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Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity

BACKGROUND: Soil microbial communities are major drivers of cycling of soil nutrients that sustain plant growth and productivity. Yet, a holistic understanding of the impact of land-use intensification on the soil microbiome is still poorly understood. Here, we used a field experiment to investigate...

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Autores principales: Romdhane, Sana, Spor, Aymé, Banerjee, Samiran, Breuil, Marie-Christine, Bru, David, Chabbi, Abad, Hallin, Sara, van der Heijden, Marcel G. A., Saghai, Aurélien, Philippot, Laurent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740439/
https://www.ncbi.nlm.nih.gov/pubmed/34991714
http://dx.doi.org/10.1186/s40793-021-00396-9
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author Romdhane, Sana
Spor, Aymé
Banerjee, Samiran
Breuil, Marie-Christine
Bru, David
Chabbi, Abad
Hallin, Sara
van der Heijden, Marcel G. A.
Saghai, Aurélien
Philippot, Laurent
author_facet Romdhane, Sana
Spor, Aymé
Banerjee, Samiran
Breuil, Marie-Christine
Bru, David
Chabbi, Abad
Hallin, Sara
van der Heijden, Marcel G. A.
Saghai, Aurélien
Philippot, Laurent
author_sort Romdhane, Sana
collection PubMed
description BACKGROUND: Soil microbial communities are major drivers of cycling of soil nutrients that sustain plant growth and productivity. Yet, a holistic understanding of the impact of land-use intensification on the soil microbiome is still poorly understood. Here, we used a field experiment to investigate the long-term consequences of changes in land-use intensity based on cropping frequency (continuous cropping, alternating cropping with a temporary grassland, perennial grassland) on bacterial, protist and fungal communities as well as on their co-occurrence networks. RESULTS: We showed that land use has a major impact on the structure and composition of bacterial, protist and fungal communities. Grassland and arable cropping differed markedly with many taxa differentiating between both land use types. The smallest differences in the microbiome were observed between temporary grassland and continuous cropping, which suggests lasting effects of the cropping system preceding the temporary grasslands. Land-use intensity also affected the bacterial co-occurrence networks with increased complexity in the perennial grassland comparing to the other land-use systems. Similarly, co-occurrence networks within microbial groups showed a higher connectivity in the perennial grasslands. Protists, particularly Rhizaria, dominated in soil microbial associations, as they showed a higher number of connections than bacteria and fungi in all land uses. CONCLUSIONS: Our findings provide evidence of legacy effects of prior land use on the composition of the soil microbiome. Whatever the land use, network analyses highlighted the importance of protists as a key element of the soil microbiome that should be considered in future work. Altogether, this work provides a holistic perspective of the differential responses of various microbial groups and of their associations to agricultural intensification. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-021-00396-9.
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spelling pubmed-87404392022-01-10 Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity Romdhane, Sana Spor, Aymé Banerjee, Samiran Breuil, Marie-Christine Bru, David Chabbi, Abad Hallin, Sara van der Heijden, Marcel G. A. Saghai, Aurélien Philippot, Laurent Environ Microbiome Research Article BACKGROUND: Soil microbial communities are major drivers of cycling of soil nutrients that sustain plant growth and productivity. Yet, a holistic understanding of the impact of land-use intensification on the soil microbiome is still poorly understood. Here, we used a field experiment to investigate the long-term consequences of changes in land-use intensity based on cropping frequency (continuous cropping, alternating cropping with a temporary grassland, perennial grassland) on bacterial, protist and fungal communities as well as on their co-occurrence networks. RESULTS: We showed that land use has a major impact on the structure and composition of bacterial, protist and fungal communities. Grassland and arable cropping differed markedly with many taxa differentiating between both land use types. The smallest differences in the microbiome were observed between temporary grassland and continuous cropping, which suggests lasting effects of the cropping system preceding the temporary grasslands. Land-use intensity also affected the bacterial co-occurrence networks with increased complexity in the perennial grassland comparing to the other land-use systems. Similarly, co-occurrence networks within microbial groups showed a higher connectivity in the perennial grasslands. Protists, particularly Rhizaria, dominated in soil microbial associations, as they showed a higher number of connections than bacteria and fungi in all land uses. CONCLUSIONS: Our findings provide evidence of legacy effects of prior land use on the composition of the soil microbiome. Whatever the land use, network analyses highlighted the importance of protists as a key element of the soil microbiome that should be considered in future work. Altogether, this work provides a holistic perspective of the differential responses of various microbial groups and of their associations to agricultural intensification. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-021-00396-9. BioMed Central 2022-01-06 /pmc/articles/PMC8740439/ /pubmed/34991714 http://dx.doi.org/10.1186/s40793-021-00396-9 Text en © The Author(s) 2022 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 Article
Romdhane, Sana
Spor, Aymé
Banerjee, Samiran
Breuil, Marie-Christine
Bru, David
Chabbi, Abad
Hallin, Sara
van der Heijden, Marcel G. A.
Saghai, Aurélien
Philippot, Laurent
Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title_full Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title_fullStr Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title_full_unstemmed Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title_short Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
title_sort land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740439/
https://www.ncbi.nlm.nih.gov/pubmed/34991714
http://dx.doi.org/10.1186/s40793-021-00396-9
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