Phage-dependent alteration of rhizosphere microbiota in tomato plants

Bacteriophages (phages) that infect bacterial pathogens are an alternative means of controlling bacterial diseases in humans, animals, and plants. However, the effects of targeted phage therapy on indigenous microbial community has not been fully understood. In this study, we hypothesized that phages infecting plant pathogenic bacteria play a role in modulating the microbial community in the plant rhizosphere. To explore this, we used the soil-borne plant bacterial pathogen Ralstonia pseudosolanacearum as the host bacterium and its phages as a model system in the tomato rhizosphere. The effect of phages on microbiota was compared using a narrow host range phage RpY1, and a combination of two phages (RpY2 and RpT1, termed the phage combo) with a broad host range, under the natural rhizosphere microbiota of tomato plants. Both RpY1 and phage combo altered the tomato rhizosphere microbiota. The phage combo displayed phage effects mostly in the presence of R. pseudosolanacearum. However, RpY1 affected the rhizosphere microbiota even in the absence of the host bacterium. The effect of phage RpY1 on the microbiota was further investigated in the tomato rhizosphere using a synthetic community (SynCom) mimicking the natural tomato rhizosphere microbiota. Phage RpY1 affected the microbial community structure of SynCom in the tomato rhizosphere in the absence of the host bacterium. The analyses of natural microbiota and SynCom in the tomato rhizosphere indicated an indirect effect of phage RpY1 on the microbiota. This study suggests that phage application modulates indigenous microbiota through unknown interactions with non-host bacterial members in the plant rhizosphere.