Specific metabolites drive the deterministic assembly of diseased rhizosphere microbiome through weakening microbial degradation of autotoxin
Tao Wen,
Penghao Xie,
C. Ryan Penton,
Lauren Hale,
Linda S. Thomashow,
Shengdie Yang,
Zhexu Ding,
Yaqi Su,
Jun Yuan,
Qirong Shen
Affiliations
Tao Wen
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Penghao Xie
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
C. Ryan Penton
Center for Fundamental and Applied Microbiomics, Biodesign Institute, Arizona State University
Lauren Hale
Agricultural Research Service, USDA, San Joaquin Valley Agricultural Sciences Center
Linda S. Thomashow
Agricultural Research Service, US Department of Agriculture, Wheat Health, Genetics and Quality Research Unit
Shengdie Yang
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Zhexu Ding
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Yaqi Su
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Jun Yuan
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Qirong Shen
The Key Laboratory of Plant ImmunityJiangsu Provincial Key Lab for Organic Solid Waste UtilizationJiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University
Abstract Background Process and function that underlie the assembly of a rhizosphere microbial community may be strongly linked to the maintenance of plant health. However, their assembly processes and functional changes in the deterioration of soilborne disease remain unclear. Here, we investigated features of rhizosphere microbiomes related to Fusarium wilt disease and assessed their assembly by comparison pair of diseased/healthy sequencing data. The untargeted metabolomics was employed to explore potential community assembly drivers, and shotgun metagenome sequencing was used to reveal the mechanisms of metabolite-mediated process after soil conditioning. Results Results showed the deterministic assembly process associated with diseased rhizosphere microbiomes, and this process was significantly correlated to five metabolites (tocopherol acetate, citrulline, galactitol, octadecylglycerol, and behenic acid). Application of the metabolites resulted in a deterministic assembly of microbiome with the high morbidity of watermelon. Furthermore, metabolite conditioning was found to weaken the function of autotoxin degradation undertaken by specific bacterial group (Bradyrhizobium, Streptomyces, Variovorax, Pseudomonas, and Sphingomonas) while promoting the metabolism of small-molecule sugars and acids initiated from another bacterial group (Anaeromyxobacter, Bdellovibrio, Conexibacter, Flavobacterium, and Gemmatimonas). Video Abstract Conclusion These findings strongly suggest that shifts in a metabolite-mediated microbial community assembly process underpin the deterministic establishment of soilborne Fusarium wilt disease and reveal avenues for future research focusing on ameliorating crop loss due to this pathogen.
