Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes

Front Microbiol. 2023 Mar 16:14:1141585. doi: 10.3389/fmicb.2023.1141585. eCollection 2023.

Abstract

Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this study, healthy and diseased (bacterial wilt disease, BWD) tomato (Solanum lycopersicum L.) plants were harvested, and variations in the rhizosphere and root endosphere microbial communities were subsequently investigated using amplicon and shotgun metagenome sequencing. BWD led to a significant increase in rhizosphere bacterial diversity in the rhizosphere but reduced bacterial diversity in the root endosphere. The ecological null model indicated that BWD enhanced the bacterial deterministic processes in both the rhizosphere and root endosphere. Network analysis showed that microbial co-occurrence complexity was increased in BWD-infected plants. Moreover, higher universal ecological dynamics of microbial communities were observed in the diseased rhizosphere. Metagenomic analysis revealed the enrichment of more functional gene pathways in the infected rhizosphere. More importantly, when tomato plants were infected with BWD, some plant-harmful pathways such as quorum sensing were significantly enriched, while some plant-beneficial pathways such as streptomycin biosynthesis were depleted. These findings broaden the understanding of plant-microbiome interactions and provide new clues to the underlying mechanism behind the interaction between the plant microbiome and BWD.

Keywords: assembly mechanism; bacterial wilt disease; microbial interactions; microbiome function; plant microbiome.

Grants and funding

This study was supported by the Fundamental Research Funds for the Central Universities (680-ZJ21195006), the National Natural Science Foundation of China (42207349), the Natural Science Foundation of Jiangsu Province (BK20221005), the China Postdoctoral Science Foundation (2022M711653), and the Jiangsu Funding Program for Excellent Postdoctoral Talent (2022ZB331).