Root endophytic bacterial and fungal communities in a natural hot desert are differentially regulated in dry and wet seasons by stochastic processes and functional traits.


Journal

The Science of the total environment
ISSN: 1879-1026
Titre abrégé: Sci Total Environ
Pays: Netherlands
ID NLM: 0330500

Informations de publication

Date de publication:
15 Nov 2023
Historique:
received: 12 02 2023
revised: 10 07 2023
accepted: 11 07 2023
medline: 20 9 2023
pubmed: 20 7 2023
entrez: 19 7 2023
Statut: ppublish

Résumé

Dryland ecosystems experience seasonal cycles of severe drought and moderate precipitation. Desert plants may develop symbiotic relationships with root endophytic microbes to survive under the repeated wet and extremely dry conditions. Although community coalescence has been found in many systems, the colonization by functional microbes and its relationship to seasonal transitions in arid regions are not well understood. Here we examined root endophytic microbial taxa, and their traits in relation to their root colonization, during the dry and wet seasons in a hot desert of the southwestern United States. We used high-throughput DNA sequencing of 16S rRNA and internal transcribed spacer gene profiling of five desert shrubs, and analyzed the seasonal change in endophytic microbial lineages. Goodness of fit to the neutral community model in relationship to microbial traits was evaluated. In summer, Actinobacteria and Bacteroidia increased, although this was not genus-specific. For fungi, Glomeraceae selectively increased in summer. In winter, Gram-negative bacterial genera, including those capable of nitrogen fixation and plant growth promotion, increased. Neutral model analysis revealed a strong stochastic influence on endophytic bacteria but a weak effect for fungi, especially in summer. The taxa with higher frequency than that predicted by neutral model shared environmental adaptability and symbiotic traits, whereas the frequency of pathogenic fungi was at or under the predicted value. These results suggest that community assembly of bacteria and fungi is regulated differently. The bacterial community was affected by stochastic and deterministic processes via bacterial response to drought (response trait), beneficial effect on plants (effect trait), and likely stable mutualistic interactions with plants suggested by the frequency of nodule bacteria. For fungi, mycorrhizal fungi were selected by plants in summer. The regulation of beneficial microbes by plants in both dry and wet seasons suggests the presence of plant-soil positive feedback in this natural desert ecosystem.

Identifiants

pubmed: 37467971
pii: S0048-9697(23)04147-5
doi: 10.1016/j.scitotenv.2023.165524
pii:
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

165524

Informations de copyright

Copyright © 2023 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Takeshi Taniguchi (T)

Arid Land Research Center, Tottori University, Tottori 680-0001, Japan. Electronic address: takeshi@tottori-u.ac.jp.

Kazuo Isobe (K)

Institute of Ecology, College of Urban and Environmental Sciences, Peking University, Beijing 100871, China.

Shogo Imada (S)

Department of Radioecology, Institute for Environmental Sciences, Aomori 039-3212, Japan.

Mohamed M Eltayeb (MM)

Arid Land Research Center, Tottori University, Tottori 680-0001, Japan; Department of Food Science and Technology, Faculty of Agriculture, University of Khartoum, Shambat 13314, Sudan.

Yasuaki Akaji (Y)

Biodiversity Division, National Institute for Environmental Studies, Ibaraki 305-8506, Japan.

Masataka Nakayama (M)

Research Group for Environmental Science, Japan Atomic Energy Agency, Ibaraki 319-1195, Japan.

Michael F Allen (MF)

Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521, USA.

Emma L Aronson (EL)

Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521, USA.

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Classifications MeSH