IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43759-1.html
   My bibliography  Save this article

The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria

Author

Listed:
  • Owain J. Bryant

    (University of Cambridge
    National Cancer Institute)

  • Filip Lastovka

    (University of Cambridge)

  • Jessica Powell

    (University of Cambridge)

  • Betty Y. -W. Chung

    (University of Cambridge)

Abstract

Translational control in pathogenic bacteria is fundamental to gene expression and affects virulence and other infection phenotypes. We used an enhanced ribosome profiling protocol coupled with parallel transcriptomics to capture accurately the global translatome of two evolutionarily distant pathogenic bacteria—the Gram-negative bacterium Salmonella and the Gram-positive bacterium Listeria. We find that the two bacteria use different mechanisms to translationally regulate protein synthesis. In Salmonella, in addition to the expected correlation between translational efficiency and cis-regulatory features such as Shine–Dalgarno (SD) strength and RNA secondary structure around the initiation codon, our data reveal an effect of the 2nd and 3rd codons, where the presence of tandem lysine codons (AAA-AAA) enhances translation in both Salmonella and E. coli. Strikingly, none of these features are seen in efficiently translated Listeria transcripts. Instead, approximately 20% of efficiently translated Listeria genes exhibit 70 S footprints seven nt upstream of the authentic start codon, suggesting that these genes may be subject to a novel translational initiation mechanism. Our results show that SD strength is not a direct hallmark of translational efficiency in all bacteria. Instead, Listeria has evolved additional mechanisms to control gene expression level that are distinct from those utilised by Salmonella and E. coli.

Suggested Citation

  • Owain J. Bryant & Filip Lastovka & Jessica Powell & Betty Y. -W. Chung, 2023. "The distinct translational landscapes of gram-negative Salmonella and gram-positive Listeria," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43759-1
    DOI: 10.1038/s41467-023-43759-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43759-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43759-1?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. Manasvi Verma & Junhong Choi & Kyle A. Cottrell & Zeno Lavagnino & Erica N. Thomas & Slavica Pavlovic-Djuranovic & Pawel Szczesny & David W. Piston & Hani S. Zaher & Joseph D. Puglisi & Sergej Djurano, 2019. "A short translational ramp determines the efficiency of protein synthesis," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. Asuteka Nagao & Yui Nakanishi & Yutaro Yamaguchi & Yoshifumi Mishina & Minami Karoji & Takafumi Toya & Tomoya Fujita & Shintaro Iwasaki & Kenjyo Miyauchi & Yuriko Sakaguchi & Tsutomu Suzuki, 2023. "Quality control of protein synthesis in the early elongation stage," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Gene-Wei Li & Eugene Oh & Jonathan S. Weissman, 2012. "The anti-Shine–Dalgarno sequence drives translational pausing and codon choice in bacteria," Nature, Nature, vol. 484(7395), pages 538-541, April.
    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. Asuteka Nagao & Yui Nakanishi & Yutaro Yamaguchi & Yoshifumi Mishina & Minami Karoji & Takafumi Toya & Tomoya Fujita & Shintaro Iwasaki & Kenjyo Miyauchi & Yuriko Sakaguchi & Tsutomu Suzuki, 2023. "Quality control of protein synthesis in the early elongation stage," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Pietro Bongini & Niccolò Pancino & Veronica Lachi & Caterina Graziani & Giorgia Giacomini & Paolo Andreini & Monica Bianchini, 2024. "Point-Wise Ribosome Translation Speed Prediction with Recurrent Neural Networks," Mathematics, MDPI, vol. 12(3), pages 1-12, January.
    3. Fajin Li & Jianhuo Fang & Yifan Yu & Sijia Hao & Qin Zou & Qinglin Zeng & Xuerui Yang, 2023. "Reanalysis of ribosome profiling datasets reveals a function of rocaglamide A in perturbing the dynamics of translation elongation via eIF4A," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Alexey A Gritsenko & Marc Hulsman & Marcel J T Reinders & Dick de Ridder, 2015. "Unbiased Quantitative Models of Protein Translation Derived from Ribosome Profiling Data," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-26, August.
    5. Bin Shao & Jiawei Yan & Jing Zhang & Lili Liu & Ye Chen & Allen R. Buskirk, 2024. "Riboformer: a deep learning framework for predicting context-dependent translation dynamics," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Poonam Roshan & Sahiti Kuppa & Jenna R. Mattice & Vikas Kaushik & Rahul Chadda & Nilisha Pokhrel & Brunda R. Tumala & Aparna Biswas & Brian Bothner & Edwin Antony & Sofia Origanti, 2023. "An Aurora B-RPA signaling axis secures chromosome segregation fidelity," Nature Communications, Nature, vol. 14(1), pages 1-19, 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:14:y:2023:i:1:d:10.1038_s41467-023-43759-1. 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.