IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44965-1.html
   My bibliography  Save this article

Phage-inducible chromosomal minimalist islands (PICMIs), a novel family of small marine satellites of virulent phages

Author

Listed:
  • Rubén Barcia-Cruz

    (Station Biologique de Roscoff
    Universidade de Santiago de Compostela)

  • David Goudenège

    (Station Biologique de Roscoff
    ZI de la Pointe du Diable)

  • Jorge A. Moura de Sousa

    (Microbial Evolutionary Genomics)

  • Damien Piel

    (Station Biologique de Roscoff
    ZI de la Pointe du Diable)

  • Martial Marbouty

    (Organization and Dynamics of Viral Genomes Group, CNRS UMR 3525)

  • Eduardo P. C. Rocha

    (Microbial Evolutionary Genomics)

  • Frédérique Roux

    (Station Biologique de Roscoff
    ZI de la Pointe du Diable
    Université de Montréal)

Abstract

Phage satellites are bacterial genetic elements that co-opt phage machinery for their own dissemination. Here we identify a family of satellites, named Phage-Inducible Chromosomal Minimalist Islands (PICMIs), that are broadly distributed in marine bacteria of the family Vibrionaceae. A typical PICMI is characterized by reduced gene content, does not encode genes for capsid remodelling, and packages its DNA as a concatemer. PICMIs integrate in the bacterial host genome next to the fis regulator, and encode three core proteins necessary for excision and replication. PICMIs are dependent on virulent phage particles to spread to other bacteria, and protect their hosts from other competitive phages without interfering with their helper phage. Thus, our work broadens our understanding of phage satellites and narrows down the minimal number of functions necessary to hijack a tailed phage.

Suggested Citation

  • Rubén Barcia-Cruz & David Goudenège & Jorge A. Moura de Sousa & Damien Piel & Martial Marbouty & Eduardo P. C. Rocha & Frédérique Roux, 2024. "Phage-inducible chromosomal minimalist islands (PICMIs), a novel family of small marine satellites of virulent phages," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44965-1
    DOI: 10.1038/s41467-024-44965-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44965-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44965-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. Ying Chen & Fan Nie & Shang-Qian Xie & Ying-Feng Zheng & Qi Dai & Thomas Bray & Yao-Xin Wang & Jian-Feng Xing & Zhi-Jian Huang & De-Peng Wang & Li-Juan He & Feng Luo & Jian-Xin Wang & Yi-Zhi Liu & Chu, 2021. "Efficient assembly of nanopore reads via highly accurate and intact error correction," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    3. Pierrick Moreau & Axel Cournac & Gianna Aurora Palumbo & Martial Marbouty & Shogofa Mortaza & Agnes Thierry & Stefano Cairo & Marc Lavigne & Romain Koszul & Christine Neuveut, 2018. "Tridimensional infiltration of DNA viruses into the host genome shows preferential contact with active chromatin," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Kathryn M. Kauffman & William K. Chang & Julia M. Brown & Fatima A. Hussain & Joy Yang & Martin F. Polz & Libusha Kelly, 2022. "Resolving the structure of phage–bacteria interactions in the context of natural diversity," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    5. Martin Steinegger & Johannes Söding, 2018. "Clustering huge protein sequence sets in linear time," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    6. Cyril Matthey-Doret & Lyam Baudry & Axel Breuer & Rémi Montagne & Nadège Guiglielmoni & Vittore Scolari & Etienne Jean & Arnaud Campeas & Philippe Henri Chanut & Edgar Oriol & Adrien Méot & Laurent Po, 2020. "Computer vision for pattern detection in chromosome contact maps," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Peicong Lin & Yumeng Yan & Huanyu Tao & Sheng-You Huang, 2023. "Deep transfer learning for inter-chain contact predictions of transmembrane protein complexes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Ana Paula Zotta Mota & Georgios D. Koutsovoulos & Laetitia Perfus-Barbeoch & Evelin Despot-Slade & Karine Labadie & Jean-Marc Aury & Karine Robbe-Sermesant & Marc Bailly-Bechet & Caroline Belser & Art, 2024. "Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Dimitri Boeckaerts & Michiel Stock & Celia Ferriol-González & Jesús Oteo-Iglesias & Rafael Sanjuán & Pilar Domingo-Calap & Bernard Baets & Yves Briers, 2024. "Prediction of Klebsiella phage-host specificity at the strain level," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    4. Danielle Miller & Adi Stern & David Burstein, 2022. "Deciphering microbial gene function using natural language processing," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Kunpeng Li & Peng Xu & Jinpeng Wang & Xin Yi & Yuannian Jiao, 2023. "Identification of errors in draft genome assemblies at single-nucleotide resolution for quality assessment and improvement," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Pedro Leão & Mary E. Little & Kathryn E. Appler & Daphne Sahaya & Emily Aguilar-Pine & Kathryn Currie & Ilya J. Finkelstein & Valerie Anda & Brett J. Baker, 2024. "Asgard archaea defense systems and their roles in the origin of eukaryotic immunity," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    7. Lingchen He & Laura Miguel-Romero & Jonasz B. Patkowski & Nasser Alqurainy & Eduardo P. C. Rocha & Tiago R. D. Costa & Alfred Fillol-Salom & José R. Penadés, 2024. "Tail assembly interference is a common strategy in bacterial antiviral defenses," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Tom J. Arrowsmith & Xibing Xu & Shangze Xu & Ben Usher & Peter Stokes & Megan Guest & Agnieszka K. Bronowska & Pierre Genevaux & Tim R. Blower, 2024. "Inducible auto-phosphorylation regulates a widespread family of nucleotidyltransferase toxins," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Yiqian Duan & Célio Dias Santos-Júnior & Thomas Sebastian Schmidt & Anthony Fullam & Breno L. S. Almeida & Chengkai Zhu & Michael Kuhn & Xing-Ming Zhao & Peer Bork & Luis Pedro Coelho, 2024. "A catalog of small proteins from the global microbiome," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Carolien Bastiaanssen & Pilar Bobadilla Ugarte & Kijun Kim & Giada Finocchio & Yanlei Feng & Todd A. Anzelon & Stephan Köstlbacher & Daniel Tamarit & Thijs J. G. Ettema & Martin Jinek & Ian J. MacRae , 2024. "RNA-guided RNA silencing by an Asgard archaeal Argonaute," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    11. Angelina Beavogui & Auriane Lacroix & Nicolas Wiart & Julie Poulain & Tom O. Delmont & Lucas Paoli & Patrick Wincker & Pedro H. Oliveira, 2024. "The defensome of complex bacterial communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Shao-Ming Gao & Han-Lan Fei & Qi Li & Li-Ying Lan & Li-Nan Huang & Peng-Fei Fan, 2024. "Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    13. Jan D. Brüwer & Chandni Sidhu & Yanlin Zhao & Andreas Eich & Leonard Rößler & Luis H. Orellana & Bernhard M. Fuchs, 2024. "Globally occurring pelagiphage infections create ribosome-deprived cells," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    14. Mirjana Domazet-Lošo & Tin Široki & Korina Šimičević & Tomislav Domazet-Lošo, 2024. "Macroevolutionary dynamics of gene family gain and loss along multicellular eukaryotic lineages," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    15. Patrick Bryant & Frank Noé, 2024. "Structure prediction of alternative protein conformations," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    16. David Moi & Shunsuke Nishio & Xiaohui Li & Clari Valansi & Mauricio Langleib & Nicolas G. Brukman & Kateryna Flyak & Christophe Dessimoz & Daniele de Sanctis & Kathryn Tunyasuvunakool & John Jumper & , 2022. "Discovery of archaeal fusexins homologous to eukaryotic HAP2/GCS1 gamete fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    17. Motaher Hossain & Barbaros Aslan & Asma Hatoum-Aslan, 2024. "Tandem mobilization of anti-phage defenses alongside SCCmec elements in staphylococci," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. Jacques Serizay & Cyril Matthey-Doret & Amaury Bignaud & Lyam Baudry & Romain Koszul, 2024. "Orchestrating chromosome conformation capture analysis with Bioconductor," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    19. Yanlin Zhang & Mathieu Blanchette, 2022. "Reference panel guided topological structure annotation of Hi-C data," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    20. Olivier Messina & Flavien Raynal & Julian Gurgo & Jean-Bernard Fiche & Vera Pancaldi & Marcelo Nollmann, 2023. "3D chromatin interactions involving Drosophila insulators are infrequent but preferential and arise before TADs and transcription," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44965-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.