Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

<p>Bacteriophages, viruses that specifically target plant pathogenic bacteria, have emerged as a promising alternative to traditional agrochemicals. However, it remains unclear how phages should be applied to achieve efficient pathogen biocontrol, and to what extent their efficacy is shaped by indirect interactions with the resident microbiota. Here we tested if the phage biocontrol efficacy of <em>Ralstonia solanacearum</em> phytopathogenic bacterium can be improved by increasing the phage cocktail application frequency, and if the phage efficacy is affected by pathogen-suppressing bacteria already present in the rhizosphere. We find that increasing phage application frequency improves <em>R. solanacearum</em> density control, leading to a clear reduction in bacterial wilt disease in both greenhouse and field experiments with tomatoes. The high phage application frequency also increased the diversity of resident rhizosphere microbiota and enriched several bacterial taxa that were associated with the reduction in pathogen densities. Interestingly, these taxa often belonged to <em>Actinobacteria</em> known for antibiotics production and soil suppressiveness. To test if they could have had secondary effects on <em>R. solanacearum </em>biocontrol, we isolated Actinobacteria from <em>Nocardia</em> and <em>Streptomyces</em> genera and tested their suppressiveness to the pathogen <em>in vitro</em> and <em>in planta</em>. We found that these taxa could clearly inhibit <em>R. solanacearum</em> growth and constrain bacterial wilt disease, especially when combined with the phage cocktail. Together, our findings unravel an undiscovered benefit of phage therapy, where phages trigger a second line of defense by the pathogen-suppressing bacteria that already exist in resident microbial communities.</p>