Impact of phage treatment on fire blight disease outcome and floral microbiome composition

With the increasing importance of alternative pesticides for the control of bacterial pathogens in agricultural and clinical settings, the use of bacteriophage viruses (phages) to reduce bacterial growth and prevent disease is gaining in popularity. Phages have been shown to be highly effective in killing bacterial cells both in vitro and across plant and animal host systems, although many questions remain about the predictability of their success across more realistic ecological conditions and in light of natural strain variation of pathogens. Furthermore, as phage application becomes more common, it is imperative that we better understand the consequences of these treatments on the microbial communities associated with hosts (i.e., their microbiomes). Here, we leverage a recently developed phage cocktail targeting the causal agent of fire blight disease, Erwinia amylovora, to both test the efficacy of these phages in pear flowers inoculated with the pathogen and to ask whether such application has adverse effects on the resident microbiome of flowers. We found that phages are capable of greatly reducing both pathogen numbers and disease symptoms, but their application does not significantly alter the floral microbiome, emphasizing their high specificity to their target host. These data support the safe and effective use of phages in this disease system.IMPORTANCEThere is a critical need to develop new strategies to control bacterial diseases in crops, particularly to address the emerging problem of fire blight in pomme fruit. Bacteriophages, as viruses that infect and kill bacteria, are an appealing strategy. However, there is little information on how these viruses are impacting natural microbial communities, their potential off-target effects, and their environmental safety. This study addresses these questions, looking at the impact of an effective phage cocktail targeting Erwinia amylovora, the causal agent of fire blight in pomme fruit. In our research, we demonstrated that our phage cocktail does not affect the natural floral microbiome of Bradford pear blossoms. We further found that in the presence of E. amylovora, our phage cocktail significantly increases the richness and diversity of the microbial community. Our data, together with other studies performed in parallel, add to the small but growing evidence that phage application is unlikely to have an impact beyond the target bacterial pathogens they are used to treat.