Differential dynamics of microbial community networks help identify microorganisms interacting with residue-borne pathogens: the case of Zymoseptoria tritici in wheat

Abstract Background Wheat residues are a crucial determinant of the epidemiology of Septoria tritici blotch, as they support the sexual reproduction of the causal agent Zymoseptoria tritici . We aimed to characterize the effect of infection with this fungal pathogen on the microbial communities present on wheat residues, and to identify microorganisms interacting with it. We used metabarcoding to compare the microbiome associated with wheat residues placed outdoors, with and without preliminary Z. tritici inoculation, comparing a first set of residues in contact with the soil and a second set without contact with the soil, on four sampling dates in two consecutive years. Results The diversity of the tested conditions, leading to the establishment of different microbial communities according to the origins of the constitutive taxa (plant only, or plant and soil), highlighted the effect of Z. tritici on the wheat residue microbiome. Several microorganisms were affected by Z. tritici infection, even after the disappearance of the pathogen. Linear discriminant analyses and ecological network analyses were combined to describe the communities affected by infection. The number of fungi and bacteria promoted or inhibited by inoculation with Z. tritici decreased over time, and was smaller for residues in contact with the soil. The interactions between the pathogen and other microorganisms appeared to be mostly indirect, despite the strong position of the pathogen as a keystone taxon in networks. Direct interactions with other members of the communities mostly involved fungi, including other wheat pathogens. Conclusions Our results provide essential information about the alterations to the microbial community in wheat residues induced by the mere presence of a fungal pathogen, and vice versa. Species already described as beneficial or biocontrol agents were found to be affected by pathogen inoculation. The strategy developed here can be viewed as a proof-of-concept for crop residues serving as a particularly rich ecological compartment, with a high diversity of taxa originating from both the plant and soil compartments, and for Z. tritici -wheat as a model pathosystem. By revealing putative antagonistic interactions, we demonstrate that this strategy can be used to improve the biological control of residue-borne diseases.