IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45351-7.html
   My bibliography  Save this article

Host association and intracellularity evolved multiple times independently in the Rickettsiales

Author

Listed:
  • Michele Castelli

    (University of Pavia)

  • Tiago Nardi

    (University of Pavia)

  • Leandro Gammuto

    (University of Pisa)

  • Greta Bellinzona

    (University of Pavia)

  • Elena Sabaneyeva

    (Saint Petersburg State University)

  • Alexey Potekhin

    (Saint Petersburg State University
    University of Innsbruck)

  • Valentina Serra

    (University of Pisa)

  • Giulio Petroni

    (University of Pisa)

  • Davide Sassera

    (University of Pavia
    IRCCS Policlinico San Matteo)

Abstract

The order Rickettsiales (Alphaproteobacteria) encompasses multiple diverse lineages of host-associated bacteria, including pathogens, reproductive manipulators, and mutualists. Here, in order to understand how intracellularity and host association originated in this order, and whether they are ancestral or convergently evolved characteristics, we built a large and phylogenetically-balanced dataset that includes de novo sequenced genomes and a selection of published genomic and metagenomic assemblies. We perform detailed functional reconstructions that clearly indicates “late” and parallel evolution of obligate host-association in different Rickettsiales lineages. According to the depicted scenario, multiple independent horizontal acquisitions of transporters led to the progressive loss of biosynthesis of nucleotides, amino acids and other metabolites, producing distinct conditions of host-dependence. Each clade experienced a different pattern of evolution of the ancestral arsenal of interaction apparatuses, including development of specialised effectors involved in the lineage-specific mechanisms of host cell adhesion and/or invasion.

Suggested Citation

  • Michele Castelli & Tiago Nardi & Leandro Gammuto & Greta Bellinzona & Elena Sabaneyeva & Alexey Potekhin & Valentina Serra & Giulio Petroni & Davide Sassera, 2024. "Host association and intracellularity evolved multiple times independently in the Rickettsiales," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45351-7
    DOI: 10.1038/s41467-024-45351-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45351-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45351-7?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. Hiroyuki Imachi & Masaru K. Nobu & Nozomi Nakahara & Yuki Morono & Miyuki Ogawara & Yoshihiro Takaki & Yoshinori Takano & Katsuyuki Uematsu & Tetsuro Ikuta & Motoo Ito & Yohei Matsui & Masayuki Miyaza, 2020. "Isolation of an archaeon at the prokaryote–eukaryote interface," Nature, Nature, vol. 577(7791), pages 519-525, January.
    2. Sishuo Wang & Haiwei Luo, 2021. "Dating Alphaproteobacteria evolution with eukaryotic fossils," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    3. Gina M. Borgo & Thomas P. Burke & Cuong J. Tran & Nicholas T. N. Lo & Patrik Engström & Matthew D. Welch, 2022. "A patatin-like phospholipase mediates Rickettsia parkeri escape from host membranes," Nature Communications, Nature, vol. 13(1), pages 1-15, 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. Jonathan Filée & Hubert F. Becker & Lucille Mellottee & Rima Zein Eddine & Zhihui Li & Wenlu Yin & Jean-Christophe Lambry & Ursula Liebl & Hannu Myllykallio, 2023. "Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Allen G. Sanderlin & Hannah Kurka Margolis & Abigail F. Meyer & Rebecca L. Lamason, 2024. "Cell-selective proteomics reveal novel effectors secreted by an obligate intracellular bacterial pathogen," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Zhiping Yang & Xiaoya Ma & Qiuping Wang & Xiaolin Tian & Jingyan Sun & Zhenhua Zhang & Shuhai Xiao & Olivier Clerck & Frederik Leliaert & Bojian Zhong, 2023. "Phylotranscriptomics unveil a Paleoproterozoic-Mesoproterozoic origin and deep relationships of the Viridiplantae," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Mizue Anda & Shun Yamanouchi & Salvatore Cosentino & Mitsuo Sakamoto & Moriya Ohkuma & Masako Takashima & Atsushi Toyoda & Wataru Iwasaki, 2023. "Bacteria can maintain rRNA operons solely on plasmids for hundreds of millions of years," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Zhiguang Qiu & Li Yuan & Chun-Ang Lian & Bin Lin & Jie Chen & Rong Mu & Xuejiao Qiao & Liyu Zhang & Zheng Xu & Lu Fan & Yunzeng Zhang & Shanquan Wang & Junyi Li & Huiluo Cao & Bing Li & Baowei Chen & , 2024. "BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Giovanni Scarinci & Jan-Luca Ariens & Georgia Angelidou & Sebastian Schmidt & Timo Glatter & Nicole Paczia & Victor Sourjik, 2024. "Enhanced metabolic entanglement emerges during the evolution of an interkingdom microbial community," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Zhongyi Lu & Runyue Xia & Siyu Zhang & Jie Pan & Yang Liu & Yuri I. Wolf & Eugene V. Koonin & Meng Li, 2024. "Evolution of optimal growth temperature in Asgard archaea inferred from the temperature dependence of GDP binding to EF-1A," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    9. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Matthew Herdman & Buse Isbilir & Andriko Kügelgen & Ulrike Schulze & Alan Wainman & Tanmay A. M. Bharat, 2024. "Cell cycle dependent coordination of surface layer biogenesis in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    11. Tomoyuki Hatano & Saravanan Palani & Dimitra Papatziamou & Ralf Salzer & Diorge P. Souza & Daniel Tamarit & Mehul Makwana & Antonia Potter & Alexandra Haig & Wenjue Xu & David Townsend & David Rochest, 2022. "Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery," Nature Communications, Nature, vol. 13(1), pages 1-16, 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_s41467-024-45351-7. 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.