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

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.

Pinpointing the distinctive impacts of ten cover crop species on the resident and active fractions of the soil microbiome

“…It is premature to couple the increased activity of members of this predatory protistan order with the strong stimulation of Pseudomonadaceae in this cover crop species. However, a novel study by Guo et al (2022) connected the enrichment of protistan predators with the stimulation of disease-suppressive bacteria belonging to Bacillus spp . in the rhizosphere.…”

Microbiomes in agroecosystem: Diversity, function and assembly mechanisms

“…Interestingly, the seed‐endophytic bacterium Sphingomonas melonis can be transmitted across generations in disease‐resistant rice seeds and positively affects rice resistance to pathogens by producing anthranilic acid (Matsumoto et al, 2021). Besides bacteria and fungi, accumulating evidence suggests that protists and algae are also important members of the crop microbiome, which can provide protective effect on crop health (Guo et al, 2022; Lee & Ryu, 2021; Xiong et al, 2020). For instance, a recent study showed that protistan predators can strongly enhance banana health and yield by stimulating disease‐suppressive bacteria like Bacillus spp.…”

“…For instance, a recent study showed that protistan predators can strongly enhance banana health and yield by stimulating disease‐suppressive bacteria like Bacillus spp. (Guo et al, 2022). Algal species like prokaryotic Anabaena spp.…”

“…The plant microbiome consists of diverse microbial taxa including bacteria, archaea, fungi, protists and viruses, which play a variety of important roles such as nutrient uptake, disease resistance, and abiotic stress tolerance for plant growth and health (Carrión et al, 2019; de Vries et al, 2020; Toju et al, 2018; Trivedi et al, 2020). Many recent discoveries suggest that crop‐associated microbiomes can be harnessed to protect the crops against pathogens (Carrión et al, 2019; Guo et al, 2022; Lee et al, 2021) and to enhance crop resilience to abiotic stresses like drought and salt (Qi et al, 2022; Schmitz et al, 2022; Xu, Dong, et al, 2021). It was reported that global demand for agricultural crops is expected to rise 70% by 2050 to feed the growing population, and the microbiome engineering was proposed as a vital biotechnological strategy to improve crop productivity and health in a sustainable way (Arif et al, 2020; Haskett et al, 2021; Singh et al, 2020).…”

High bacterial diversity and siderophore-producing bacteria collectively suppress Fusarium oxysporum in maize/faba bean intercropping

“…In contrast, legumes such as faba bean and chickpea acidify the rhizosphere by releasing protons and organic acids (Li et al, 2007;Wen et al, 2021), which may increase Fe availability but decrease siderophore production by bacteria. Most microbial siderophores are synthesized by nonribosomal peptide synthetase (NRPS)-dependent pathway (Kadi and Challis, 2009;Verbon et al, 2017), and act as microbicides to suppress plant pathogens (Guo et al, 2022), such as the pyochelin (De Vleesschauwer et al, 2006) and enterochelin (Lambrese et al, 2018). Hence, competition for iron between crop and rhizosphere microbiome may be an important mechanism explaining disease suppression, although other mechanisms such as antibiosis or activation of plant immunity are also involved (Li et al, 2021c).…”