Rhizosphere Microbiome Recruited from a Suppressive Compost Improves Plant Fitness and Increases Protection against Vascular Wilt Pathogens of Tomato

Abstract

Suppressive composts represent a sustainable approach to combat soilborne plant pathogens and an alternative to the ineffective chemical fungicides used against those. Nevertheless, suppressiveness to plant pathogens and reliability of composts are often inconsistent with unpredictable effects. While suppressiveness is usually attributed to the compost’s microorganisms, the mechanisms governing microbial recruitment by the roots and the composition of selected microbial communities are not fully elucidated. Herein, the purpose of the study was to evaluate the impact of a compost on tomato plant growth and its suppressiveness against Fusarium oxysporum f. sp. lycopersici (Foxl) and Verticillium dahliae (Vd). First, growth parameters of tomato plants grown in sterile peat-based substrates including 20 and 30% sterile compost (80P/20C-ST and 70P/30C-ST) or non-sterile compost (80P/20C and 70P/30C) were evaluated in a growth room experiment. Plant height, total leaf surface, and fresh and dry weight of plants grown in the non-sterile compost mixes were increased compared to the plants grown in the sterile compost substrates, indicating the plant growth promoting activity of the compost’s microorganisms. Subsequently, compost’s suppressiveness against Foxl and Vd was evaluated with pathogenicity experiments on tomato plants grown in 70P/30C-ST and 70P/30C substrates. Disease intensity was significantly less in plants grown in the non-sterile compost than in those grown in the sterile compost substrate; AUDPC was 2.3- and 1.4-fold less for Foxl and Vd, respectively. Moreover, fungal quantification in planta demonstrated reduced colonization in plants grown in the non-sterile mixture. To further investigate these findings, we characterized the culturable microbiome attracted by the roots compared to the unplanted compost. Bacteria and fungi isolated from unplanted compost and the rhizosphere of plants were sequence-identified. Community-level analysis revealed differential microbial communities between the compost and the rhizosphere, suggesting a clear effect of the plant in the microbiome assembly. Proteobacteria and Actinobacteria were highly enriched in the rhizosphere whereas Firmicutes were strongly represented in both compartments with Bacillus being the most abundant species. Our results shed light on the composition of a microbial consortium that could protect plants against the wilt pathogens of tomato and improve plant overall health.

Rhizosphere-enriched microbes as a pool to design synthetic communities for reproducible beneficial outputs

“…To understand whether the previously observed disease suppressiveness of soil-borne pathogens 26 is attributed to specific microbes selected in tomato rhizosphere, we tested in dual-culture assays the antagonistic activity of the rhizobacterial strains against Vd and Fox (Fig. 1).…”

“…Previously, the compost-derived and rhizosphere-enriched isolates were not only associated with disease suppressiveness, but also with plant growth promotion 26 . Therefore, the 47 strains displaying an inhibitory effect on Vd and Fox mycelial growth in vitro (Fig.…”

“…In an effort to assess how the rhizosphere enrichment of diverse bacterial isolates from a compost can benefit the host plant 26 , we designed two simplified SynComs from the bacteria characterized in the current study. SynCom1 was composed of 25 strains, aiming to reflect the representation of the most abundant phylogenetic groups detected in the rhizosphere (Supplementary Information Table S3).…”

“…SynCom1 was composed of 25 strains, aiming to reflect the representation of the most abundant phylogenetic groups detected in the rhizosphere (Supplementary Information Table S3). SynCom2 was composed of 25 Bacillus strains (Supplementary Information Table S3), in order to test if the dominance of the Phylum Firmicutes in the rhizosphere of tomato plants (33%, Supplementary Information Table S1) can explain by itself the beneficial effects on plant fitness 26 . Initially, SynComs were tested in vitro for their effect on Arabidopsis growth, 20 d after root inoculation.…”

“…In this study, we build on our previous work where we demonstrated that the activity of the microorganisms contained in a compost promoted plant growth and enhanced the protection of tomato plants against Verticillium dahliae ( Vd ) and Fusarium oxysporum f. sp lycopersici ( Fox ). Community-level analysis of the culturable microbiome revealed differential distribution of the microbial communities between the compost and the rhizosphere, suggesting that plants recruit beneficial soil microorganisms for their own benefit 26 . The aims of the present study are: (a) to assess if bacterial genera enriched in the rhizosphere of tomato plants have antifungal potential and can improve plant fitness; (b) to test whether the composition of synthetic communities (SynComs) can affect growth and defense outputs; and (c) to use simplified SynComs in sterile peat-based growth substrate and reproduce the suppressive and growth promotion properties of the compost on tomato plants.…”