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

Author

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  • 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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
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