Rhizosphere Mysteries: Metabolite Reduction Down-regulated Fungal Diversity and Community Function

The rhizosphere serves as the primary defense against pathogens, but rhizosphere metabolites can also act as carbon sources and signaling molecules that attract soil borne pathogenic fungi to the destruction of rhizosphere defenses. We propose that whether reducing rhizosphere metabolites improves complex microbial networks defense. Here, we found that reducing rhizosphere metabolites altered fungal community structure more than bacteria, resulting in a downward trend in fungal diversity, soil-borne pathogenic fungal Fusarium abundance, and soil microbial community functions, e.g., metabolic functions, enzyme activities, and protein expression. However, the trend is more favorable to plant growth, which might be explained by the combined effect of the upward trend in bacterial diversity in the rhizosphere and bulk soil. Furthermore, we identified biomarkers Monographella, Acremonium, Geosmithia, and Funneliformis, which negatively correlated with other differential microbiology, play a competitive role in community member interactions. they optimized the microbial ecology with functions that mobilize soil nutrients, reduce pathogens and soil acidification, and lower phenolic acids. Integrating our findings proposes new avenues for understanding the complex soil rhizosphere mysteries of the critical role of metabolites in "soil environment - microorganisms - metabolites" ecology interactions and provides a design to build synthetic microbial community to enhance defense. IMPORTANCEWhile rhizosphere metabolites are known to regulate microorganisms composition to enhance plant immunity cooperatively. However, they also have a harmful side, which attracts soil-borne pathogenic fungi to form synergistic damage that inhibits beneficial bacteria, produces autotoxicity, destroys the rhizosphere microbial ecology, and negatively affects soil productivity and plant health. Currently, our planet is experiencing unprecedented anthropogenic-induced changes. Moreover, the complex and dynamic ecological network in the rhizosphere-an important microbial hotspot-is among the most fascinating yet elusive topics in microbial ecology. Whether reduced rhizosphere metabolites improves the microbial ecological networks remains unknown. Our findings revealed that reduced rhizosphere metabolites decrease fungal diversity, microbial community function, and pathogen abundance, while increase bacterial diversity, soil nutrients, pH, and similar factors. It is clear that reduced rhizosphere metabolites is undoubtedly beneficial for plant health and the rhizosphere ecology. Ultimately, This study provided a new comprehensive understanding of how fungi and bacteria assemble and alter in the rhizosphere and bulk soil when reduced rhizosphere metabolites. Understanding the critical role of rhizosphere metabolites in restoring micro-ecological balance will allow us to focus on regulating microbial community metabolism and root exudates, facilitate the discovery of new metabolites and interactions with microorganisms, and harness their the beneficial properties that contribute to rhizosphere microbial community assembly.