Specific metabolites drive the deterministic assembly of diseased rhizosphere microbiome through weakening microbial degradation of autotoxin

Authors: WEN, TAO - Nanjing Agricultural University; XIE, PENGHAO - Nanjing Agricultural University; PENTON, RYAN - Arizona State University; Hale, Lauren; Thomashow, Linda; YANG, SHENGDIE - Nanjing Agricultural University; FANG, YIYI - Nanjing Agricultural University; YUAN, JUN - Nanjing Agricultural University; SHEN, QIRONG - Nanjing Agricultural University

Submitted to: Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/19/2022
Publication Date: 10/21/2022
Citation: Wen, T., et al. Specific metabolites drive the deterministic assembly of diseased rhizosphere microbiome through weakening microbial degradation of autotoxin. Microbiome. (2022)10. Article 177. https://doi.org/10.1186/s40168-022-01375-z.
DOI: https://doi.org/10.1186/s40168-022-01375-z

Interpretive Summary: Fusarium wilt disease causes major crop losses worldwide because the pathogen has a broad host range. However, the processes that provide an environment favorable to the initiation of the disease are poorly understood. This study investigated the bacterial species in soil environments favoring the establishment of Fusarium wilt disease and the chemicals released by the roots of diseased host plants in these environments. Five bacteria and five compounds were identified that, together, appeared to favor the assembly of a microbial community favoring the establishment of Fusarium wilt disease. Application of the compounds to soils resulted in the assembly of the bacterial community and a high rate of wilt disease of watermelon in soil containing the Fusarium pathogen. Collectively, the results suggest that the identified root compounds drive the assembly of microbial groups in the root environment that favor the development of Fusarium wilt disease. The work helps to set the stage for future research aimed at lessening crop loss due to this pathogen.

Technical Abstract: Fusarium wilt disease causes substantial crop loss world-wide due to the widespread occurrence and broad host range of its causative pathogen, Fusarium oxysporum. Processes that underlie the assembly of a rhizosphere microbial community may be strongly linked to the initiation and maintenance of Fusarium wilt disease. However, the characteristics that drive the assembly of such a community, as well as the mechanisms that influence the process, remain unclear. To address these questions, we investigated features of rhizosphere microbiomes related to Fusarium wilt disease and assessed their assembly using integrated sequence metadata. We employed un-targeted metabolomics to explore potential community assembly drivers. Lower diversity and deterministic assembly processes were associated with diseased rhizosphere microbiomes. Several compounds (tocopherol acetate, citrulline, galactitol, octadecylglycerol and behenic acid) had the greatest impact on the relative abundances of specific bacterial taxa (Anaeromyxobacter, Bdellovibrio, Conexibacter, Flavobacterium and Gemmatimonas) which, in concert, appeared to drive the assembly of a microbial community favoring the establishment of soil-borne Fusarium wilt disease. . Application of these compounds to soils resulted in a deterministic assembly of the bacterial community and high (up to 60%-80%) morbidity of watermelon when the soil was inoculated with F. oxysporum.. Our study revealed inherent differences in the composition of diseased and ‘healthy’ rhizosphere microbiomes and identified particular rhizosphere metabolites that drove the assembly of metabolite-responsive microbial groups contributing significantly to the characteristics of a diseased rhizosphere microbiome. Collectively, these findings suggest strongly that shifts in a metabolite-mediated microbial community assembly process underpin the deterministic establishment of soil-borne Fusarium wilt disease and reveal avenues for future research focused on ameliorating crop loss to this pathogen.