Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient

ABSTRACTMicroorganisms regulate numerous ecosystem functions and show considerable differences along a latitudinal gradient. Although studies have revealed the latitudinal patterns of microbial community structure and single ecosystem function, the latitudinal patterns of ecosystem multifunctionalit...

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Main Authors: Miaomiao Cai, Caifang Zhang, Caroline Njambi Ndungu, Guihua Liu, Wenzhi Liu, Quanfa Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.00147-24
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author Miaomiao Cai
Caifang Zhang
Caroline Njambi Ndungu
Guihua Liu
Wenzhi Liu
Quanfa Zhang
author_facet Miaomiao Cai
Caifang Zhang
Caroline Njambi Ndungu
Guihua Liu
Wenzhi Liu
Quanfa Zhang
author_sort Miaomiao Cai
collection DOAJ
description ABSTRACTMicroorganisms regulate numerous ecosystem functions and show considerable differences along a latitudinal gradient. Although studies have revealed the latitudinal patterns of microbial community structure and single ecosystem function, the latitudinal patterns of ecosystem multifunctionality (EMF) and how microbial communities affect EMF along a latitudinal gradient remain unclear. Here, we collected channel sediments, riparian rhizosphere soils, and riparian bulk soils from 30 rivers across China and calculated EMF using 18 variables related to nitrogen cycling, nutrient pool, plant productivity, and water quality. We also determined microbial diversity (taxonomic and functional) and microbial network complexity using metagenomic sequencing. The results showed that EMF significantly decreased with increasing latitude in riparian rhizosphere and bulk soils but not in channel sediments. Microbial taxonomic and functional richness (observed species) in channel sediments were significantly higher in the low-latitude group than in the high-latitude group. However, microbial co-occurrence networks were more complex in the high-latitude group compared with the low-latitude group. Abiotic factors, primarily geographic and climatic factors, contributed more to EMF than microbial diversity and network complexity parameters in which only betweenness centralization had a significant relationship with EMF. Together, this study provides insight into the latitudinal pattern of EMF in rivers and highlights the importance of large-scale factors in explaining such latitudinal patterns.IMPORTANCEEcosystem multifunctionality (EMF) is the capacity of an ecosystem to provide multiple functions simultaneously. Microorganisms, as dominant drivers of belowground processes, have a profound effect on ecosystem functions. Although studies have revealed the latitudinal patterns of microbial community structure and single ecosystem function, the latitudinal patterns of EMF and how microbial communities affect EMF along a latitudinal gradient remain unclear. We collected channel sediments, riparian rhizosphere soils, and riparian bulk soils from 30 rivers along a latitudinal gradient across China and calculated EMF using 18 variables related to nitrogen cycling, nutrient pool, plant productivity, and water quality. This study fills a critical knowledge gap regarding the latitudinal patterns and drivers of EMF in river ecosystems and gives new insights into how microbial diversity and network complexity affect EMF from a metagenomic perspective.
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spelling doaj.art-e7cb0509fca644f7801e99283d107d882024-04-16T13:00:56ZengAmerican Society for MicrobiologymSystems2379-50772024-04-019410.1128/msystems.00147-24Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradientMiaomiao Cai0Caifang Zhang1Caroline Njambi Ndungu2Guihua Liu3Wenzhi Liu4Quanfa Zhang5CAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaCAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, ChinaABSTRACTMicroorganisms regulate numerous ecosystem functions and show considerable differences along a latitudinal gradient. Although studies have revealed the latitudinal patterns of microbial community structure and single ecosystem function, the latitudinal patterns of ecosystem multifunctionality (EMF) and how microbial communities affect EMF along a latitudinal gradient remain unclear. Here, we collected channel sediments, riparian rhizosphere soils, and riparian bulk soils from 30 rivers across China and calculated EMF using 18 variables related to nitrogen cycling, nutrient pool, plant productivity, and water quality. We also determined microbial diversity (taxonomic and functional) and microbial network complexity using metagenomic sequencing. The results showed that EMF significantly decreased with increasing latitude in riparian rhizosphere and bulk soils but not in channel sediments. Microbial taxonomic and functional richness (observed species) in channel sediments were significantly higher in the low-latitude group than in the high-latitude group. However, microbial co-occurrence networks were more complex in the high-latitude group compared with the low-latitude group. Abiotic factors, primarily geographic and climatic factors, contributed more to EMF than microbial diversity and network complexity parameters in which only betweenness centralization had a significant relationship with EMF. Together, this study provides insight into the latitudinal pattern of EMF in rivers and highlights the importance of large-scale factors in explaining such latitudinal patterns.IMPORTANCEEcosystem multifunctionality (EMF) is the capacity of an ecosystem to provide multiple functions simultaneously. Microorganisms, as dominant drivers of belowground processes, have a profound effect on ecosystem functions. Although studies have revealed the latitudinal patterns of microbial community structure and single ecosystem function, the latitudinal patterns of EMF and how microbial communities affect EMF along a latitudinal gradient remain unclear. We collected channel sediments, riparian rhizosphere soils, and riparian bulk soils from 30 rivers along a latitudinal gradient across China and calculated EMF using 18 variables related to nitrogen cycling, nutrient pool, plant productivity, and water quality. This study fills a critical knowledge gap regarding the latitudinal patterns and drivers of EMF in river ecosystems and gives new insights into how microbial diversity and network complexity affect EMF from a metagenomic perspective.https://journals.asm.org/doi/10.1128/msystems.00147-24ecosystem functioningfunctional diversitylatitudinal patternnetwork complexitynitrogen cycling
spellingShingle Miaomiao Cai
Caifang Zhang
Caroline Njambi Ndungu
Guihua Liu
Wenzhi Liu
Quanfa Zhang
Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
mSystems
ecosystem functioning
functional diversity
latitudinal pattern
network complexity
nitrogen cycling
title Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
title_full Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
title_fullStr Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
title_full_unstemmed Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
title_short Linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
title_sort linking ecosystem multifunctionality to microbial community features in rivers along a latitudinal gradient
topic ecosystem functioning
functional diversity
latitudinal pattern
network complexity
nitrogen cycling
url https://journals.asm.org/doi/10.1128/msystems.00147-24
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AT carolinenjambindungu linkingecosystemmultifunctionalitytomicrobialcommunityfeaturesinriversalongalatitudinalgradient
AT guihualiu linkingecosystemmultifunctionalitytomicrobialcommunityfeaturesinriversalongalatitudinalgradient
AT wenzhiliu linkingecosystemmultifunctionalitytomicrobialcommunityfeaturesinriversalongalatitudinalgradient
AT quanfazhang linkingecosystemmultifunctionalitytomicrobialcommunityfeaturesinriversalongalatitudinalgradient