Dataset Information

Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept.

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.

SUBMITTER: Duhaime MB

PROVIDER: S-EPMC5498523 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Comparative Omics and Trait Analyses of Marine <i>Pseudoalteromonas</i> Phages Advance the Phage OTU Concept.

Duhaime Melissa B MB Solonenko Natalie N Roux Simon S Verberkmoes Nathan C NC Wichels Antje A Sullivan Matthew B MB

Frontiers in microbiology 20170706

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 <i>Pseudoalteromo ...[more]

PMID: 28729861

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Project description:Chitin is the most abundant polymer in the marine environment and a nutrient-rich surface for adhering marine bacteria. We have previously shown that chitin can induce the production of antibiotic compounds in Vibrionaceae, suggesting that the discovery of novel bioactive molecules from bacteria can be facilitated by mimicking their natural habitat. The purpose of this study was to determine the glycosyl hydrolase (GH) profiles of strains of the genus Pseudoalteromonas to enable selection of presumed growth substrates and explore possible links to secondary metabolism. Genomic analyses were conducted on 62 pigmented and 95 nonpigmented strains. Analysis of the total GH profiles and multidimensional scaling suggested that the degradation of chitin is a significant trait of pigmented strains, whereas nonpigmented strains seem to be driven toward the degradation of alga-derived carbohydrates. The genomes of all pigmented strains and 40 nonpigmented strains encoded at least one conserved chitin degradation cluster, and chitinolytic activity was phenotypically confirmed. Additionally, the genomes of all pigmented and a few nonpigmented strains encoded chitinases of the rare GH family 19. Pigmented strains devote up to 15% of their genome to secondary metabolism, while for nonpigmented species it was 3% at most. Thus, pigmented Pseudoalteromonas strains have a bioactive potential similar to that of well-known antibiotic producers of the Actinobacteria phylum. Growth on chitin did not measurably enhance the antibacterial activity of the strains; however, we demonstrated a remarkable co-occurrence of chitin degradation and the potential for secondary metabolite production in pigmented Pseudoalteromonas strains. This indicates that chitin and its colonizers of the Pseudoalteromonas genus represent a so far underexplored niche for novel enzymes and bioactive compounds.IMPORTANCE Infectious bacteria are developing and spreading resistance to conventional treatments at a rapid pace. To provide novel potent antimicrobials, we must develop new bioprospecting strategies. Here, we combined in silico and phenotypic approaches to explore the bioactive potential of the marine bacterial genus Pseudoalteromonas We found that pigmented strains in particular represent an untapped resource of secondary metabolites and that they also harbor an elaborate chitinolytic machinery. Furthermore, our analysis showed that chitin is likely a preferred substrate for pigmented species, in contrast to nonpigmented species. Potentially, chitin could facilitate the production of new secondary metabolites in pigmented Pseudoalteromonas strains.

Dataset Information

Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept.

Publications

Comparative Omics and Trait Analyses of Marine <i>Pseudoalteromonas</i> Phages Advance the Phage OTU Concept.

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