Dynamics of infection in a novel group of promiscuous phages and hosts of multiple bacterial genera retrieved from river communities

Abstract

Phages are generally described as species- or even strain-specific viruses, implying an inherent limitation for some to be maintained and spread in diverse bacterial communities. Moreover, phage isolation and host range determination rarely consider the phage ecological context, likely biasing our notion on phage specificity. Here we identified and characterized a novel group of promiscuous phages existing in rivers by using diverse bacteria isolated from the same samples, and then used this biological system to investigate infection dynamics in distantly related hosts. We assembled a diverse collection of over 600 native bacterial strains and used them to isolate six podophages, named Atoyac, from different geographic origin and capable of infecting six genera in the Gammaproteobacteria. Atoyac phage genomes are highly similar to each other but not to those currently available in the genome and metagenome public databases. Detailed comparison of the phages infectivity in diverse hosts and trough hundreds of interactions revealed variation in plating efficiency amongst bacterial genera, implying a cost associated with infection of distant hosts, and between phages, despite their sequence similarity. We show, through experimental evolution in single or alternate hosts of different genera, that plaque production efficiency is highly dynamic and tends towards optimization in hosts rendering low plaque formation. Complex adaptation outcomes observed in the evolution experiments differed between highly similar phages and suggest that propagation in multiple hosts may be key to maintain promiscuity in some viruses. Our study expands our knowledge of the virosphere and uncovers bacteria-phage interactions overlooked in natural systems. ImportanceIn natural environments, phages co-exist and interact with a broad variety of bacteria, posing a conundrum for narrow-host-range phages maintenance in diverse communities. This context is rarely considered in the study of host-phage interactions, typically focused on narrow-host-range viruses and their infectivity in target bacteria isolated from sources distinct to where the phages were retrieved from. By studying phage-host interactions in bacteria and viruses isolated from river microbial communities, we show that novel phages with promiscuous host range encompassing multiple bacterial genera can be found in the environment. Assessment of hundreds of interactions in diverse hosts revealed that similar phages exhibit different infection efficiency and adaptation patterns. Understanding host range is fundamental in our knowledge of bacteria-phage interactions and their impact in microbial communities. The dynamic nature of phage promiscuity revealed in our study has implications in different aspects of phage research such as horizontal gene transfer or phage therapy.