Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept
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...
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doaj-24b6d93145284b8cb7a770b6e38546ea2020-11-24T21:36:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-07-01810.3389/fmicb.2017.01241262926Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU ConceptMelissa B. Duhaime0Natalie Solonenko1Simon Roux2Nathan C. Verberkmoes3Antje Wichels4Matthew B. Sullivan5Matthew B. Sullivan6Department of Ecology and Evolutionary Biology, University of Michigan, Ann ArborMI, United StatesDepartment of Microbiology, The Ohio State University, ColumbusOH, United StatesDepartment of Microbiology, The Ohio State University, ColumbusOH, United StatesDepartment of Biological Sciences, Border Biomedical Research Center, University of Texas at El Paso, El PasoTX, United StatesBiologische Anstalt Helgoland, Alfred Wegener Institute, Helmholtz Centre for Polar and Marine ResearchHelgoland, GermanyDepartment of Microbiology, The Ohio State University, ColumbusOH, United StatesDepartment of Civil, Environmental, and Geodetic Engineering, The Ohio State University, ColumbusOH, United StatesViruses 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01241/fullphagemarine microbiologyparticle-associatedcomparative genomicsPseudoalteromonas |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Melissa B. Duhaime Natalie Solonenko Simon Roux Nathan C. Verberkmoes Antje Wichels Matthew B. Sullivan Matthew B. Sullivan |
spellingShingle |
Melissa B. Duhaime Natalie Solonenko Simon Roux Nathan C. Verberkmoes Antje Wichels Matthew B. Sullivan Matthew B. Sullivan Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept Frontiers in Microbiology phage marine microbiology particle-associated comparative genomics Pseudoalteromonas |
author_facet |
Melissa B. Duhaime Natalie Solonenko Simon Roux Nathan C. Verberkmoes Antje Wichels Matthew B. Sullivan Matthew B. Sullivan |
author_sort |
Melissa B. Duhaime |
title |
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept |
title_short |
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept |
title_full |
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept |
title_fullStr |
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept |
title_full_unstemmed |
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept |
title_sort |
comparative omics and trait analyses of marine pseudoalteromonas phages advance the phage otu concept |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2017-07-01 |
description |
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. |
topic |
phage marine microbiology particle-associated comparative genomics Pseudoalteromonas |
url |
http://journal.frontiersin.org/article/10.3389/fmicb.2017.01241/full |
work_keys_str_mv |
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