Abstract
Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.
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Data availability
All raw 16 S rRNA, ITS and 18 S rRNA gene sequences are available at the NCBI Sequence Read Archive (SRA) under the accession number BioProject PRJNA737165. The raw data of metagenomics-derived gene catalogues are publicly available under the accession number BioProject PRJNA736854.
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Acknowledgements
This study was funded by the National Natural Science Foundation of China (42090065, 31972509, 41867006 and 32102475), the Fundamental Research Funds for the Central Universities (KYXK202009), the China Postdoctoral Science Foundation (2021TQ0156 and 2021M691613), the 111 project (B12009), and the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD). Stefan Geisen was supported by an NWO-VENI grant from the Netherlands Organisation for Scientific Research (016.Veni.181.078).
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SG, CT, AJ, WX, ZX, ZG, RL, QS, GAK and SG developed the ideas and designed the experimental plans. SG, CT, ZW, ZS, BW, SL, RL and YR performed the experiments. SG, CT, WX, RL and SG analyzed the data. SG, CT, AJ, RL, QS, GAK and SG participated in the completion of the manuscript.
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Guo, S., Tao, C., Jousset, A. et al. Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. ISME J 16, 1932–1943 (2022). https://doi.org/10.1038/s41396-022-01244-5
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DOI: https://doi.org/10.1038/s41396-022-01244-5
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