Abstract
Viruses influence the ecology and evolutionary trajectory of microbial communities. Yet our understanding of their roles in ecosystems is limited by the paucity of model systems available for hypothesis generation and testing. Further, virology is limited by the lack of a broadly accepted conceptual framework to classify viral diversity into evolutionary and ecologically cohesive units. Here, we introduce genomes, structural proteomes, and quantitative host range data for eight Pseudoalteromonas phages isolated from Helgoland (North Sea, Germany) and use these data to advance a genome-based viral operational taxonomic unit (OTU) definition. These viruses represent five new genera and inform 498 unaffiliated or unannotated protein clusters (PCs) from global virus metagenomes. In a comparison of previously sequenced Pseudoalteromonas phage isolates (n = 7) and predicted prophages (n = 31), the eight phages are unique. They share a genus with only one other isolate, Pseudoalteromonas podophage RIO-1 (East Sea, South Korea) and two Pseudoalteromonas prophages. Mass-spectrometry of purified viral particles identified 12–20 structural proteins per phage. When combined with 3-D structural predictions, these data led to the functional characterization of five previously unidentified major capsid proteins. Protein functional predictions revealed mechanisms for hijacking host metabolism and resources. Further, they uncovered a hybrid sipho-myovirus that encodes genes for Mu-like infection rarely described in ocean systems. Finally, we used these data to evaluate a recently introduced definition for virus populations that requires members of the same population to have >95% average nucleotide identity across at least 80% of their genes. Using physiological traits and genomics, we proposed a conceptual model for a viral OTU definition that captures evolutionarily cohesive and ecologically distinct units. In this trait-based framework, sensitive hosts are considered viral niches, while host ranges and infection efficiencies are tracked as viral traits. Quantitative host range assays revealed conserved traits within virus OTUs that break down between OTUs, suggesting the defined units capture niche and fitness differentiation. Together these analyses provide a foundation for model system-based hypothesis testing that will improve our understanding of marine copiotrophs, as well as phage–host interactions on the ocean particles and aggregates where Pseudoalteromonas thrive.
Highlights
Microbes and their metabolic outputs impact diverse ecosystem functions (Falkowski et al, 2008) and viruses tune these microbial metabolisms through mortality, horizontal gene transfer, and host metabolic reprogramming (Fuhrman, 1999; Wommack and Colwell, 2000; Suttle, 2007; Breitbart, 2012; Brum and Sullivan, 2015)
These recent reports highlight the need to revisit decades-old hypotheses about particle-adsorbed viruses (Proctor and Fuhrman, 1991). They invite questions, such as what is the impact of sinking particle microcosms on virus and host biogeography, phage–host co-evolution, and predator–prey infection dynamics? And in turn, what are the impacts of these viral processes on the sinking rates of ocean particles and thereby the efficiency of the global biological carbon pump?
At t = 0, the number of total viruses was quantified via plaque-forming units (PFUs) to determine the number of phages that contributed to subsequent infections
Summary
Microbes and their metabolic outputs impact diverse ecosystem functions (Falkowski et al, 2008) and viruses tune these microbial metabolisms through mortality, horizontal gene transfer, and host metabolic reprogramming (Fuhrman, 1999; Wommack and Colwell, 2000; Suttle, 2007; Breitbart, 2012; Brum and Sullivan, 2015). A recent study that examined the coupling between omics-based plankton community structure and surface ocean carbon export found that viruses are the best predictors of ocean carbon flux (Guidi et al, 2016) These recent reports highlight the need to revisit decades-old hypotheses about particle-adsorbed viruses (Proctor and Fuhrman, 1991). We hypothesized that if the currently proposed population (or phage OTU) definition were meaningful (i.e., capture evolutionarily and ecologically cohesive populations; Polz et al, 2006), trait-based differentiation would arise consistent with these genome-based boundaries These analyses provide a baseline for understanding the ecological and evolutionary impact of viruses infecting Pseudoalteromonas, a model ocean particle-associated copiotrophic microbe
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