IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46993-3.html
   My bibliography  Save this article

Patchy and widespread distribution of bacterial translation arrest peptides associated with the protein localization machinery

Author

Listed:
  • Keigo Fujiwara

    (Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku
    Kyoto Sangyo University)

  • Naoko Tsuji

    (Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku
    Kyoto Sangyo University)

  • Mayu Yoshida

    (Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku
    Kyoto Sangyo University)

  • Hiraku Takada

    (Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku
    Kyoto Sangyo University)

  • Shinobu Chiba

    (Kyoto Sangyo University, Motoyama, Kamigamo, Kita-Ku
    Kyoto Sangyo University)

Abstract

Regulatory arrest peptides interact with specific residues on bacterial ribosomes and arrest their own translation. Here, we analyse over 30,000 bacterial genome sequences to identify additional Sec/YidC-related arrest peptides, followed by in vivo and in vitro analyses. We find that Sec/YidC-related arrest peptides show patchy, but widespread, phylogenetic distribution throughout the bacterial domain. Several of the identified peptides contain distinct conserved sequences near the C-termini, but are still able to efficiently stall bacterial ribosomes in vitro and in vivo. In addition, we identify many arrest peptides that share an R-A-P-P-like sequence, suggesting that this sequence might serve as a common evolutionary seed to overcome ribosomal structural differences across species.

Suggested Citation

  • Keigo Fujiwara & Naoko Tsuji & Mayu Yoshida & Hiraku Takada & Shinobu Chiba, 2024. "Patchy and widespread distribution of bacterial translation arrest peptides associated with the protein localization machinery," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46993-3
    DOI: 10.1038/s41467-024-46993-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46993-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46993-3?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. Martino Morici & Sara Gabrielli & Keigo Fujiwara & Helge Paternoga & Bertrand Beckert & Lars V. Bock & Shinobu Chiba & Daniel N. Wilson, 2024. "RAPP-containing arrest peptides induce translational stalling by short circuiting the ribosomal peptidyltransferase activity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Tomoya Tsukazaki & Hiroyuki Mori & Yuka Echizen & Ryuichiro Ishitani & Shuya Fukai & Takeshi Tanaka & Anna Perederina & Dmitry G. Vassylyev & Toshiyuki Kohno & Andrés D. Maturana & Koreaki Ito & Osamu, 2011. "Structure and function of a membrane component SecDF that enhances protein export," Nature, Nature, vol. 474(7350), pages 235-238, June.
    3. Felix Gersteuer & Martino Morici & Sara Gabrielli & Keigo Fujiwara & Haaris A. Safdari & Helge Paternoga & Lars V. Bock & Shinobu Chiba & Daniel N. Wilson, 2024. "The SecM arrest peptide traps a pre-peptide bond formation state of the ribosome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Kaoru Kumazaki & Shinobu Chiba & Mizuki Takemoto & Arata Furukawa & Ken-ichi Nishiyama & Yasunori Sugano & Takaharu Mori & Naoshi Dohmae & Kunio Hirata & Yoshiko Nakada-Nakura & Andrés D. Maturana & Y, 2014. "Structural basis of Sec-independent membrane protein insertion by YidC," Nature, Nature, vol. 509(7501), pages 516-520, May.
    5. Liang Xue & Swantje Lenz & Maria Zimmermann-Kogadeeva & Dimitry Tegunov & Patrick Cramer & Peer Bork & Juri Rappsilber & Julia Mahamid, 2022. "Publisher Correction: Visualizing translation dynamics at atomic detail inside a bacterial cell," Nature, Nature, vol. 611(7937), pages 13-13, November.
    6. Liang Xue & Swantje Lenz & Maria Zimmermann-Kogadeeva & Dimitry Tegunov & Patrick Cramer & Peer Bork & Juri Rappsilber & Julia Mahamid, 2022. "Visualizing translation dynamics at atomic detail inside a bacterial cell," Nature, Nature, vol. 610(7930), pages 205-211, October.
    7. Daniel Sohmen & Shinobu Chiba & Naomi Shimokawa-Chiba & C. Axel Innis & Otto Berninghausen & Roland Beckmann & Koreaki Ito & Daniel N. Wilson, 2015. "Structure of the Bacillus subtilis 70S ribosome reveals the basis for species-specific stalling," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    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. Lior Aram & Diede Haan & Neta Varsano & James B. Gilchrist & Christoph Heintze & Ron Rotkopf & Katya Rechav & Nadav Elad & Nils Kröger & Assaf Gal, 2024. "Intracellular morphogenesis of diatom silica is guided by local variations in membrane curvature," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Timo Flügel & Magdalena Schacherl & Anett Unbehaun & Birgit Schroeer & Marylena Dabrowski & Jörg Bürger & Thorsten Mielke & Thiemo Sprink & Christoph A. Diebolder & Yollete V. Guillén Schlippe & Chris, 2024. "Transient disome complex formation in native polysomes during ongoing protein synthesis captured by cryo-EM," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Iskander Khusainov & Natalie Romanov & Camille Goemans & Beata Turoňová & Christian E. Zimmerli & Sonja Welsch & Julian D. Langer & Athanasios Typas & Martin Beck, 2024. "Bactericidal effect of tetracycline in E. coli strain ED1a may be associated with ribosome dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Jianfang Liu & Ewan K. S. McRae & Meng Zhang & Cody Geary & Ebbe Sloth Andersen & Gang Ren, 2024. "Non-averaged single-molecule tertiary structures reveal RNA self-folding through individual-particle cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Simon A. Fromm & Kate M. O’Connor & Michael Purdy & Pramod R. Bhatt & Gary Loughran & John F. Atkins & Ahmad Jomaa & Simone Mattei, 2023. "The translating bacterial ribosome at 1.55 Å resolution generated by cryo-EM imaging services," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    6. Nikita Balyschew & Artsemi Yushkevich & Vasilii Mikirtumov & Ricardo M. Sanchez & Thiemo Sprink & Mikhail Kudryashev, 2023. "Streamlined structure determination by cryo-electron tomography and subtomogram averaging using TomoBEAR," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Sergio Cruz-León & Tomáš Majtner & Patrick C. Hoffmann & Jan Philipp Kreysing & Sebastian Kehl & Maarten W. Tuijtel & Stefan L. Schaefer & Katharina Geißler & Martin Beck & Beata Turoňová & Gerhard Hu, 2024. "High-confidence 3D template matching for cryo-electron tomography," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Zikun Zhu & Shuai Wang & Shu-ou Shan, 2022. "Ribosome profiling reveals multiple roles of SecA in cotranslational protein export," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Patrick C. Hoffmann & Jan Philipp Kreysing & Iskander Khusainov & Maarten W. Tuijtel & Sonja Welsch & Martin Beck, 2022. "Structures of the eukaryotic ribosome and its translational states in situ," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    10. Pawel R. Laskowski & Kristyna Pluhackova & Maximilian Haase & Brian M. Lang & Gisela Nagler & Andreas Kuhn & Daniel J. Müller, 2021. "Monitoring the binding and insertion of a single transmembrane protein by an insertase," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    11. Felix Gersteuer & Martino Morici & Sara Gabrielli & Keigo Fujiwara & Haaris A. Safdari & Helge Paternoga & Lars V. Bock & Shinobu Chiba & Daniel N. Wilson, 2024. "The SecM arrest peptide traps a pre-peptide bond formation state of the ribosome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Martino Morici & Sara Gabrielli & Keigo Fujiwara & Helge Paternoga & Bertrand Beckert & Lars V. Bock & Shinobu Chiba & Daniel N. Wilson, 2024. "RAPP-containing arrest peptides induce translational stalling by short circuiting the ribosomal peptidyltransferase activity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Laura Czech & Christopher-Nils Mais & Hanna Kratzat & Pinku Sarmah & Pietro Giammarinaro & Sven-Andreas Freibert & Hanna Folke Esser & Joanna Musial & Otto Berninghausen & Wieland Steinchen & Roland B, 2022. "Inhibition of SRP-dependent protein secretion by the bacterial alarmone (p)ppGpp," Nature Communications, Nature, vol. 13(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_s41467-024-46993-3. 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.