ~ 3.96%和2.13 ~ 3.02%,巢性对群落差异的相对贡献增加,说明丰富度的增加改变了土壤细菌群落结构。然而,3年和4年的湿地恢复使好氧厚壁菌门丰富度指数下降了5.04-5.74%,这是由于厌氧条件较强,土壤Fe2+/Fe3+从0.20增加到0.64。4年湿地恢复降低了网络复杂性(节点数减少2.51%,边数减少9.62%,正/负边数减少6.37%,平均程度减少5.74%,程度集中化减少6.34%)。稳健性指数随恢复时间的增加而降低,脆弱性指数随恢复时间的增加而增加,表明湿地恢复降低了土壤细菌群落的网络稳定性。这可能是由于较强的厌氧条件导致keystone模块中好氧杆菌丰富度指数下降,从而降低了keystone模块内的正相关性。keystone模块内正相关物种的减少反过来又削弱了微生物的碳代谢,水解酶活性从7.49降低到5.37 mmol kg SOC-1 h-1,氧化酶活性从627降低到411 mmol kg SOC-1 h-1,导致湿地恢复过程中有机碳分解率从1.39降低到1.08 g C kg SOC-1。总体而言,我们的研究结果表明,尽管农业废弃地后湿地恢复增加了土壤细菌多样性,但在厌氧条件较强的情况下,bacillii主导的keystone模块内的正相关关系减弱,从而削弱了微生物C代谢和SOC分解。
期刊介绍:
Frontiers in Microbiology is a leading journal in its field, publishing rigorously peer-reviewed research across the entire spectrum of microbiology. Field Chief Editor Martin G. Klotz at Washington State University is supported by an outstanding Editorial Board of international researchers. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide.