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Comparative genomic analysis of dwarf Vibrio myoviruses defines a conserved gene cluster for successful phage infection

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Abstract

Tailed bacteriophages have been at the center of attention, not only for their ability to infect and kill pathogenic bacteria but also due to their peculiar and intriguing complex contractile tail structure. Tailed bacteriophages with contractile tails are known to have a Myoviridae morphotype and are members of the order Caudovirales. Large bacteriophages with a genome larger than 150 kbp have been studied for their ability to use multiple infection and lysis strategies to replicate more efficiently. On the other hand, smaller bacteriophages with fewer genes are represented in the GenBank database in greater numbers, and have several genes with unknown function. Isolation and molecular characterization of a newly reported bacteriophage named Athena1 revealed that it is a strongly lytic bacteriophage with a genome size of 39,826 bp. This prompted us to perform a comparative genomic analysis of Vibrio myoviruses with a genome size of no more than 50 kbp. The results revealed a pattern of genomic organization that includes sets of genes responsible for virion morphogenesis, replication/recombination of DNA, and lysis/lysogeny switching. By studying phylogenetic gene markers, we were able to draw conclusions about evolutionary events that shaped the genomic mosaicism of these phages, pinpointing the importance of a conserved organization of the genomic region encoding the baseplate protein for successful infection of Gram-negative bacteria. In addition, we propose the creation of new genera for dwarf Vibrio myoviruses. Comparative genomics of phages infecting aquatic bacteria could provide information that is useful for combating fish pathogens in aquaculture, using novel strategies.

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Availability of data and material

The genome sequence of bacteriophage Athena1 is available in the GenBank database under the accession number MG640035. All raw data presented in the manuscript are available upon request.

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Acknowledgments

We would like to thank Assistant Professor Gerasimos Daras for assisting with PhageTerm software analysis.

Funding

This research was co-financed by Greece and the European Union (European Social Fund- ESF) through the Operational Programme "Human Resources Development, Education and Lifelong Learning" in the context of the project “Reinforcement of Postdoctoral Researchers—2nd Cycle” (MIS-5033021), implemented by the State Scholarships Foundation (ΙΚΥ).

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Authors and Affiliations

  1. Laboratory of Molecular Biology, Department of Biotechnology, School of Applied Biology and Biotechnology, Agricultural University of Athens, Athens, Greece

    Dimitrios Skliros, Efthymios Karpouzis, Chrysanthi Kalloniati & Emmanouil Flemetakis

  2. Institute of Marine Biology, Biotechnology, and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Crete, Greece

    Pantelis Katharios

  3. EU-CONEXUS European University, Athens, Greece

    Emmanouil Flemetakis

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  1. Dimitrios Skliros
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  2. Efthymios Karpouzis
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  4. Pantelis Katharios
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  5. Emmanouil Flemetakis
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Contributions

DS and EF acquired funding. EF, DS and EK conceived the study. DS performed DNA extraction. DS and EK performed phage bioinformatic analysis and wrote the manuscript. PK assisted in TEM photography. PK and CK assisted in data curation. All authors critically reviewed the manuscript, commented on the final draft, and approved the version to be published.

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Correspondence to Emmanouil Flemetakis.

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705_2021_5340_MOESM3_ESM.docx

Supplementary Table S1 Coding DNA products of newly reported bacteriophage Athena1, including their protein_id and presence or absence of protein products in Vibrio phage VBM1 and reference phage PLPE (DOCX 16 KB)

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Skliros, D., Karpouzis, E., Kalloniati, C. et al. Comparative genomic analysis of dwarf Vibrio myoviruses defines a conserved gene cluster for successful phage infection. Arch Virol 167, 501–516 (2022). https://doi.org/10.1007/s00705-021-05340-3

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