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Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification

Cropping system diversity provides yield benefits that may result from shifts in the composition of root-associated bacterial and fungal communities, which either enhance nutrient availability or limit nutrient loss. We investigated whether temporal diversity of annual cropping systems (four versus...

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Autores principales: Bay, Guillaume, Lee, Conard, Chen, Chiliang, Mahal, Navreet K., Castellano, Michael J., Hofmockel, Kirsten S., Halverson, Larry J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8547420/
https://www.ncbi.nlm.nih.gov/pubmed/34581600
http://dx.doi.org/10.1128/mSystems.00651-21
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author Bay, Guillaume
Lee, Conard
Chen, Chiliang
Mahal, Navreet K.
Castellano, Michael J.
Hofmockel, Kirsten S.
Halverson, Larry J.
author_facet Bay, Guillaume
Lee, Conard
Chen, Chiliang
Mahal, Navreet K.
Castellano, Michael J.
Hofmockel, Kirsten S.
Halverson, Larry J.
author_sort Bay, Guillaume
collection PubMed
description Cropping system diversity provides yield benefits that may result from shifts in the composition of root-associated bacterial and fungal communities, which either enhance nutrient availability or limit nutrient loss. We investigated whether temporal diversity of annual cropping systems (four versus two crops in rotation) influences the composition and metabolic activities of root-associated microbial communities in maize at a developmental stage when the peak rate of nitrogen uptake occurs. We monitored total (DNA-based) and potentially active (RNA-based) bacterial communities and total (DNA-based) fungal communities in the soil, rhizosphere, and endosphere. Cropping system diversity strongly influenced the composition of the soil microbial communities, which influenced the recruitment of the resident microbial communities and, in particular, the potentially active rhizosphere and endosphere bacterial communities. The diversified cropping system rhizosphere recruited a more diverse bacterial community (species richness), even though there was little difference in soil species richness between the two cropping systems. In contrast, fungal species richness was greater in the conventional rhizosphere, which was enriched in fungal pathogens; the diversified rhizosphere, however, was enriched in Glomeromycetes. While cropping system influenced endosphere community composition, greater correspondence between DNA- and RNA-based profiles suggests a higher representation of active bacterial populations. Cropping system diversity influenced the composition of ammonia oxidizers, which coincided with diminished potential nitrification activity and gross nitrate production rates, particularly in the rhizosphere. The results of our study suggest that diversified cropping systems shift the composition of the rhizosphere’s active bacterial and total fungal communities, resulting in tighter coupling between plants and microbial processes that influence nitrogen acquisition and retention. IMPORTANCE Crops in simplified, low-diversity agroecosystems assimilate only a fraction of the inorganic nitrogen (N) fertilizer inputs. Much of this N fertilizer is lost to the environment as N oxides, which degrade water quality and contribute to climate change and loss of biodiversity. Ecologically inspired management may facilitate mutualistic interactions between plant roots and microbes to liberate nutrients when plants need them, while also decreasing nutrient loss and pathogen pressure. In this study, we investigate the effects of a conventional (2-year rotation, inorganic fertilization) and a diversified (4-year rotation, manure amendments) cropping system on the assembly of bacterial and fungal root-associated communities, at a maize developmental stage when nitrogen demand is beginning to increase. Our results indicate that agricultural management influences the recruitment of root-associated microbial communities and that diversified cropping systems have lower rates of nitrification (particularly in the rhizosphere), thereby reducing the potential for loss of nitrate from these systems.
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spelling pubmed-85474202021-10-27 Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification Bay, Guillaume Lee, Conard Chen, Chiliang Mahal, Navreet K. Castellano, Michael J. Hofmockel, Kirsten S. Halverson, Larry J. mSystems Research Article Cropping system diversity provides yield benefits that may result from shifts in the composition of root-associated bacterial and fungal communities, which either enhance nutrient availability or limit nutrient loss. We investigated whether temporal diversity of annual cropping systems (four versus two crops in rotation) influences the composition and metabolic activities of root-associated microbial communities in maize at a developmental stage when the peak rate of nitrogen uptake occurs. We monitored total (DNA-based) and potentially active (RNA-based) bacterial communities and total (DNA-based) fungal communities in the soil, rhizosphere, and endosphere. Cropping system diversity strongly influenced the composition of the soil microbial communities, which influenced the recruitment of the resident microbial communities and, in particular, the potentially active rhizosphere and endosphere bacterial communities. The diversified cropping system rhizosphere recruited a more diverse bacterial community (species richness), even though there was little difference in soil species richness between the two cropping systems. In contrast, fungal species richness was greater in the conventional rhizosphere, which was enriched in fungal pathogens; the diversified rhizosphere, however, was enriched in Glomeromycetes. While cropping system influenced endosphere community composition, greater correspondence between DNA- and RNA-based profiles suggests a higher representation of active bacterial populations. Cropping system diversity influenced the composition of ammonia oxidizers, which coincided with diminished potential nitrification activity and gross nitrate production rates, particularly in the rhizosphere. The results of our study suggest that diversified cropping systems shift the composition of the rhizosphere’s active bacterial and total fungal communities, resulting in tighter coupling between plants and microbial processes that influence nitrogen acquisition and retention. IMPORTANCE Crops in simplified, low-diversity agroecosystems assimilate only a fraction of the inorganic nitrogen (N) fertilizer inputs. Much of this N fertilizer is lost to the environment as N oxides, which degrade water quality and contribute to climate change and loss of biodiversity. Ecologically inspired management may facilitate mutualistic interactions between plant roots and microbes to liberate nutrients when plants need them, while also decreasing nutrient loss and pathogen pressure. In this study, we investigate the effects of a conventional (2-year rotation, inorganic fertilization) and a diversified (4-year rotation, manure amendments) cropping system on the assembly of bacterial and fungal root-associated communities, at a maize developmental stage when nitrogen demand is beginning to increase. Our results indicate that agricultural management influences the recruitment of root-associated microbial communities and that diversified cropping systems have lower rates of nitrification (particularly in the rhizosphere), thereby reducing the potential for loss of nitrate from these systems. American Society for Microbiology 2021-09-28 /pmc/articles/PMC8547420/ /pubmed/34581600 http://dx.doi.org/10.1128/mSystems.00651-21 Text en Copyright © 2021 Bay et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Bay, Guillaume
Lee, Conard
Chen, Chiliang
Mahal, Navreet K.
Castellano, Michael J.
Hofmockel, Kirsten S.
Halverson, Larry J.
Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title_full Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title_fullStr Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title_full_unstemmed Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title_short Agricultural Management Affects the Active Rhizosphere Bacterial Community Composition and Nitrification
title_sort agricultural management affects the active rhizosphere bacterial community composition and nitrification
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8547420/
https://www.ncbi.nlm.nih.gov/pubmed/34581600
http://dx.doi.org/10.1128/mSystems.00651-21
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