Enhanced microbial network stability and biogeochemical cycles in saline-alkali soil through simplified prokaryotes and complex fungal networks

IF 4.8 2区 农林科学 Q1 SOIL SCIENCE
Ruihong Wang , Hao Qin , Zhijian Shi , Mengben Wang , Junjian Li
{"title":"Enhanced microbial network stability and biogeochemical cycles in saline-alkali soil through simplified prokaryotes and complex fungal networks","authors":"Ruihong Wang ,&nbsp;Hao Qin ,&nbsp;Zhijian Shi ,&nbsp;Mengben Wang ,&nbsp;Junjian Li","doi":"10.1016/j.apsoil.2025.106245","DOIUrl":null,"url":null,"abstract":"<div><div>Soil salinization has rapidly become a critical global environmental issue in the current century. Understanding the structure of microbial networks and their interactions with biogeochemical cycles is vital to maintaining the stability of microbial communities and predicting ecosystem responses to salinization under climate change scenarios. Using metagenomic sequencing focuses on analyzing microbial community characteristics, as well as the function genes responsible for the cycles of carbon (C), nitrogen (N), phosphorus (P), and sulfur (S), in four distinct natural saline-alkali gradients: Non-saline, Low salinity, Medium salinity, and High salinity. The result revealed that salinity significantly alters the structures of bacterial, fungal, and archaeal communities and influences the functional genes related to the biogeochemical cycles. Notably, the increase of relative abundance in Proteobacteria (0.20, 0.30, 0.36, 0.38) with salinity, suggest its utility as a salinity indicator. Linear regression model revealed a significant negative correlation between salinity and the network complexity of prokaryotic, with higher network complexity does not favor the structural stability. In contrast, fungi network complexity positively correlated with salinity and stability. Additionally, while the complexity of prokaryotic networks significant negatively correlated with the metabolic potential of C, N, and S cycles, fungal showed a significantly positive correlation with P cycling. Random forest results identified salinity as the top driver of microbial network complexity (bacteria: 8.28 %; fungi: 7.22 %, archaea: 9.28 %). These insights suggest that the structural differences between prokaryotes and fungi result in varying responses to salinity, network structure, and elemental cycles. The interplay between simplified prokaryotic networks and more complex fungal networks could enhance microbial network stability and improve biogeochemical cycling. This study newly identifies the divergent responses of prokaryotic and fungal networks to salinity, challenging previous assumptions about uniform microbial responses. Therefore, maintaining the appropriate complexity of belowground communities is essential for the effective management of saline-alkali ecosystems and sustainable agricultural development.</div></div>","PeriodicalId":8099,"journal":{"name":"Applied Soil Ecology","volume":"213 ","pages":"Article 106245"},"PeriodicalIF":4.8000,"publicationDate":"2025-06-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied Soil Ecology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S092913932500383X","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"SOIL SCIENCE","Score":null,"Total":0}
引用次数: 0

Abstract

Soil salinization has rapidly become a critical global environmental issue in the current century. Understanding the structure of microbial networks and their interactions with biogeochemical cycles is vital to maintaining the stability of microbial communities and predicting ecosystem responses to salinization under climate change scenarios. Using metagenomic sequencing focuses on analyzing microbial community characteristics, as well as the function genes responsible for the cycles of carbon (C), nitrogen (N), phosphorus (P), and sulfur (S), in four distinct natural saline-alkali gradients: Non-saline, Low salinity, Medium salinity, and High salinity. The result revealed that salinity significantly alters the structures of bacterial, fungal, and archaeal communities and influences the functional genes related to the biogeochemical cycles. Notably, the increase of relative abundance in Proteobacteria (0.20, 0.30, 0.36, 0.38) with salinity, suggest its utility as a salinity indicator. Linear regression model revealed a significant negative correlation between salinity and the network complexity of prokaryotic, with higher network complexity does not favor the structural stability. In contrast, fungi network complexity positively correlated with salinity and stability. Additionally, while the complexity of prokaryotic networks significant negatively correlated with the metabolic potential of C, N, and S cycles, fungal showed a significantly positive correlation with P cycling. Random forest results identified salinity as the top driver of microbial network complexity (bacteria: 8.28 %; fungi: 7.22 %, archaea: 9.28 %). These insights suggest that the structural differences between prokaryotes and fungi result in varying responses to salinity, network structure, and elemental cycles. The interplay between simplified prokaryotic networks and more complex fungal networks could enhance microbial network stability and improve biogeochemical cycling. This study newly identifies the divergent responses of prokaryotic and fungal networks to salinity, challenging previous assumptions about uniform microbial responses. Therefore, maintaining the appropriate complexity of belowground communities is essential for the effective management of saline-alkali ecosystems and sustainable agricultural development.
通过简化原核生物和复杂真菌网络增强盐碱地微生物网络稳定性和生物地球化学循环
土壤盐碱化已迅速成为本世纪一个重要的全球性环境问题。了解微生物网络的结构及其与生物地球化学循环的相互作用对于维持气候变化情景下微生物群落的稳定性和预测生态系统对盐渍化的响应至关重要。利用宏基因组测序技术分析了在非盐、低盐、中盐和高盐四种不同天然盐碱梯度下微生物群落特征,以及负责碳(C)、氮(N)、磷(P)和硫(S)循环的功能基因。结果表明,盐度显著改变了细菌、真菌和古细菌群落的结构,并影响了与生物地球化学循环相关的功能基因。值得注意的是,变形菌门的相对丰度随盐度的增加而增加(0.20,0.30,0.36,0.38),这表明它可以作为盐度指标。线性回归模型显示,盐度与原核生物的网络复杂度呈显著负相关,网络复杂度越高,结构稳定性越差。相反,真菌网络复杂性与盐度和稳定性正相关。此外,原核生物网络的复杂性与C、N和S循环的代谢势呈显著负相关,而真菌与P循环的代谢势呈显著正相关。随机森林结果表明,盐度是微生物网络复杂性的首要驱动因素(细菌:8.28%;真菌:7.22%,古生菌:9.28%)。这些见解表明,原核生物和真菌之间的结构差异导致了对盐度、网络结构和元素循环的不同反应。简化的原核生物网络和更复杂的真菌网络之间的相互作用可以增强微生物网络的稳定性,促进生物地球化学循环。这项研究新发现了原核生物和真菌网络对盐度的不同反应,挑战了以前关于微生物反应统一的假设。因此,保持地下群落的适当复杂性对于盐碱生态系统的有效管理和农业的可持续发展至关重要。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Applied Soil Ecology
Applied Soil Ecology 农林科学-土壤科学
CiteScore
9.70
自引率
4.20%
发文量
363
审稿时长
5.3 months
期刊介绍: Applied Soil Ecology addresses the role of soil organisms and their interactions in relation to: sustainability and productivity, nutrient cycling and other soil processes, the maintenance of soil functions, the impact of human activities on soil ecosystems and bio(techno)logical control of soil-inhabiting pests, diseases and weeds.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信