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Diverse and abundant phages exploit conjugative plasmids

Author

Listed:
  • Natalia Quinones-Olvera

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School)

  • Siân V. Owen

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School)

  • Lucy M. McCully

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School)

  • Maximillian G. Marin

    (Harvard Medical School)

  • Eleanor A. Rand

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School)

  • Alice C. Fan

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School
    Boston University)

  • Oluremi J. Martins Dosumu

    (Harvard Medical School
    Roxbury Community College)

  • Kay Paul

    (Harvard Medical School
    Roxbury Community College)

  • Cleotilde E. Sanchez Castaño

    (Harvard Medical School
    Roxbury Community College)

  • Rachel Petherbridge

    (Harvard Medical School)

  • Jillian S. Paull

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Michael Baym

    (Harvard Medical School
    Harvard Medical School
    Harvard Medical School
    Broad Institute of MIT and Harvard)

Abstract

Phages exert profound evolutionary pressure on bacteria by interacting with receptors on the cell surface to initiate infection. While the majority of phages use chromosomally encoded cell surface structures as receptors, plasmid-dependent phages exploit plasmid-encoded conjugation proteins, making their host range dependent on horizontal transfer of the plasmid. Despite their unique biology and biotechnological significance, only a small number of plasmid-dependent phages have been characterized. Here we systematically search for new plasmid-dependent phages targeting IncP and IncF plasmids using a targeted discovery platform, and find that they are common and abundant in wastewater, and largely unexplored in terms of their genetic diversity. Plasmid-dependent phages are enriched in non-canonical types of phages, and all but one of the 65 phages we isolated were non-tailed, and members of the lipid-containing tectiviruses, ssDNA filamentous phages or ssRNA phages. We show that plasmid-dependent tectiviruses exhibit profound differences in their host range which is associated with variation in the phage holin protein. Despite their relatively high abundance in wastewater, plasmid-dependent tectiviruses are missed by metaviromic analyses, underscoring the continued importance of culture-based phage discovery. Finally, we identify a tailed phage dependent on the IncF plasmid, and find related structural genes in phages that use the orthogonal type 4 pilus as a receptor, highlighting the evolutionarily promiscuous use of these distinct contractile structures by multiple groups of phages. Taken together, these results indicate plasmid-dependent phages play an under-appreciated evolutionary role in constraining horizontal gene transfer via conjugative plasmids.

Suggested Citation

  • Natalia Quinones-Olvera & Siân V. Owen & Lucy M. McCully & Maximillian G. Marin & Eleanor A. Rand & Alice C. Fan & Oluremi J. Martins Dosumu & Kay Paul & Cleotilde E. Sanchez Castaño & Rachel Petherbr, 2024. "Diverse and abundant phages exploit conjugative plasmids," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47416-z
    DOI: 10.1038/s41467-024-47416-z
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    References listed on IDEAS

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    1. Florian Tesson & Alexandre Hervé & Ernest Mordret & Marie Touchon & Camille d’Humières & Jean Cury & Aude Bernheim, 2022. "Systematic and quantitative view of the antiviral arsenal of prokaryotes," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Francisco Martinez-Hernandez & Oscar Fornas & Monica Lluesma Gomez & Benjamin Bolduc & Maria Jose de la Cruz Peña & Joaquín Martínez Martínez & Josefa Anton & Josep M. Gasol & Riccardo Rosselli & Fran, 2017. "Single-virus genomics reveals hidden cosmopolitan and abundant viruses," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    3. Robert C. Edgar & Brie Taylor & Victor Lin & Tomer Altman & Pierre Barbera & Dmitry Meleshko & Dan Lohr & Gherman Novakovsky & Benjamin Buchfink & Basem Al-Shayeb & Jillian F. Banfield & Marcos Peña &, 2022. "Petabase-scale sequence alignment catalyses viral discovery," Nature, Nature, vol. 602(7895), pages 142-147, February.
    4. Kathryn M. Kauffman & Fatima A. Hussain & Joy Yang & Philip Arevalo & Julia M. Brown & William K. Chang & David VanInsberghe & Joseph Elsherbini & Radhey S. Sharma & Michael B. Cutler & Libusha Kelly , 2018. "A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria," Nature, Nature, vol. 554(7690), pages 118-122, February.
    5. Yang Huang & Hui Sun & Shuzhen Wei & Lanlan Cai & Liqin Liu & Yanan Jiang & Jiabao Xin & Zhenqin Chen & Yuqiong Que & Zhibo Kong & Tingting Li & Hai Yu & Jun Zhang & Ying Gu & Qingbing Zheng & Shaowei, 2023. "Structure and proposed DNA delivery mechanism of a marine roseophage," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
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