Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

• Published in: The ISME Journal Vol. 16; no. 8; pp. 1932 - 1943
• Main Authors: Guo, Sai, Tao, Chengyuan, Jousset, Alexandre, Xiong, Wu, Wang, Zhe, Shen, Zongzhuan, Wang, Beibei, Xu, Zhihui, Gao, Zhilei, Liu, Shanshan, Li, Rong, Ruan, Yunze, Shen, Qirong, Kowalchuk, George A., Geisen, Stefan
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.08.2022; Oxford University Press
• Subjects: 45/22; 45/23; 45/47; 45/77; 631/326/2565/2134; 704/158/855; Agricultural practices; Bacillus; Bacteria; Bacteria - genetics; Biological models (mathematics); Biomedical and Life Sciences; Ecology; Eukaryota - genetics; Evolutionary Biology; Fertilization; Fungi - genetics; Life Sciences; Metabolites; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microbiomes; Microorganisms; Organic fertilizers; Pathogens; Plant Diseases - microbiology; Predator-prey interactions; Predators; Prey; Relative abundance; Soil - chemistry; Soil bacteria; Soil investigations; Soil Microbiology; Soil microorganisms; Soils; Steering; Sustainable agriculture; Sustainable practices; Trophic relationships; Wilt
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/s41396-022-01244-5

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.