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Archaeal DNA-import apparatus is homologous to bacterial conjugation machinery

Author

Listed:
  • Leticia C. Beltran

    (University of Virginia)

  • Virginija Cvirkaite-Krupovic

    (Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit)

  • Jessalyn Miller

    (Emory University)

  • Fengbin Wang

    (University of Virginia
    University of Alabama Birmingham)

  • Mark A. B. Kreutzberger

    (University of Virginia)

  • Jonasz B. Patkowski

    (Imperial College)

  • Tiago R. D. Costa

    (Imperial College)

  • Stefan Schouten

    (NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry)

  • Ilya Levental

    (University of Virginia)

  • Vincent P. Conticello

    (Emory University)

  • Edward H. Egelman

    (University of Virginia)

  • Mart Krupovic

    (Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit)

Abstract

Conjugation is a major mechanism of horizontal gene transfer promoting the spread of antibiotic resistance among human pathogens. It involves establishing a junction between a donor and a recipient cell via an extracellular appendage known as the mating pilus. In bacteria, the conjugation machinery is encoded by plasmids or transposons and typically mediates the transfer of cognate mobile genetic elements. Much less is known about conjugation in archaea. Here, we determine atomic structures by cryo-electron microscopy of three conjugative pili, two from hyperthermophilic archaea (Aeropyrum pernix and Pyrobaculum calidifontis) and one encoded by the Ti plasmid of the bacterium Agrobacterium tumefaciens, and show that the archaeal pili are homologous to bacterial mating pili. However, the archaeal conjugation machinery, known as Ced, has been ‘domesticated’, that is, the genes for the conjugation machinery are encoded on the chromosome rather than on mobile genetic elements, and mediates the transfer of cellular DNA.

Suggested Citation

  • Leticia C. Beltran & Virginija Cvirkaite-Krupovic & Jessalyn Miller & Fengbin Wang & Mark A. B. Kreutzberger & Jonasz B. Patkowski & Tiago R. D. Costa & Stefan Schouten & Ilya Levental & Vincent P. Co, 2023. "Archaeal DNA-import apparatus is homologous to bacterial conjugation machinery," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36349-8
    DOI: 10.1038/s41467-023-36349-8
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Xiangan Liu & Pratick Khara & Matthew L. Baker & Peter J. Christie & Bo Hu, 2022. "Structure of a type IV secretion system core complex encoded by multi-drug resistance F plasmids," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Harry H. Low & Francesca Gubellini & Angel Rivera-Calzada & Nathalie Braun & Sarah Connery & Annick Dujeancourt & Fang Lu & Adam Redzej & Rémi Fronzes & Elena V. Orlova & Gabriel Waksman, 2014. "Structure of a type IV secretion system," Nature, Nature, vol. 508(7497), pages 550-553, April.
    4. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. Xiangan Liu & Pratick Khara & Matthew L. Baker & Peter J. Christie & Bo Hu, 2022. "Author Correction: Structure of a type IV secretion system core complex encoded by multi-drug resistance F plasmids," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
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    Cited by:

    1. Rebecca Conners & Rayén Ignacia León-Quezada & Mathew McLaren & Nicholas J. Bennett & Bertram Daum & Jasna Rakonjac & Vicki A. M. Gold, 2023. "Cryo-electron microscopy of the f1 filamentous phage reveals insights into viral infection and assembly," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Matthew C. Gaines & Shamphavi Sivabalasarma & Michail N. Isupov & Risat Ul Haque & Mathew McLaren & Cyril Hanus & Vicki A. M. Gold & Sonja-Verena Albers & Bertram Daum, 2024. "CryoEM reveals the structure of an archaeal pilus involved in twitching motility," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Jonasz B. Patkowski & Tobias Dahlberg & Himani Amin & Dharmender K. Gahlot & Sukhithasri Vijayrajratnam & Joseph P. Vogel & Matthew S. Francis & Joseph L. Baker & Magnus Andersson & Tiago R. D. Costa, 2023. "The F-pilus biomechanical adaptability accelerates conjugative dissemination of antimicrobial resistance and biofilm formation," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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