Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link

The relationship between biodiversity and ecosystem functioning (BEF) is a central issue in soil and microbial ecology. To date, most belowground BEF studies focus on the diversity of microbes analyzed by barcoding on total DNA, which targets both active and inactive microbes. This approach creates...

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Main Authors: Sara Fareed Mohamed Wahdan, Anna Heintz-Buschart, Chakriya Sansupa, Benjawan Tanunchai, Yu-Ting Wu, Martin Schädler, Matthias Noll, Witoon Purahong, François Buscot
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.629169/full
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spelling doaj-06ecc39add274e7aaa0a213c31dfc0672021-02-01T04:53:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-02-011210.3389/fmicb.2021.629169629169Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning LinkSara Fareed Mohamed Wahdan0Sara Fareed Mohamed Wahdan1Sara Fareed Mohamed Wahdan2Anna Heintz-Buschart3Anna Heintz-Buschart4Chakriya Sansupa5Benjawan Tanunchai6Yu-Ting Wu7Martin Schädler8Martin Schädler9Matthias Noll10Witoon Purahong11François Buscot12François Buscot13Department of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyDepartment of Biology, Leipzig University, Leipzig, GermanyDepartment of Botany, Faculty of Science, Suez Canal University, Ismailia, EgyptDepartment of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyDepartment of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyDepartment of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyDepartment of Forestry, National Pingtung University of Science and Technology, Pingtung, TaiwanGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyDepartment of Community Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyInstitute for Bioanalysis, Coburg University of Applied Sciences and Arts, Coburg, GermanyDepartment of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyDepartment of Soil Ecology, Helmholtz Centre for Environmental Research-UFZ, Halle (Saale), GermanyGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, GermanyThe relationship between biodiversity and ecosystem functioning (BEF) is a central issue in soil and microbial ecology. To date, most belowground BEF studies focus on the diversity of microbes analyzed by barcoding on total DNA, which targets both active and inactive microbes. This approach creates a bias as it mixes the part of the microbiome currently steering processes that provide actual ecosystem functions with the part not directly involved. Using experimental extensive grasslands under current and future climate, we used the bromodeoxyuridine (BrdU) immunocapture technique combined with pair-end Illumina sequencing to characterize both total and active microbiomes (including both bacteria and fungi) in the rhizosphere of Trifolium pratense. Rhizosphere function was assessed by measuring the activity of three microbial extracellular enzymes (β-glucosidase, N-acetyl-glucosaminidase, and acid phosphatase), which play central roles in the C, N, and P acquisition. We showed that the richness of overall and specific functional groups of active microbes in rhizosphere soil significantly correlated with the measured enzyme activities, while total microbial richness did not. Active microbes of the rhizosphere represented 42.8 and 32.1% of the total bacterial and fungal taxa, respectively, and were taxonomically and functionally diverse. Nitrogen fixing bacteria were highly active in this system with 71% of the total operational taxonomic units (OTUs) assigned to this group detected as active. We found the total and active microbiomes to display different responses to variations in soil physicochemical factors in the grassland, but with some degree of resistance to a manipulation mimicking future climate. Our findings provide critical insights into the role of active microbes in defining soil ecosystem functions in a grassland ecosystem. We demonstrate that the relationship between biodiversity-ecosystem functioning in soil may be stronger than previously thought.https://www.frontiersin.org/articles/10.3389/fmicb.2021.629169/fullactive microbiomerhizospherebiodiversity-ecosystem functioningGCEFBrdU
collection DOAJ
language English
format Article
sources DOAJ
author Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Anna Heintz-Buschart
Anna Heintz-Buschart
Chakriya Sansupa
Benjawan Tanunchai
Yu-Ting Wu
Martin Schädler
Martin Schädler
Matthias Noll
Witoon Purahong
François Buscot
François Buscot
spellingShingle Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Anna Heintz-Buschart
Anna Heintz-Buschart
Chakriya Sansupa
Benjawan Tanunchai
Yu-Ting Wu
Martin Schädler
Martin Schädler
Matthias Noll
Witoon Purahong
François Buscot
François Buscot
Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
Frontiers in Microbiology
active microbiome
rhizosphere
biodiversity-ecosystem functioning
GCEF
BrdU
author_facet Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Sara Fareed Mohamed Wahdan
Anna Heintz-Buschart
Anna Heintz-Buschart
Chakriya Sansupa
Benjawan Tanunchai
Yu-Ting Wu
Martin Schädler
Martin Schädler
Matthias Noll
Witoon Purahong
François Buscot
François Buscot
author_sort Sara Fareed Mohamed Wahdan
title Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
title_short Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
title_full Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
title_fullStr Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
title_full_unstemmed Targeting the Active Rhizosphere Microbiome of Trifolium pratense in Grassland Evidences a Stronger-Than-Expected Belowground Biodiversity-Ecosystem Functioning Link
title_sort targeting the active rhizosphere microbiome of trifolium pratense in grassland evidences a stronger-than-expected belowground biodiversity-ecosystem functioning link
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-02-01
description The relationship between biodiversity and ecosystem functioning (BEF) is a central issue in soil and microbial ecology. To date, most belowground BEF studies focus on the diversity of microbes analyzed by barcoding on total DNA, which targets both active and inactive microbes. This approach creates a bias as it mixes the part of the microbiome currently steering processes that provide actual ecosystem functions with the part not directly involved. Using experimental extensive grasslands under current and future climate, we used the bromodeoxyuridine (BrdU) immunocapture technique combined with pair-end Illumina sequencing to characterize both total and active microbiomes (including both bacteria and fungi) in the rhizosphere of Trifolium pratense. Rhizosphere function was assessed by measuring the activity of three microbial extracellular enzymes (β-glucosidase, N-acetyl-glucosaminidase, and acid phosphatase), which play central roles in the C, N, and P acquisition. We showed that the richness of overall and specific functional groups of active microbes in rhizosphere soil significantly correlated with the measured enzyme activities, while total microbial richness did not. Active microbes of the rhizosphere represented 42.8 and 32.1% of the total bacterial and fungal taxa, respectively, and were taxonomically and functionally diverse. Nitrogen fixing bacteria were highly active in this system with 71% of the total operational taxonomic units (OTUs) assigned to this group detected as active. We found the total and active microbiomes to display different responses to variations in soil physicochemical factors in the grassland, but with some degree of resistance to a manipulation mimicking future climate. Our findings provide critical insights into the role of active microbes in defining soil ecosystem functions in a grassland ecosystem. We demonstrate that the relationship between biodiversity-ecosystem functioning in soil may be stronger than previously thought.
topic active microbiome
rhizosphere
biodiversity-ecosystem functioning
GCEF
BrdU
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.629169/full
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