The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland

The decoupling of microbial functional and taxonomic components refers to the phenomenon that a drastic change in microbial taxonomic composition leads to no or only a gentle change in functional composition. Although many studies have identified this phenomenon, the mechanisms underlying it are sti...

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Main Authors: Huaiqiang Liu, Frank Yonghong Li, Jiayue Liu, Chunjun Shi, Kuanyan Tang, Qianhui Yang, Yu Liu, Qiang Fu, Xiaotian Gao, Ning Wang, Wei Guo
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1113157/full
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author Huaiqiang Liu
Frank Yonghong Li
Frank Yonghong Li
Jiayue Liu
Chunjun Shi
Kuanyan Tang
Qianhui Yang
Yu Liu
Qiang Fu
Xiaotian Gao
Ning Wang
Wei Guo
author_facet Huaiqiang Liu
Frank Yonghong Li
Frank Yonghong Li
Jiayue Liu
Chunjun Shi
Kuanyan Tang
Qianhui Yang
Yu Liu
Qiang Fu
Xiaotian Gao
Ning Wang
Wei Guo
author_sort Huaiqiang Liu
collection DOAJ
description The decoupling of microbial functional and taxonomic components refers to the phenomenon that a drastic change in microbial taxonomic composition leads to no or only a gentle change in functional composition. Although many studies have identified this phenomenon, the mechanisms underlying it are still unclear. Here we demonstrate, using metagenomics data from a steppe grassland soil under different grazing and phosphorus addition treatments, that there is no “decoupling” in the variation of taxonomic and metabolic functional composition of the microbial community within functional groups at species level. In contrast, the high consistency and complementarity between the abundance and functional gene diversity of two dominant species made metabolic functions unaffected by grazing and phosphorus addition. This complementarity between the two dominant species shapes a bistability pattern that differs from functional redundancy in that only two species cannot form observable redundancy in a large microbial community. In other words, the “monopoly” of metabolic functions by the two most abundant species leads to the disappearance of functional redundancy. Our findings imply that for soil microbial communities, the impact of species identity on metabolic functions is much greater than that of species diversity, and it is more important to monitor the dynamics of key dominant microorganisms for accurately predicting the changes in the metabolic functions of the ecosystems.
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spelling doaj.art-ed569249f16a44acb5cdfa24d67284992023-03-16T05:04:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.11131571113157The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grasslandHuaiqiang Liu0Frank Yonghong Li1Frank Yonghong Li2Jiayue Liu3Chunjun Shi4Kuanyan Tang5Qianhui Yang6Yu Liu7Qiang Fu8Xiaotian Gao9Ning Wang10Wei Guo11Ministry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaCollaborative Innovation Center for Grassland Ecological Security, Ministry of Education of China, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaMinistry of Education Key Laboratory of Ecology and Resource Use on the Mongolian Plateau and Inner Mongolia Key Laboratory of Grassland Ecology, School of Ecology and Environment, Inner Mongolia University, Hohhot, ChinaThe decoupling of microbial functional and taxonomic components refers to the phenomenon that a drastic change in microbial taxonomic composition leads to no or only a gentle change in functional composition. Although many studies have identified this phenomenon, the mechanisms underlying it are still unclear. Here we demonstrate, using metagenomics data from a steppe grassland soil under different grazing and phosphorus addition treatments, that there is no “decoupling” in the variation of taxonomic and metabolic functional composition of the microbial community within functional groups at species level. In contrast, the high consistency and complementarity between the abundance and functional gene diversity of two dominant species made metabolic functions unaffected by grazing and phosphorus addition. This complementarity between the two dominant species shapes a bistability pattern that differs from functional redundancy in that only two species cannot form observable redundancy in a large microbial community. In other words, the “monopoly” of metabolic functions by the two most abundant species leads to the disappearance of functional redundancy. Our findings imply that for soil microbial communities, the impact of species identity on metabolic functions is much greater than that of species diversity, and it is more important to monitor the dynamics of key dominant microorganisms for accurately predicting the changes in the metabolic functions of the ecosystems.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1113157/fullgrazingphosphorus additionfunctional redundancybistabilitybroad/specialized metabolic functionsgrassland
spellingShingle Huaiqiang Liu
Frank Yonghong Li
Frank Yonghong Li
Jiayue Liu
Chunjun Shi
Kuanyan Tang
Qianhui Yang
Yu Liu
Qiang Fu
Xiaotian Gao
Ning Wang
Wei Guo
The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
Frontiers in Microbiology
grazing
phosphorus addition
functional redundancy
bistability
broad/specialized metabolic functions
grassland
title The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
title_full The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
title_fullStr The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
title_full_unstemmed The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
title_short The reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
title_sort reciprocal changes in dominant species with complete metabolic functions explain the decoupling phenomenon of microbial taxonomic and functional composition in a grassland
topic grazing
phosphorus addition
functional redundancy
bistability
broad/specialized metabolic functions
grassland
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1113157/full
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