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A symbiotic footprint in the plant root microbiome

BACKGROUND: A major aim in plant microbiome research is determining the drivers of plant-associated microbial communities. While soil characteristics and host plant identity present key drivers of root microbiome composition, it is still unresolved whether the presence or absence of important plant...

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Autores principales: Hartman, Kyle, Schmid, Marc W., Bodenhausen, Natacha, Bender, S. Franz, Valzano-Held, Alain Y., Schlaeppi, Klaus, van der Heijden, Marcel G.A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10391997/
https://www.ncbi.nlm.nih.gov/pubmed/37525294
http://dx.doi.org/10.1186/s40793-023-00521-w
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author Hartman, Kyle
Schmid, Marc W.
Bodenhausen, Natacha
Bender, S. Franz
Valzano-Held, Alain Y.
Schlaeppi, Klaus
van der Heijden, Marcel G.A.
author_facet Hartman, Kyle
Schmid, Marc W.
Bodenhausen, Natacha
Bender, S. Franz
Valzano-Held, Alain Y.
Schlaeppi, Klaus
van der Heijden, Marcel G.A.
author_sort Hartman, Kyle
collection PubMed
description BACKGROUND: A major aim in plant microbiome research is determining the drivers of plant-associated microbial communities. While soil characteristics and host plant identity present key drivers of root microbiome composition, it is still unresolved whether the presence or absence of important plant root symbionts also determines overall microbiome composition. Arbuscular mycorrhizal fungi (AMF) and N-fixing rhizobia bacteria are widespread, beneficial root symbionts that significantly enhance plant nutrition, plant health, and root structure. Thus, we hypothesized that symbiont types define the root microbiome structure. RESULTS: We grew 17 plant species from five families differing in their symbiotic associations (no symbioses, AMF only, rhizobia only, or AMF and rhizobia) in a greenhouse and used bacterial and fungal amplicon sequencing to characterize their root microbiomes. Although plant phylogeny and species identity were the most important factors determining root microbiome composition, we discovered that the type of symbioses also presented a significant driver of diversity and community composition. We found consistent responses of bacterial phyla, including members of the Acidobacteria, Chlamydiae, Firmicutes, and Verrucomicrobia, to the presence or absence of AMF and rhizobia and identified communities of OTUs specifically enriched in the different symbiotic groups. A total of 80, 75 and 57 bacterial OTUs were specific for plant species without symbiosis, plant species forming associations with AMF or plant species associating with both AMF and rhizobia, respectively. Similarly, 9, 14 and 4 fungal OTUs were specific for these plant symbiont groups. Importantly, these generic symbiosis footprints in microbial community composition were also apparent in absence of the primary symbionts. CONCLUSION: Our results reveal that symbiotic associations of the host plant leaves an imprint on the wider root microbiome – which we term the symbiotype. These findings suggest the existence of a fundamental assembly principle of root microbiomes, dependent on the symbiotic associations of the host plant. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00521-w.
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spelling pubmed-103919972023-08-02 A symbiotic footprint in the plant root microbiome Hartman, Kyle Schmid, Marc W. Bodenhausen, Natacha Bender, S. Franz Valzano-Held, Alain Y. Schlaeppi, Klaus van der Heijden, Marcel G.A. Environ Microbiome Research BACKGROUND: A major aim in plant microbiome research is determining the drivers of plant-associated microbial communities. While soil characteristics and host plant identity present key drivers of root microbiome composition, it is still unresolved whether the presence or absence of important plant root symbionts also determines overall microbiome composition. Arbuscular mycorrhizal fungi (AMF) and N-fixing rhizobia bacteria are widespread, beneficial root symbionts that significantly enhance plant nutrition, plant health, and root structure. Thus, we hypothesized that symbiont types define the root microbiome structure. RESULTS: We grew 17 plant species from five families differing in their symbiotic associations (no symbioses, AMF only, rhizobia only, or AMF and rhizobia) in a greenhouse and used bacterial and fungal amplicon sequencing to characterize their root microbiomes. Although plant phylogeny and species identity were the most important factors determining root microbiome composition, we discovered that the type of symbioses also presented a significant driver of diversity and community composition. We found consistent responses of bacterial phyla, including members of the Acidobacteria, Chlamydiae, Firmicutes, and Verrucomicrobia, to the presence or absence of AMF and rhizobia and identified communities of OTUs specifically enriched in the different symbiotic groups. A total of 80, 75 and 57 bacterial OTUs were specific for plant species without symbiosis, plant species forming associations with AMF or plant species associating with both AMF and rhizobia, respectively. Similarly, 9, 14 and 4 fungal OTUs were specific for these plant symbiont groups. Importantly, these generic symbiosis footprints in microbial community composition were also apparent in absence of the primary symbionts. CONCLUSION: Our results reveal that symbiotic associations of the host plant leaves an imprint on the wider root microbiome – which we term the symbiotype. These findings suggest the existence of a fundamental assembly principle of root microbiomes, dependent on the symbiotic associations of the host plant. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00521-w. BioMed Central 2023-07-31 /pmc/articles/PMC10391997/ /pubmed/37525294 http://dx.doi.org/10.1186/s40793-023-00521-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Hartman, Kyle
Schmid, Marc W.
Bodenhausen, Natacha
Bender, S. Franz
Valzano-Held, Alain Y.
Schlaeppi, Klaus
van der Heijden, Marcel G.A.
A symbiotic footprint in the plant root microbiome
title A symbiotic footprint in the plant root microbiome
title_full A symbiotic footprint in the plant root microbiome
title_fullStr A symbiotic footprint in the plant root microbiome
title_full_unstemmed A symbiotic footprint in the plant root microbiome
title_short A symbiotic footprint in the plant root microbiome
title_sort symbiotic footprint in the plant root microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10391997/
https://www.ncbi.nlm.nih.gov/pubmed/37525294
http://dx.doi.org/10.1186/s40793-023-00521-w
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