To defend or to attack? Antagonistic interactions between Serratia plymuthica and fungal plant pathogens, a species-specific volatile dialogue

Abstract

Volatile organic compounds (VOCs) are involved in microbial interspecies communication and in the mode of action of various antagonistic interactions. They are important for balancing host-microbe interactions and provide the basis for developing biological control strategies to control plant pathogens. We studied the interactions between the bacterial antagonist Serratia plymuthica HRO-C48 and three fungal plant pathogens Rhizoctonia solani, Leptosphaeria maculans and Verticillium longisporum. Significant differences in fungal growth inhibition by the Serratia-emitted VOCs in pairwise dual culture assays and changes in the transcriptome of the bacterium and in the volatilomes of both interacting partners were observed. Even though the rate of fungal growth inhibition by Serratia was variable, the confrontation of the bacterium with the VOCs of all three fungi changed the levels of expression of the genes involved in stress response, biofilm formation, and the production of antimicrobial VOCs. Pairwise interacting microorganisms switched between defense (downregulation of gene expression) and attack (upregulation of gene expression and metabolism followed by growth inhibition of the interacting partner) modes, subject to the combinations of microorganisms that were interacting. In the attack mode HRO-C48 significantly inhibited the growth of R. solani while simultaneously boosting its own metabolism; by contrast, its metabolism was downregulated when HRO-C48 went into a defense mode that was induced by the L. maculans and V. longisporum VOCs. L. maculans growth was slightly reduced by the one bacterial VOC methyl acetate that induced a strong downregulation of expression of genes involved in almost all metabolic functions in S. plymuthica. Similarly, the interaction between S. plymuthica and V. longisporum resulted in an insignificant growth reduction of the fungus and repressed the rate of bacterial metabolism on the transcriptional level, accompanied by an intense volatile dialogue. Overall, our results indicate that VOCs substantially contribute to the highly break species-specific interactions between pathogens and their natural antagonists and thus deserving of increased consideration for pathogen control.

A new system to study directional volatile-mediated interactions reveals the ability of fungi to specifically react to other fungal volatiles

“…They can affect their growth and development, their motility, they can attract or repel, as well as inhibit or promote the growth of individuals from the same species or other kingdoms including animals and plants (Schmidt et al, 2016;Bruisson et al, 2020;Farh and Jeon, 2020). In the past few years, evidence showed that once a microorganism is affected by external volatiles, the composition of its own volatilome (i.e., the sum of all the volatiles it emits) may also change; some compounds will therefore be detected in higher vs. lower abundances, while others will only be detected or in contrast will no longer be detected as a result of the interaction (Rybakova et al, 2017(Rybakova et al, , 2022. Until now, such interactions have only been studied in confined environments with the partners sharing the same headspace, allowing the reciprocal influence of the two partners.…”