IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41491-4.html
   My bibliography  Save this article

A linear and circular dual-conformation noncoding RNA involved in oxidative stress tolerance in Bacillus altitudinis

Author

Listed:
  • Ting-Ting He

    (Sichuan University
    West China Hospital, Sichuan University)

  • Yun-Fan Xu

    (Sichuan University)

  • Xiang Li

    (Sichuan University)

  • Xia Wang

    (Sichuan University)

  • Jie-Yu Li

    (Sichuan University)

  • Dan Ou-Yang

    (Sichuan University)

  • Han-Sen Cheng

    (Sichuan University)

  • Hao-Yang Li

    (Sichuan University)

  • Jia Qin

    (Sichuan University)

  • Yu Huang

    (Sichuan University)

  • Hai-Yan Wang

    (Sichuan University)

Abstract

Circular RNAs have been extensively studied in eukaryotes, but their presence and/or biological functionality in bacteria are unclear. Here, we show that a regulatory noncoding RNA (DucS) exists in both linear and circular conformation in Bacillus altitudinis. The linear forms promote B. altitudinis tolerance to H2O2 stress, partly through increased translation of a stress-responsive gene, htrA. The 3′ end sequences of the linear forms are crucial for RNA circularization, and formation of circular forms can decrease the levels of the regulatory linear cognates. Bioinformatic analysis of available RNA-seq datasets from 30 bacterial species revealed multiple circular RNA candidates, distinct from DucS, for all the examined species. Experiments testing for the presence of selected circular RNA candidates in four species successfully validated 7 out of 9 candidates from B. altitudinis and 4 out of 5 candidates from Bacillus paralicheniformis; However, none of the candidates tested for Bacillus subtilis and Escherichia coli were detected. Our work identifies a dual-conformation regulatory RNA in B. altitutidinis, and indicates that circular RNAs exist in diverse bacteria. However, circularization of specific RNAs does not seem to be conserved across species, and the circularization mechanisms and biological functionality of the circular forms remain unclear.

Suggested Citation

  • Ting-Ting He & Yun-Fan Xu & Xiang Li & Xia Wang & Jie-Yu Li & Dan Ou-Yang & Han-Sen Cheng & Hao-Yang Li & Jia Qin & Yu Huang & Hai-Yan Wang, 2023. "A linear and circular dual-conformation noncoding RNA involved in oxidative stress tolerance in Bacillus altitudinis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41491-4
    DOI: 10.1038/s41467-023-41491-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41491-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41491-4?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. Sebastian Memczak & Marvin Jens & Antigoni Elefsinioti & Francesca Torti & Janna Krueger & Agnieszka Rybak & Luisa Maier & Sebastian D. Mackowiak & Lea H. Gregersen & Mathias Munschauer & Alexander Lo, 2013. "Circular RNAs are a large class of animal RNAs with regulatory potency," Nature, Nature, vol. 495(7441), pages 333-338, March.
    2. Thomas B. Hansen & Trine I. Jensen & Bettina H. Clausen & Jesper B. Bramsen & Bente Finsen & Christian K. Damgaard & Jørgen Kjems, 2013. "Natural RNA circles function as efficient microRNA sponges," Nature, Nature, vol. 495(7441), pages 384-388, March.
    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. Bin Li & Wen-Wu Bai & Tao Guo & Zhen-Yu Tang & Xue-Jiao Jing & Ti-Chao Shan & Sen Yin & Ying Li & Fu Wang & Mo-Li Zhu & Jun-Xiu Lu & Yong-Ping Bai & Bo Dong & Peng Li & Shuang-Xi Wang, 2024. "Statins improve cardiac endothelial function to prevent heart failure with preserved ejection fraction through upregulating circRNA-RBCK1," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Roberta Piras & Emily Y. Ko & Connor Barrett & Marco Simone & Xianzhi Lin & Marina T. Broz & Fernando H. G. Tessaro & Mireia Castillo-Martin & Carlos Cordon-Cardo & Helen S. Goodridge & Dolores Vizio , 2022. "circCsnk1g3- and circAnkib1-regulated interferon responses in sarcoma promote tumorigenesis by shaping the immune microenvironment," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Zhenzhen Chen & Qiankun He & Tiankun Lu & Jiayi Wu & Gaoli Shi & Luyun He & Hong Zong & Benyu Liu & Pingping Zhu, 2023. "mcPGK1-dependent mitochondrial import of PGK1 promotes metabolic reprogramming and self-renewal of liver TICs," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Yu Dong & Qian Gao & Yong Chen & Zhao Zhang & Yanhua Du & Yuan Liu & Guangxiong Zhang & Shengli Li & Gaoyang Wang & Xiang Chen & Hong Liu & Leng Han & Youqiong Ye, 2023. "Identification of CircRNA signature associated with tumor immune infiltration to predict therapeutic efficacy of immunotherapy," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Mateja Rybiczka-Tešulov & Oxana Garritsen & Morten T. Venø & Laura Wieg & Roland van Dijk & Karim Rahimi & Andreia Gomes-Duarte & Marina de Wit & Lieke L. Haar & Lars Michels & Nicky C. H. van Kronenb, 2024. "Circular RNAs regulate neuron size and migration of midbrain dopamine neurons during development," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    6. Steffen Fuchs & Clara Danßmann & Filippos Klironomos & Annika Winkler & Jörg Fallmann & Louisa-Marie Kruetzfeldt & Annabell Szymansky & Julian Naderi & Stephan H. Bernhart & Laura Grunewald & Konstant, 2023. "Defining the landscape of circular RNAs in neuroblastoma unveils a global suppressive function of MYCN," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    7. Xiaojuan Fan & Yun Yang & Chuyun Chen & Zefeng Wang, 2022. "Pervasive translation of circular RNAs driven by short IRES-like elements," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    8. Federica Conte & Giulia Fiscon & Matteo Chiara & Teresa Colombo & Lorenzo Farina & Paola Paci, 2017. "Role of the long non-coding RNA PVT1 in the dysregulation of the ceRNA-ceRNA network in human breast cancer," PLOS ONE, Public Library of Science, vol. 12(2), pages 1-22, February.
    9. Nana Xu & Jiebang Jiang & Fei Jiang & Guokai Dong & Li Meng & Meng Wang & Jing Chen & Cong Li & Yongping Shi & Sisi He & Rongpeng Li, 2024. "CircCDC42-encoded CDC42-165aa regulates macrophage pyroptosis in Klebsiella pneumoniae infection through Pyrin inflammasome activation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Xiujuan Lei & Wenxiang Zhang, 2019. "BRWSP: Predicting circRNA-Disease Associations Based on Biased Random Walk to Search Paths on a Multiple Heterogeneous Network," Complexity, Hindawi, vol. 2019, pages 1-12, November.
    11. Yue Liu & Yue Yang & Chenying Xu & Jianxing Liu & Jiale Chen & Guoqing Li & Bin Huang & Yi Pan & Yanfeng Zhang & Qiong Wei & Stephen J. Pandol & Fangfang Zhang & Ling Li & Liang Jin, 2023. "Circular RNA circGlis3 protects against islet β-cell dysfunction and apoptosis in obesity," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    12. Maya Ron & Igor Ulitsky, 2022. "Context-specific effects of sequence elements on subcellular localization of linear and circular RNAs," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Junliang Yin & Xiaowen Han & Yongxing Zhu & Zhengwu Fang & Derong Gao & Dongfang Ma, 2022. "Transcriptome Profiles of Circular RNAs in Common Wheat during Fusarium Head Blight Disease," Data, MDPI, vol. 7(9), pages 1-8, August.
    14. Amir Bar & Liron Argaman & Michal Eldar & Hanah Margalit, 2023. "TRS: a method for determining transcript termini from RNAtag-seq sequencing data," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Sen Ma & Xiaochun Xu & Xiaolong Wang & Yuxin Yang & Yinghua Shi & Yulin Chen, 2022. "Comprehensive Profiling of Circular RNAs in Goat Dermal Papilla Cells and Prediction of Their Modulatory Roles in Hair Growth," Agriculture, MDPI, vol. 12(9), pages 1-14, August.
    16. Xianjun Dong & Yunfei Bai & Zhixiang Liao & David Gritsch & Xiaoli Liu & Tao Wang & Rebeca Borges-Monroy & Alyssa Ehrlich & Geidy E. Serrano & Mel B. Feany & Thomas G. Beach & Clemens R. Scherzer, 2023. "Circular RNAs in the human brain are tailored to neuron identity and neuropsychiatric disease," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    17. Shaomin Yang & Di Cao & Dabbu Kumar Jaijyan & Mei Wang & Jian Liu & Ruth Cruz-cosme & Songbin Wu & Jiabin Huang & Mulan Zeng & Xiaolian Liu & Wuping Sun & Donglin Xiong & Qiyi Tang & Lizu Xiao & Hua Z, 2024. "Identification and characterization of Varicella Zoster Virus circular RNA in lytic infection," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Jian Zhong & Xujia Wu & Yixin Gao & Junju Chen & Maolei Zhang & Huangkai Zhou & Jia Yang & Feizhe Xiao & Xuesong Yang & Nunu Huang & Haoyue Qi & Xiuxing Wang & Fan Bai & Yu Shi & Nu Zhang, 2023. "Circular RNA encoded MET variant promotes glioblastoma tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Humberto J. Ferreira & Brian J. Stevenson & HuiSong Pak & Fengchao Yu & Jessica Almeida Oliveira & Florian Huber & Marie Taillandier-Coindard & Justine Michaux & Emma Ricart-Altimiras & Anne I. Kraeme, 2024. "Immunopeptidomics-based identification of naturally presented non-canonical circRNA-derived peptides," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Ke Li & Jiawei Guo & Yue Ming & Shuang Chen & Tingting Zhang & Hulin Ma & Xin Fu & Jin Wang & Wenrong Liu & Yong Peng, 2023. "A circular RNA activated by TGFβ promotes tumor metastasis through enhancing IGF2BP3-mediated PDPN mRNA stability," Nature Communications, Nature, vol. 14(1), pages 1-18, 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_s41467-023-41491-4. 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.