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Leveraging microbiome rediversification for the ecological rescue of soil function

Leveraging microbiome rediversification for the ecological rescue of soil function
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 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.
Biodiversity, Community inoculum, Microbial establishment, Microbial function, Nitrification
2524-6372
King, William L.
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Richards, Sarah C.
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Kaminsky, Laura M.
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Bradley, Brosi A.
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Kaye, Jason P.
9a20833c-f457-41f8-9b57-1c9c9ca8d0fe
Bell, Terrence H.
29863b8c-a89c-4077-b22d-62052cfb7225
King, William L.
0bd4328a-34ba-4b9a-bf4e-1442c18c43fc
Richards, Sarah C.
ba7e0707-3e1c-43aa-a72e-0623abb12c18
Kaminsky, Laura M.
cdd71929-138a-4719-875f-972240a3f79e
Bradley, Brosi A.
58498666-542e-46d3-a68b-45c0133e1746
Kaye, Jason P.
9a20833c-f457-41f8-9b57-1c9c9ca8d0fe
Bell, Terrence H.
29863b8c-a89c-4077-b22d-62052cfb7225

King, William L., Richards, Sarah C., Kaminsky, Laura M., Bradley, Brosi A., Kaye, Jason P. and Bell, Terrence H. (2023) Leveraging microbiome rediversification for the ecological rescue of soil function. Environmental Microbiome, 18 (1), [7]. (doi:10.1186/s40793-023-00462-4).

Record type: Article

Abstract

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.

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s40793-023-00462-4 - Version of Record
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Accepted/In Press date: 6 January 2023
Published date: 23 January 2023
Additional Information: Funding Information: This work was supported by the USDA National Institute of Food and Agriculture (NIFA) under Project #PEN04651 (Accession no. 1016233), #PEN04710 (Accession no. 1020049), PEN04571 (Accession no. 1003346), the USDA Organic Transitions (ORG) Grant 2019-51106-30196, and a National Science Foundation Graduate Research Fellowship Program under Grant no. DGE1255832 to LM Kaminsky. Publisher Copyright: © 2023, The Author(s).
Keywords: Biodiversity, Community inoculum, Microbial establishment, Microbial function, Nitrification

Identifiers

Local EPrints ID: 486537
URI: http://eprints.soton.ac.uk/id/eprint/486537
ISSN: 2524-6372
PURE UUID: 3b2af8fb-680d-453b-acb5-6e02b3124ee5
ORCID for William L. King: ORCID iD orcid.org/0000-0001-7272-8242

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Date deposited: 25 Jan 2024 17:35
Last modified: 12 Jul 2024 02:17

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Contributors

Author: William L. King ORCID iD
Author: Sarah C. Richards
Author: Laura M. Kaminsky
Author: Brosi A. Bradley
Author: Jason P. Kaye
Author: Terrence H. Bell

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