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Leveraging microbiome rediversification for the ecological rescue of soil function

BACKGROUND: Global biodiversity losses threaten ecosystem services and can impact important functional insurance in a changing world. Microbial diversity and function can become depleted in agricultural systems and attempts to rediversify agricultural soils rely on either targeted microbial introduc...

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Autores principales: King, William L., Richards, Sarah C., Kaminsky, Laura M., Bradley, Brosi A., Kaye, Jason P., Bell, Terrence H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9872425/
https://www.ncbi.nlm.nih.gov/pubmed/36691096
http://dx.doi.org/10.1186/s40793-023-00462-4
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author King, William L.
Richards, Sarah C.
Kaminsky, Laura M.
Bradley, Brosi A.
Kaye, Jason P.
Bell, Terrence H.
author_facet King, William L.
Richards, Sarah C.
Kaminsky, Laura M.
Bradley, Brosi A.
Kaye, Jason P.
Bell, Terrence H.
author_sort King, William L.
collection PubMed
description BACKGROUND: Global biodiversity losses threaten ecosystem services and can impact important functional insurance in a changing world. Microbial diversity and function can become depleted in agricultural systems and attempts to rediversify agricultural soils rely on either targeted microbial introductions or retaining natural lands as biodiversity reservoirs. As many soil functions are provided by a combination of microbial taxa, rather than outsized impacts by single taxa, such functions may benefit more from diverse microbiome additions than additions of individual commercial strains. In this study, we measured the impact of soil microbial diversity loss and rediversification (i.e. rescue) on nitrification by quantifying ammonium and nitrate pools. We manipulated microbial assemblages in two distinct soil types, an agricultural and a forest soil, with a dilution-to-extinction approach and performed a microbiome rediversification experiment by re-introducing microorganisms lost from the dilution. A microbiome water control was included to act as a reference point. We assessed disruption and potential restoration of (1) nitrification, (2) bacterial and fungal composition through 16S rRNA gene and fungal ITS amplicon sequencing and (3) functional genes through shotgun metagenomic sequencing on a subset of samples. RESULTS: Disruption of nitrification corresponded with diversity loss, but nitrification was successfully rescued in the rediversification experiment when high diversity inocula were introduced. Bacterial composition clustered into groups based on high and low diversity inocula. Metagenomic data showed that genes responsible for the conversion of nitrite to nitrate and taxa associated with nitrogen metabolism were absent in the low diversity inocula microcosms but were rescued with high diversity introductions. CONCLUSIONS: In contrast to some previous work, our data suggest that soil functions can be rescued by diverse microbiome additions, but that the concentration of the microbial inoculum is important. By understanding how microbial rediversification impacts soil microbiome performance, we can further our toolkit for microbial management in human-controlled systems in order to restore depleted microbial functions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00462-4.
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spelling pubmed-98724252023-01-25 Leveraging microbiome rediversification for the ecological rescue of soil function King, William L. Richards, Sarah C. Kaminsky, Laura M. Bradley, Brosi A. Kaye, Jason P. Bell, Terrence H. Environ Microbiome Research BACKGROUND: Global biodiversity losses threaten ecosystem services and can impact important functional insurance in a changing world. Microbial diversity and function can become depleted in agricultural systems and attempts to rediversify agricultural soils rely on either targeted microbial introductions or retaining natural lands as biodiversity reservoirs. As many soil functions are provided by a combination of microbial taxa, rather than outsized impacts by single taxa, such functions may benefit more from diverse microbiome additions than additions of individual commercial strains. In this study, we measured the impact of soil microbial diversity loss and rediversification (i.e. rescue) on nitrification by quantifying ammonium and nitrate pools. We manipulated microbial assemblages in two distinct soil types, an agricultural and a forest soil, with a dilution-to-extinction approach and performed a microbiome rediversification experiment by re-introducing microorganisms lost from the dilution. A microbiome water control was included to act as a reference point. We assessed disruption and potential restoration of (1) nitrification, (2) bacterial and fungal composition through 16S rRNA gene and fungal ITS amplicon sequencing and (3) functional genes through shotgun metagenomic sequencing on a subset of samples. RESULTS: Disruption of nitrification corresponded with diversity loss, but nitrification was successfully rescued in the rediversification experiment when high diversity inocula were introduced. Bacterial composition clustered into groups based on high and low diversity inocula. Metagenomic data showed that genes responsible for the conversion of nitrite to nitrate and taxa associated with nitrogen metabolism were absent in the low diversity inocula microcosms but were rescued with high diversity introductions. CONCLUSIONS: In contrast to some previous work, our data suggest that soil functions can be rescued by diverse microbiome additions, but that the concentration of the microbial inoculum is important. By understanding how microbial rediversification impacts soil microbiome performance, we can further our toolkit for microbial management in human-controlled systems in order to restore depleted microbial functions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-023-00462-4. BioMed Central 2023-01-23 /pmc/articles/PMC9872425/ /pubmed/36691096 http://dx.doi.org/10.1186/s40793-023-00462-4 Text en © The Author(s) 2023 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
King, William L.
Richards, Sarah C.
Kaminsky, Laura M.
Bradley, Brosi A.
Kaye, Jason P.
Bell, Terrence H.
Leveraging microbiome rediversification for the ecological rescue of soil function
title Leveraging microbiome rediversification for the ecological rescue of soil function
title_full Leveraging microbiome rediversification for the ecological rescue of soil function
title_fullStr Leveraging microbiome rediversification for the ecological rescue of soil function
title_full_unstemmed Leveraging microbiome rediversification for the ecological rescue of soil function
title_short Leveraging microbiome rediversification for the ecological rescue of soil function
title_sort leveraging microbiome rediversification for the ecological rescue of soil function
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9872425/
https://www.ncbi.nlm.nih.gov/pubmed/36691096
http://dx.doi.org/10.1186/s40793-023-00462-4
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