Protist diversity and community complexity in the rhizosphere of switchgrass are dynamic as plants develop.

Community assembly Rhizosphere Soil microbiome Soil protist Switchgrass

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
28 04 2021
Historique:
received: 27 12 2020
accepted: 26 02 2021
entrez: 29 4 2021
pubmed: 30 4 2021
medline: 7 5 2021
Statut: epublish

Résumé

Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues to grow, but there remains a need to understand the extent to which biological and environmental factors mediate protist community assembly and dynamics. We hypothesize that protists communities are filtered by the influence of plants on their rhizosphere biological and physicochemical environment, resulting in patterns of protist diversity and composition that mirror previously observed diversity and successional dynamics in rhizosphere bacterial communities. We analyzed protist communities associated with the rhizosphere and bulk soil of switchgrass (SG) plants (Panicum virgatum) at different phenological stages, grown in two marginal soils as part of a large-scale field experiment. Our results reveal that the diversity of protists is lower in rhizosphere than bulk soils, and that temporal variations depend on soil properties but are less pronounced in rhizosphere soil. Patterns of significantly prevalent protists groups in the rhizosphere suggest that most protists play varied ecological roles across plant growth stages and that some plant pathogenic protists and protists with omnivorous diets reoccur over time in the rhizosphere. We found that protist co-occurrence network dynamics are more complex in the rhizosphere compared to bulk soil. A phylogenetic bin-based null model analysis showed that protists' community assembly in our study sites is mainly controlled by homogenous selection and dispersal limitation, with stronger selection in rhizosphere than bulk soil as SG grew and senesced. We demonstrate that environmental filtering is a dominant determinant of overall protist community properties and that at the rhizosphere level, plant control on the physical and biological environment is a critical driver of protist community composition and dynamics. Since protists are key contributors to plant nutrient availability and bacterial community composition and abundance, mapping and understanding their patterns in rhizosphere soil is foundational to understanding the ecology of the root-microbe-soil system. Video Abstract.

Sections du résumé

BACKGROUND
Despite their widespread distribution and ecological importance, protists remain one of the least understood components of the soil and rhizosphere microbiome. Knowledge of the roles that protists play in stimulating organic matter decomposition and shaping microbiome dynamics continues to grow, but there remains a need to understand the extent to which biological and environmental factors mediate protist community assembly and dynamics. We hypothesize that protists communities are filtered by the influence of plants on their rhizosphere biological and physicochemical environment, resulting in patterns of protist diversity and composition that mirror previously observed diversity and successional dynamics in rhizosphere bacterial communities.
RESULTS
We analyzed protist communities associated with the rhizosphere and bulk soil of switchgrass (SG) plants (Panicum virgatum) at different phenological stages, grown in two marginal soils as part of a large-scale field experiment. Our results reveal that the diversity of protists is lower in rhizosphere than bulk soils, and that temporal variations depend on soil properties but are less pronounced in rhizosphere soil. Patterns of significantly prevalent protists groups in the rhizosphere suggest that most protists play varied ecological roles across plant growth stages and that some plant pathogenic protists and protists with omnivorous diets reoccur over time in the rhizosphere. We found that protist co-occurrence network dynamics are more complex in the rhizosphere compared to bulk soil. A phylogenetic bin-based null model analysis showed that protists' community assembly in our study sites is mainly controlled by homogenous selection and dispersal limitation, with stronger selection in rhizosphere than bulk soil as SG grew and senesced.
CONCLUSIONS
We demonstrate that environmental filtering is a dominant determinant of overall protist community properties and that at the rhizosphere level, plant control on the physical and biological environment is a critical driver of protist community composition and dynamics. Since protists are key contributors to plant nutrient availability and bacterial community composition and abundance, mapping and understanding their patterns in rhizosphere soil is foundational to understanding the ecology of the root-microbe-soil system. Video Abstract.

Identifiants

pubmed: 33910643
doi: 10.1186/s40168-021-01042-9
pii: 10.1186/s40168-021-01042-9
pmc: PMC8082632
doi:

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Video-Audio Media

Langues

eng

Sous-ensembles de citation

IM

Pagination

96

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Auteurs

Javier A Ceja-Navarro (JA)

Bioengineering and Biomedical Sciences Department, Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. jcnavarro@lbl.gov.
Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA. jcnavarro@lbl.gov.

Yuan Wang (Y)

Noble Research Institute, LLC, Ardmore, OK, USA.

Daliang Ning (D)

Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, USA.
State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, China.

Abelardo Arellano (A)

Bioengineering and Biomedical Sciences Department, Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Leila Ramanculova (L)

Bioengineering and Biomedical Sciences Department, Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Mengting Maggie Yuan (MM)

Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA.

Alyssa Byer (A)

Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA.

Kelly D Craven (KD)

Noble Research Institute, LLC, Ardmore, OK, USA.

Malay C Saha (MC)

Noble Research Institute, LLC, Ardmore, OK, USA.

Eoin L Brodie (EL)

Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA.
Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Jennifer Pett-Ridge (J)

Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA.

Mary K Firestone (MK)

Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA. mkfstone@berkeley.edu.
Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. mkfstone@berkeley.edu.

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Classifications MeSH