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Regional biogeography versus intra-annual dynamics of the root and soil microbiome

BACKGROUND: Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host...

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Autores principales: Bell-Dereske, Lukas P., Benucci, Gian Maria Niccolò, da Costa, Pedro Beschoren, Bonito, Gregory, Friesen, Maren L., Tiemann, Lisa K., Evans, Sarah E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245661/
https://www.ncbi.nlm.nih.gov/pubmed/37287059
http://dx.doi.org/10.1186/s40793-023-00504-x
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author Bell-Dereske, Lukas P.
Benucci, Gian Maria Niccolò
da Costa, Pedro Beschoren
Bonito, Gregory
Friesen, Maren L.
Tiemann, Lisa K.
Evans, Sarah E.
author_facet Bell-Dereske, Lukas P.
Benucci, Gian Maria Niccolò
da Costa, Pedro Beschoren
Bonito, Gregory
Friesen, Maren L.
Tiemann, Lisa K.
Evans, Sarah E.
author_sort Bell-Dereske, Lukas P.
collection PubMed
description BACKGROUND: Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). RESULTS: To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. CONCLUSIONS: Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00504-x.
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spelling pubmed-102456612023-06-08 Regional biogeography versus intra-annual dynamics of the root and soil microbiome Bell-Dereske, Lukas P. Benucci, Gian Maria Niccolò da Costa, Pedro Beschoren Bonito, Gregory Friesen, Maren L. Tiemann, Lisa K. Evans, Sarah E. Environ Microbiome Research BACKGROUND: Root and soil microbial communities constitute the below-ground plant microbiome, are drivers of nutrient cycling, and affect plant productivity. However, our understanding of their spatiotemporal patterns is confounded by exogenous factors that covary spatially, such as changes in host plant species, climate, and edaphic factors. These spatiotemporal patterns likely differ across microbiome domains (bacteria and fungi) and niches (root vs. soil). RESULTS: To capture spatial patterns at a regional scale, we sampled the below-ground microbiome of switchgrass monocultures of five sites spanning > 3 degrees of latitude within the Great Lakes region. To capture temporal patterns, we sampled the below-ground microbiome across the growing season within a single site. We compared the strength of spatiotemporal factors to nitrogen addition determining the major drivers in our perennial cropping system. All microbial communities were most strongly structured by sampling site, though collection date also had strong effects; in contrast, nitrogen addition had little to no effect on communities. Though all microbial communities were found to have significant spatiotemporal patterns, sampling site and collection date better explained bacterial than fungal community structure, which appeared more defined by stochastic processes. Root communities, especially bacterial, were more temporally structured than soil communities which were more spatially structured, both across and within sampling sites. Finally, we characterized a core set of taxa in the switchgrass microbiome that persists across space and time. These core taxa represented < 6% of total species richness but > 27% of relative abundance, with potential nitrogen fixing bacteria and fungal mutualists dominating the root community and saprotrophs dominating the soil community. CONCLUSIONS: Our results highlight the dynamic variability of plant microbiome composition and assembly across space and time, even within a single variety of a plant species. Root and soil fungal community compositions appeared spatiotemporally paired, while root and soil bacterial communities showed a temporal lag in compositional similarity suggesting active recruitment of soil bacteria into the root niche throughout the growing season. A better understanding of the drivers of these differential responses to space and time may improve our ability to predict microbial community structure and function under novel conditions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00504-x. BioMed Central 2023-06-07 /pmc/articles/PMC10245661/ /pubmed/37287059 http://dx.doi.org/10.1186/s40793-023-00504-x 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
Bell-Dereske, Lukas P.
Benucci, Gian Maria Niccolò
da Costa, Pedro Beschoren
Bonito, Gregory
Friesen, Maren L.
Tiemann, Lisa K.
Evans, Sarah E.
Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title_full Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title_fullStr Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title_full_unstemmed Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title_short Regional biogeography versus intra-annual dynamics of the root and soil microbiome
title_sort regional biogeography versus intra-annual dynamics of the root and soil microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245661/
https://www.ncbi.nlm.nih.gov/pubmed/37287059
http://dx.doi.org/10.1186/s40793-023-00504-x
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