Predatory protists impact plant performance by promoting plant growth-promoting rhizobacterial consortia

Sai Guo, Stefan Geisen, Yani Mo, Xinyue Yan, Ruoling Huang, Hongjun Liu, Zhilei Gao, Chengyuan Tao, Xuhui Deng, Wu Xiong, Qirong Shen, George A. Kowalchuk, Rong Li*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Plant performance is impacted by rhizosphere bacteria. These bacteria are subjected to both bottom-up control by root exudates as well as top-down control by predators, particularly protists. Protists stimulate plant growth-promoting microbes resulting in improved plant performance. However, knowledge of the mechanisms that determine the interconnections within such tripartite protist-bacteria-plant interactions remains limited. We conducted experiments examining the effects of different densities of the predatory protist Cercomonas lenta on rhizosphere bacterial communities, specifically zooming on interactions between Cercomonas lenta and key bacterial taxa, as well as interactions among key bacterial taxa. We tracked rhizosphere bacterial community composition, potential microbial interactions, and plant performance. We found that Cercomonas lenta inoculation led to an average increase in plant biomass of 92.0%. This effect was linked to an increase in plant growth-promoting rhizobacteria (Pseudomonas and Sphingomonas) and a decrease in bacteria (Chitinophaga) that negatively impact on plant growth-promoting rhizobacteria. We also found evidence for cooperative enhancements in biofilm formation within the plant growth-promoting rhizobacterial consortium. Cercomonas lenta enhanced a plant growth-promoting rhizobacterial consortium colonization by promoting its cooperative biofilm formation in the rhizosphere, leading to a 14.5% increase in phosphate solubilization that benefits plant growth. Taken together, we provide mechanistic insights into how the predatory protist Cercomonas lenta impacts plant growth, namely by stimulating plant beneficial microbes and enhancing their interactive activities such as biofilm formation. Predatory protists may therefore represent promising biological agents that can contribute to sustainable agricultural practices by promoting interactions between the plant and its microbiome.

Original languageEnglish
Article numberwrae180
Number of pages11
JournalThe ISME Journal
Volume18
Issue number1
DOIs
Publication statusPublished - 8 Jan 2024

Bibliographical note

Publisher Copyright:
© 2024 The Author(s).

Funding

This work was supported by the National Key Research and Development Program (2023YFE0104700), the Fundamental Research Funds for the Central Universities (KJJQ2024020 and KYPT2024005), and the Achievement Transformation Fund project of the Sanya Institute of Nanjing Agricultural University (NAUSY-CG-ZD-01).

FundersFunder number
Achievement Transformation Fund
National Key Research and Development Program of China2023YFE0104700
National Key Research and Development Program of China
Fundamental Research Funds for the Central UniversitiesKJJQ2024020, KYPT2024005
Fundamental Research Funds for the Central Universities
Sanya Institute, Nanjing Agricultural UniversityNAUSY-CG-ZD-01
Sanya Institute, Nanjing Agricultural University

    Keywords

    • plant growth-promoting rhizobacteria
    • plant performance enhancement
    • predatory protists
    • rhizosphere microbial interactions

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