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

Panicum virgatum Plant microbiome Root bacteria Root fungi Soil bacteria Soil fungi

Journal

Environmental microbiome
ISSN: 2524-6372
Titre abrégé: Environ Microbiome
Pays: England
ID NLM: 101768168

Informations de publication

Date de publication:
07 Jun 2023
Historique:
received: 15 12 2022
accepted: 17 05 2023
medline: 8 6 2023
pubmed: 8 6 2023
entrez: 7 6 2023
Statut: epublish

Résumé

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). 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. 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.

Sections du résumé

BACKGROUND 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 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 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.

Identifiants

pubmed: 37287059
doi: 10.1186/s40793-023-00504-x
pii: 10.1186/s40793-023-00504-x
pmc: PMC10245661
doi:

Types de publication

Journal Article

Langues

eng

Pagination

50

Subventions

Organisme : U.S. Department of Energy
ID : DE-SC0014108
Organisme : U.S. Department of Energy
ID : DE-SC0018409
Organisme : U.S. Department of Energy
ID : DE-SC0018409
Organisme : U.S. Department of Energy
ID : DE-SC0018409
Organisme : U.S. Department of Energy
ID : DE-SC0014108
Organisme : U.S. Department of Energy
ID : DE-SC0014108
Organisme : U.S. Department of Energy
ID : DE-SC0014108
Organisme : U.S. National Science Foundation
ID : DEB 1832042
Organisme : U.S. National Science Foundation
ID : DEB 1832042

Informations de copyright

© 2023. The Author(s).

Références

Science. 2019 Oct 25;366(6464):480-485
pubmed: 31649197
Proc Natl Acad Sci U S A. 2014 Apr 29;111(17):6341-6
pubmed: 24733885
PLoS One. 2018 Jun 1;13(6):e0197320
pubmed: 29856843
Sci Rep. 2014 May 30;4:5135
pubmed: 24875794
mBio. 2020 Jan 21;11(1):
pubmed: 31964728
PLoS Comput Biol. 2017 Feb 21;13(2):e1005404
pubmed: 28222096
FEMS Microbiol Ecol. 2019 Feb 1;95(2):
pubmed: 30629168
Sci Total Environ. 2021 Nov 10;794:148644
pubmed: 34192632
Appl Environ Microbiol. 2013 Sep;79(17):5112-20
pubmed: 23793624
Nature. 2013 Jan 24;493(7433):514-7
pubmed: 23334409
Front Microbiol. 2020 Jun 03;11:1116
pubmed: 32582080
Ecology. 2009 Sep;90(9):2352-9
pubmed: 19769113
Glob Chang Biol. 2018 Aug;24(8):3452-3461
pubmed: 29645398
Nucleic Acids Res. 2014 Jan;42(Database issue):D643-8
pubmed: 24293649
Sci Rep. 2018 Mar 12;8(1):4382
pubmed: 29531240
ISME J. 2020 Jul;14(7):1886-1896
pubmed: 32341471
PLoS One. 2014 Jun 27;9(6):e101238
pubmed: 24971901
Bioinformatics. 2015 Aug 1;31(15):2461-8
pubmed: 25819674
Proc Natl Acad Sci U S A. 2006 Jan 17;103(3):626-31
pubmed: 16407148
Ecol Lett. 2021 Dec;24(12):2726-2738
pubmed: 34595822
Nat Methods. 2013 Oct;10(10):996-8
pubmed: 23955772
Nat Commun. 2019 Nov 13;10(1):5142
pubmed: 31723140
Mol Ecol. 2021 Sep;30(17):4305-4320
pubmed: 34160856
ISME J. 2018 Jun;12(7):1817-1825
pubmed: 29588494
Curr Opin Microbiol. 2019 Jun;49:50-58
pubmed: 31715441
Bioinformatics. 2012 Jan 1;28(1):112-8
pubmed: 22039212
Mol Ecol. 2014 Feb;23(2):254-8
pubmed: 26010467
FEMS Microbiol Ecol. 2020 Nov 27;96(12):
pubmed: 33038234
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Mol Ecol. 2014 Feb;23(2):481-97
pubmed: 24112459
Soil Biol Biochem. 2013 May;60(100):95-104
pubmed: 23645937
Glob Chang Biol. 2022 Nov;28(22):6696-6710
pubmed: 36056462
Genome Biol. 2011;12(5):R50
pubmed: 21624126
Science. 2017 Jun 30;356(6345):
pubmed: 28663443
PLoS Biol. 2022 Aug 11;20(8):e3001681
pubmed: 35951523
mBio. 2022 Apr 26;13(2):e0007922
pubmed: 35384699
ISME J. 2012 May;6(5):1007-17
pubmed: 22134642
Nature. 2018 Aug;560(7717):233-237
pubmed: 30069051
New Phytol. 2014 Jan;201(1):269-278
pubmed: 24010995
ISME J. 2016 Mar;10(3):655-64
pubmed: 26296066
Mol Ecol. 2019 Apr;28(7):1842-1856
pubmed: 30788871
Science. 2019 Aug 23;365(6455):
pubmed: 31439761
Am J Bot. 2016 Feb;103(2):207-20
pubmed: 26838365
Bioinformatics. 2021 Nov 5;37(21):3941-3943
pubmed: 33961008
Science. 2014 Nov 28;346(6213):1256688
pubmed: 25430773
PLoS Pathog. 2012;8(6):e1002701
pubmed: 22737067
Ecol Lett. 2016 Aug;19(8):926-36
pubmed: 27264635
mBio. 2019 Dec 17;10(6):
pubmed: 31848279
PeerJ. 2022 Feb 10;10:e12868
pubmed: 35186471
Nat Biotechnol. 2019 Aug;37(8):852-857
pubmed: 31341288
Front Microbiol. 2021 Jun 07;12:676251
pubmed: 34163452

Auteurs

Lukas P Bell-Dereske (LP)

W.K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, USA. lukas.dereske@gmail.com.
The Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA. lukas.dereske@gmail.com.
Laboratory of Environmental Microbiology, Institute of Microbiology, Czech Academy of Sciences, Vídeňská, Prague 4, 1083, 142 20, Czech Republic. lukas.dereske@gmail.com.

Gian Maria Niccolò Benucci (GMN)

The Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA.
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA.
Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing, MI, USA.

Pedro Beschoren da Costa (PB)

Laboratory of Entomology, Department of Plant Sciences, Wageningen University & Research, Wageningen, The Netherlands.

Gregory Bonito (G)

The Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA.
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA.
Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing, MI, USA.

Maren L Friesen (ML)

Department of Plant Pathology, Department of Crop and Soil Sciences, Washington State University, Pullman, WA, USA.

Lisa K Tiemann (LK)

The Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA.
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA.

Sarah E Evans (SE)

W.K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, USA.
The Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, USA.
Department of Integrative Biology, Michigan State University, East Lansing, MI, USA.
Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing, MI, USA.

Classifications MeSH