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A Novel Phage Infecting Alteromonas Represents a Distinct Group of Siphophages Infecting Diverse Aquatic Copiotrophs.

ABSTRACT: Bacteriophages play critical roles in impacting microbial community succession both ecologically and evolutionarily. Although the majority of phage genetic diversity has been increasingly unveiled, phages infecting members of the ecologically important genus Alteromonas remain poorly understood. Here, we present a comprehensive analysis of a newly isolated alterophage, vB_AcoS-R7M (R7M), to characterize its life cycle traits, genomic features, and putative evolutionary origin. R7M harbors abundant genes identified as host-like auxiliary metabolic genes facilitating viral propagation. Genomic analysis suggested that R7M is distinct from currently known alterophages. Interestingly, R7M was found to share a set of similar characteristics with a number of siphophages infecting diverse aquatic opportunistic copiotrophs. We therefore proposed the creation of one new subfamily (Queuovirinae) to group with these evolutionarily related phages. Notably, tail genes were less likely to be shared among them, and baseplate-related genes varied the most. In-depth analyses indicated that R7M has replaced its distal tail with a Rhodobacter capsulatus gene transfer agent (RcGTA)-like baseplate and further acquired a putative receptor interaction site targeting Alteromonas. These findings suggest that horizontal exchanges of viral tail adsorption apparatuses are widespread and vital for phages to hunt new hosts and to adapt to new niches. IMPORTANCE The evolution and ecology of phages infecting members of Alteromonas, a marine opportunistic genus that is widely distributed and of great ecological significance, remain poorly understood. The present study integrates physiological and genomic evidence to characterize the properties and putative phage-host interactions of a newly isolated Alteromonas phage, vB_AcoS-R7M (R7M). A taxonomic study reveals close evolutionary relationships among R7M and a number of siphophages infecting various aquatic copiotrophs. Their similar head morphology and overall genetic framework suggest their putative common ancestry and the grouping of a new viral subfamily. However, their major difference lies in the viral tail adsorption apparatuses and the horizontal exchanges of which possibly account for variations in host specificity. These findings outline an evolutionary scenario for the emergence of diverse viral lineages of a shared genetic pool and give insights into the genetics and ecology of viral host jumps.

SUBMITTER: Ma R

PROVIDER: S-EPMC8265664 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Phages are generally described as species specific or even strain specific, 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 isolated and characterized a novel group of six promiscuous phages, named Atoyac, existing in rivers and sewage by using a diverse collection of over 600 bacteria retrieved from the same environments as potential hosts. These podophages isolated from different regions in Mexico display a remarkably broad host range, infecting bacteria from six genera: Aeromonas, Pseudomonas, Yersinia, Hafnia, Escherichia, and Serratia Atoyac phage genomes are ∼42 kb long and highly similar to each other, but not to those currently available in genome and metagenome public databases. Detailed comparison of the phages' efficiency of plating (EOP) revealed variation among 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 efficiency of plaque production is highly dynamic and tends toward optimization in hosts rendering low plaque formation. However, adaptation to distinct hosts differed between similar phages; whereas one phage optimized its EOP in all tested hosts, the other reduced plaque production in one host, suggesting that propagation in multiple bacteria may be key to maintain promiscuity in some viruses. Our study expands our knowledge of the virosphere and uncovers bacterium-phage interactions overlooked in natural systems.IMPORTANCE In natural environments, phages coexist and interact with a broad variety of bacteria, posing a conundrum for narrow-host-range phage 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 bacterium-phage interactions and their impact on 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.

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A Novel Phage Infecting Alteromonas Represents a Distinct Group of Siphophages Infecting Diverse Aquatic Copiotrophs.

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