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Infection and Genomic Properties of Single- and Double-Stranded DNA Cellulophaga Phages

Journal Article · · Viruses
DOI:https://doi.org/10.3390/v17030365· OSTI ID:2526315

Bacterial viruses (phages) are abundant and ecologically impactful, but laboratory-based experimental model systems vastly under-represent known phage diversity, particularly for ssDNA phages. Here, we characterize the genomes and infection properties of two unrelated marine flavophages—ssDNA generalist phage phi18:4 (6.5 Kbp) and dsDNA specialist phage phi18:1 (39.2 Kbp)—when infecting the same Cellulophaga baltica strain #18 (Cba18), of the class Flavobacteriia. Phage phi18:4 belongs to a new family of ssDNA phages, has an internal lipid membrane, and its genome encodes primarily structural proteins, as well as a DNA replication protein common to ssDNA phages and a unique lysis protein. Phage phi18:1 is a siphovirus that encodes several virulence genes, despite not having a known temperate lifestyle, a CAZy enzyme likely for regulatory purposes, and four DNA methyltransferases dispersed throughout the genome that suggest both host modulation and phage DNA protection against host restriction. Physiologically, ssDNA phage phi18:4 has a shorter latent period and smaller burst size than dsDNA phage phi18:1, and both phages efficiently infect this host. These results help augment the diversity of characterized environmental phage–host model systems by studying infections of genomically diverse phages (ssDNA vs. dsDNA) on the same host.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0020173; SC0023307
OSTI ID:
2526315
Journal Information:
Viruses, Journal Name: Viruses Journal Issue: 3 Vol. 17; ISSN VIRUBR; ISSN 1999-4915
Publisher:
MDPI AGCopyright Statement
Country of Publication:
Switzerland
Language:
English

References (101)

Phage Classification and Characterization book January 2009
The significance of viruses to mortality in aquatic microbial communities journal September 1994
The evolution of phage lysis timing journal September 1996
Selection for bacteriophage latent period length by bacterial density: A theoretical examination journal September 1989
ssDNA viruses: key players in global virome journal March 2019
Cloning and sequencing of the glucosyl transferase-encoding gene from converting bacteriophage X (SFX) of Shigellaflexneri journal July 1993
Metagenomics in Virology book January 2021
Replication and Expression Strategies of Viruses book January 2018
Endo-N-acetyl-β-D-glucosaminidases and their potential substrates : structure/function relationships journal October 1997
Comparison of Lipid-Containing Bacterial and Archaeal Viruses book January 2015
Marine DNA Viral Macro- and Microdiversity from Pole to Pole journal May 2019
Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses journal October 2013
Ecology of prokaryotic viruses journal May 2004
The highly efficient T7 RNA polymerase: A wonder macromolecule in biological realm journal October 2018
Here a virus, there a virus, everywhere the same virus? journal June 2005
Virocell Metabolism: Metabolic Innovations During Host–Virus Interactions in the Ocean journal October 2016
Genetic details, optimization and phage life histories journal February 2004
The genome of AR9, a giant transducing Bacillus phage encoding two multisubunit RNA polymerases journal August 2016
Marine viruses and their biogeochemical and ecological effects journal June 1999
Nucleotide sequence of bacteriophage φX174 DNA journal February 1977
High abundance of viruses found in aquatic environments journal August 1989
The virocell concept and environmental microbiology journal October 2012
Ecology of marine Bacteroidetes: a comparative genomics approach journal January 2013
Previously unknown and highly divergent ssDNA viruses populate the oceans journal July 2013
Transcriptome dynamics of a broad host-range cyanophage and its hosts journal December 2015
Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus journal May 2016
Lysogeny in nature: mechanisms, impact and ecology of temperate phages journal March 2017
Viruses in the sea journal September 2005
Plankton networks driving carbon export in the oligotrophic ocean journal February 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses journal September 2016
Marine viruses — major players in the global ecosystem journal October 2007
Ecology and exploration of the rare biosphere journal March 2015
Multiple mechanisms drive phage infection efficiency in nearly identical hosts journal March 2018
Phage-specific metabolic reprogramming of virocells journal January 2020
Highly diverse flavobacterial phages isolated from North Sea spring blooms journal September 2021
Cryo-EM structure of ssDNA bacteriophage ΦCjT23 provides insight into early virus evolution journal December 2022
Phage puppet masters of the marine microbial realm journal June 2018
Microbial metabolites in the marine carbon cycle journal April 2022
Metabolites from intact phage-infected Synechococcus chemotactically attract heterotrophic marine bacteria journal November 2024
Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems journal November 2019
Revisiting the rules of life for viruses of microorganisms journal March 2021
Predicting global distributions of eukaryotic plankton communities from satellite data journal September 2023
Mechanism of bacteriophage SfII‐mediated serotype conversion in Shigella flexneri journal December 1997
Twelve previously unknown phage genera are ubiquitous in global oceans journal July 2013
Virus found in a boreal lake links ssDNA and dsDNA viruses journal July 2017
The biomass distribution on Earth journal May 2018
Transfer RNA coded by the T4 bacteriophage genome. journal September 1968
A separate editing exonuclease for DNA replication: the epsilon subunit of Escherichia coli DNA polymerase III holoenzyme. journal December 1984
Prokaryotes: The unseen majority journal June 1998
Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage journal March 1999
Resource-Limited Growth, Competition, and Predation: A Model and Experimental Studies with Bacteria and Bacteriophage journal January 1977
clinker & clustermap.js: automatic generation of gene cluster comparison figures journal January 2021
Pharokka: a fast scalable bacteriophage annotation tool journal December 2022
Easyfig: a genome comparison visualizer journal January 2011
InterProScan 5: genome-scale protein function classification journal January 2014
ViPTree: the viral proteomic tree server journal March 2017
Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology journal February 2016
Environment-specific virocell metabolic reprogramming journal January 2024
Cloning and sequencing of the genes of β-glucosyl-HMC-α-glucosyl-transferases of bacteriophages T2 and T6 journal January 1993
DRAM for distilling microbial metabolism to automate the curation of microbiome function journal August 2020
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
Bacteriophage DNA glucosylation impairs target DNA binding by type I and II but not by type V CRISPR–Cas effector complexes journal December 2017
ICTV Virus Taxonomy Profile: Finnlakeviridae journal September 2020
Glycosyltransferases encoded by viruses journal October 2004
Contrasting genomic patterns and infection strategies of two co-existing B acteroidetes podovirus genera : Infection strategies of co-existing podoviruse journal February 2014
Variably lytic infection dynamics of large B acteroidetes podovirus phi38:1 against two C ellulophaga baltica host strains : Infection dynamics of journal September 2015
Large-scale maps of variable infection efficiencies in aquatic Bacteroidetes phage-host model systems : Variable phage-host infection interactions journal June 2016
Polysaccharide degradation by the Bacteroidetes: mechanisms and nomenclature journal June 2021
Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter journal December 2006
Testing Optimality with Experimental Evolution: Lysis time in a Bacteriophage journal July 2007
Bacteriophage replication modules journal May 2006
Diversity and ecological footprint of Global Ocean RNA viruses journal June 2022
Large Variabilities in Host Strain Susceptibility and Phage Host Range Govern Interactions between Lytic Marine Phages and Their Flavobacterium Hosts journal August 2007
Bacteriophage Orphan DNA Methyltransferases: Insights from Their Bacterial Origin, Function, and Occurrence journal December 2013
Cultivated Single-Stranded DNA Phages That Infect Marine Bacteroidetes Prove Difficult To Detect with DNA-Binding Stains journal December 2011
Bacteriophage Latent-Period Evolution as a Response to Resource Availability journal September 2001
Are There 10 31 Virus Particles on Earth, or More, or Fewer? journal February 2020
Peptidoglycan-Hydrolyzing Activity of the FlgJ Protein, Essential for Flagellar Rod Formation inSalmonella typhimurium journal March 1999
Penetration of Membrane-Containing Double-Stranded-DNA Bacteriophage PM2 intoPseudoalteromonasHosts journal August 2004
Global Organization and Proposed Megataxonomy of the Virus World journal March 2020
Virioplankton: Viruses in Aquatic Ecosystems journal March 2000
Organizing the Global Diversity of Microviruses journal June 2022
The Rare Bacterial Biosphere journal January 2012
Hostile Takeover: How Viruses Reprogram Prokaryotic Metabolism journal October 2021
Diverse Antiphage Defenses Are Widespread Among Prophages and Mobile Genetic Elements journal September 2024
BLAST+: architecture and applications journal January 2009
Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes journal February 2020
Host-hijacking and planktonic piracy: how phages command the microbial high seas journal February 2019
Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans journal August 2024
The Marine Viromes of Four Oceanic Regions journal November 2006
Viral infection in the ocean—A journey across scales journal January 2023
Lysis Timing and Bacteriophage Fitness journal October 2005
Emerging Aspects of Jumbo Bacteriophages journal November 2021
Role of Bacteriophage-Encoded Exotoxins in the Evolution of Bacterial Pathogens journal November 2011
Viruses and Nutrient Cycles in the Sea journal October 1999
Whole-genome analysis showed the promotion of genetic diversity and coevolution in Staphylococcus aureus lytic bacteriophages and their hosts mediated by prophages via worldwide recombination events journal March 2023
Fighting Fire with Fire: Phage Potential for the Treatment of E. coli O157 Infection journal November 2018
RNA and Single-Stranded DNA Phages: Unveiling the Promise from the Underexplored World of Viruses journal December 2023
Half a Century of Research on Membrane-Containing Bacteriophages: Bringing New Concepts to Modern Virology journal January 2019
Whole-Genome Analysis Reveals That Bacteriophages Promote Environmental Adaptation of Staphylococcus aureus via Gene Exchange, Acquisition, and Loss journal May 2022
Importance of prophages to evolution and virulence of bacterial pathogens journal July 2013

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