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Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop

BACKGROUND: Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues...

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Autores principales: Ceja-Navarro, Javier A., Wang, Yuan, Ning, Daliang, Arellano, Abelardo, Ramanculova, Leila, Yuan, Mengting Maggie, Byer, Alyssa, Craven, Kelly D., Saha, Malay C., Brodie, Eoin L., Pett-Ridge, Jennifer, Firestone, Mary K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082632/
https://www.ncbi.nlm.nih.gov/pubmed/33910643
http://dx.doi.org/10.1186/s40168-021-01042-9
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author Ceja-Navarro, Javier A.
Wang, Yuan
Ning, Daliang
Arellano, Abelardo
Ramanculova, Leila
Yuan, Mengting Maggie
Byer, Alyssa
Craven, Kelly D.
Saha, Malay C.
Brodie, Eoin L.
Pett-Ridge, Jennifer
Firestone, Mary K.
author_facet Ceja-Navarro, Javier A.
Wang, Yuan
Ning, Daliang
Arellano, Abelardo
Ramanculova, Leila
Yuan, Mengting Maggie
Byer, Alyssa
Craven, Kelly D.
Saha, Malay C.
Brodie, Eoin L.
Pett-Ridge, Jennifer
Firestone, Mary K.
author_sort Ceja-Navarro, Javier A.
collection PubMed
description BACKGROUND: Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues to grow, but there remains a need to understand the extent to which biological and environmental factors mediate protist community assembly and dynamics. We hypothesize that protists communities are filtered by the influence of plants on their rhizosphere biological and physicochemical environment, resulting in patterns of protist diversity and composition that mirror previously observed diversity and successional dynamics in rhizosphere bacterial communities. RESULTS: We analyzed protist communities associated with the rhizosphere and bulk soil of switchgrass (SG) plants (Panicum virgatum) at different phenological stages, grown in two marginal soils as part of a large-scale field experiment. Our results reveal that the diversity of protists is lower in rhizosphere than bulk soils, and that temporal variations depend on soil properties but are less pronounced in rhizosphere soil. Patterns of significantly prevalent protists groups in the rhizosphere suggest that most protists play varied ecological roles across plant growth stages and that some plant pathogenic protists and protists with omnivorous diets reoccur over time in the rhizosphere. We found that protist co-occurrence network dynamics are more complex in the rhizosphere compared to bulk soil. A phylogenetic bin-based null model analysis showed that protists’ community assembly in our study sites is mainly controlled by homogenous selection and dispersal limitation, with stronger selection in rhizosphere than bulk soil as SG grew and senesced. CONCLUSIONS: We demonstrate that environmental filtering is a dominant determinant of overall protist community properties and that at the rhizosphere level, plant control on the physical and biological environment is a critical driver of protist community composition and dynamics. Since protists are key contributors to plant nutrient availability and bacterial community composition and abundance, mapping and understanding their patterns in rhizosphere soil is foundational to understanding the ecology of the root-microbe-soil system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01042-9.
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spelling pubmed-80826322021-04-29 Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop Ceja-Navarro, Javier A. Wang, Yuan Ning, Daliang Arellano, Abelardo Ramanculova, Leila Yuan, Mengting Maggie Byer, Alyssa Craven, Kelly D. Saha, Malay C. Brodie, Eoin L. Pett-Ridge, Jennifer Firestone, Mary K. Microbiome Research BACKGROUND: Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues to grow, but there remains a need to understand the extent to which biological and environmental factors mediate protist community assembly and dynamics. We hypothesize that protists communities are filtered by the influence of plants on their rhizosphere biological and physicochemical environment, resulting in patterns of protist diversity and composition that mirror previously observed diversity and successional dynamics in rhizosphere bacterial communities. RESULTS: We analyzed protist communities associated with the rhizosphere and bulk soil of switchgrass (SG) plants (Panicum virgatum) at different phenological stages, grown in two marginal soils as part of a large-scale field experiment. Our results reveal that the diversity of protists is lower in rhizosphere than bulk soils, and that temporal variations depend on soil properties but are less pronounced in rhizosphere soil. Patterns of significantly prevalent protists groups in the rhizosphere suggest that most protists play varied ecological roles across plant growth stages and that some plant pathogenic protists and protists with omnivorous diets reoccur over time in the rhizosphere. We found that protist co-occurrence network dynamics are more complex in the rhizosphere compared to bulk soil. A phylogenetic bin-based null model analysis showed that protists’ community assembly in our study sites is mainly controlled by homogenous selection and dispersal limitation, with stronger selection in rhizosphere than bulk soil as SG grew and senesced. CONCLUSIONS: We demonstrate that environmental filtering is a dominant determinant of overall protist community properties and that at the rhizosphere level, plant control on the physical and biological environment is a critical driver of protist community composition and dynamics. Since protists are key contributors to plant nutrient availability and bacterial community composition and abundance, mapping and understanding their patterns in rhizosphere soil is foundational to understanding the ecology of the root-microbe-soil system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01042-9. BioMed Central 2021-04-28 /pmc/articles/PMC8082632/ /pubmed/33910643 http://dx.doi.org/10.1186/s40168-021-01042-9 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
Ceja-Navarro, Javier A.
Wang, Yuan
Ning, Daliang
Arellano, Abelardo
Ramanculova, Leila
Yuan, Mengting Maggie
Byer, Alyssa
Craven, Kelly D.
Saha, Malay C.
Brodie, Eoin L.
Pett-Ridge, Jennifer
Firestone, Mary K.
Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title_full Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title_fullStr Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title_full_unstemmed Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title_short Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
title_sort protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082632/
https://www.ncbi.nlm.nih.gov/pubmed/33910643
http://dx.doi.org/10.1186/s40168-021-01042-9
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