IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41704-w.html
   My bibliography  Save this article

Evolution of lasR mutants in polymorphic Pseudomonas aeruginosa populations facilitates chronic infection of the lung

Author

Listed:
  • Kelei Zhao

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Xiting Yang

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Qianglin Zeng

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Yige Zhang

    (Sichuan University)

  • Heyue Li

    (Sichuan University)

  • Chaochao Yan

    (Chinese Academy of Sciences)

  • Jing Shirley Li

    (Sichuan University)

  • Huan Liu

    (Sichuan University)

  • Liangming Du

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Yi Wu

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Gui Huang

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Ting Huang

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Yamei Zhang

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Hui Zhou

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Xinrong Wang

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Yiwen Chu

    (Affiliated Hospital of Chengdu University, Chengdu University)

  • Xikun Zhou

    (Sichuan University)

Abstract

Chronic infection with the bacterial pathogen Pseudomonas aeruginosa often leads to coexistence of heterogeneous populations carrying diverse mutations. In particular, loss-of-function mutations affecting the quorum-sensing regulator LasR are often found in bacteria isolated from patients with lung chronic infection and cystic fibrosis. Here, we study the evolutionary dynamics of polymorphic P. aeruginosa populations using isolates longitudinally collected from patients with chronic obstructive pulmonary disease (COPD). We find that isolates deficient in production of different sharable extracellular products are sequentially selected in COPD airways, and lasR mutants appear to be selected first due to their quorum-sensing defects. Polymorphic populations including lasR mutants display survival advantages in animal models of infection and modulate immune responses. Our study sheds light on the multistage evolution of P. aeruginosa populations during their adaptation to host lungs.

Suggested Citation

  • Kelei Zhao & Xiting Yang & Qianglin Zeng & Yige Zhang & Heyue Li & Chaochao Yan & Jing Shirley Li & Huan Liu & Liangming Du & Yi Wu & Gui Huang & Ting Huang & Yamei Zhang & Hui Zhou & Xinrong Wang & Y, 2023. "Evolution of lasR mutants in polymorphic Pseudomonas aeruginosa populations facilitates chronic infection of the lung," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41704-w
    DOI: 10.1038/s41467-023-41704-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41704-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41704-w?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. Ashleigh S. Griffin & Stuart A. West & Angus Buckling, 2004. "Cooperation and competition in pathogenic bacteria," Nature, Nature, vol. 430(7003), pages 1024-1027, August.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Kayla A. Simanek & Megan L. Schumacher & Caleb P. Mallery & Stella Shen & Lingyun Li & Jon E. Paczkowski, 2023. "Quorum-sensing synthase mutations re-calibrate autoinducer concentrations in clinical isolates of Pseudomonas aeruginosa to enhance pathogenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    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. Felix J H Hol & Peter Galajda & Krisztina Nagy & Rutger G Woolthuis & Cees Dekker & Juan E Keymer, 2013. "Spatial Structure Facilitates Cooperation in a Social Dilemma: Empirical Evidence from a Bacterial Community," PLOS ONE, Public Library of Science, vol. 8(10), pages 1-10, October.
    2. Kerry E Boyle & Hilary Monaco & Dave van Ditmarsch & Maxime Deforet & Joao B Xavier, 2015. "Integration of Metabolic and Quorum Sensing Signals Governing the Decision to Cooperate in a Bacterial Social Trait," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-26, June.
    3. Erik Bakkeren & Ersin Gül & Jana S. Huisman & Yves Steiger & Andrea Rocker & Wolf-Dietrich Hardt & Médéric Diard, 2022. "Impact of horizontal gene transfer on emergence and stability of cooperative virulence in Salmonella Typhimurium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Richard J. Lindsay & Philippa J. Holder & Mark Hewlett & Ivana Gudelj, 2024. "Experimental evolution of yeast shows that public-goods upregulation can evolve despite challenges from exploitative non-producers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Hammerstein, Peter & Leimar, Olof, 2015. "Evolutionary Game Theory in Biology," Handbook of Game Theory with Economic Applications,, Elsevier.
    6. Dirk Helbing & Anders Johansson, 2010. "Cooperation, Norms, and Revolutions: A Unified Game-Theoretical Approach," PLOS ONE, Public Library of Science, vol. 5(10), pages 1-15, October.
    7. Ding, Zhen-Wei & Zheng, Guo-Zhong & Cai, Chao-Ran & Cai, Wei-Ran & Chen, Li & Zhang, Ji-Qiang & Wang, Xu-Ming, 2023. "Emergence of cooperation in two-agent repeated games with reinforcement learning," Chaos, Solitons & Fractals, Elsevier, vol. 175(P1).
    8. Sebastian Galiani & Matthew Staiger & Gustavo Torrens, 2017. "When Children Rule: Parenting in Modern Families," NBER Working Papers 23087, National Bureau of Economic Research, Inc.
    9. Qi Su & Lei Zhou & Long Wang, 2019. "Evolutionary multiplayer games on graphs with edge diversity," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-22, April.
    10. Liming Xia & Youzhi Miao & A’li Cao & Yan Liu & Zihao Liu & Xinli Sun & Yansheng Xue & Zhihui Xu & Weibing Xun & Qirong Shen & Nan Zhang & Ruifu Zhang, 2022. "Biosynthetic gene cluster profiling predicts the positive association between antagonism and phylogeny in Bacillus," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Asher Leeks & Stuart A. West & Melanie Ghoul, 2021. "The evolution of cheating in viruses," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    12. Hilary Monaco & Kevin S. Liu & Tiago Sereno & Maxime Deforet & Bradford P. Taylor & Yanyan Chen & Caleb C. Reagor & Joao B. Xavier, 2022. "Spatial-temporal dynamics of a microbial cooperative behavior resistant to cheating," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    13. Kazufumi Hosoda & Shingo Suzuki & Yoshinori Yamauchi & Yasunori Shiroguchi & Akiko Kashiwagi & Naoaki Ono & Kotaro Mori & Tetsuya Yomo, 2011. "Cooperative Adaptation to Establishment of a Synthetic Bacterial Mutualism," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-9, February.
    14. Aneesh P H Bose & Johanna Dabernig-Heinz & Jan Oberkofler & Lukas Koch & Jacqueline Grimm & Kristina M Sefc & Alex Jordan, 2023. "Aggression and spatial positioning of kin and non-kin fish in social groups," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(4), pages 673-681.
    15. Jorge Peña & Bin Wu & Jordi Arranz & Arne Traulsen, 2016. "Evolutionary Games of Multiplayer Cooperation on Graphs," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-15, August.
    16. Wild, Geoff & Pizzari, Tommaso & West, Stuart A., 2011. "Sexual conflict in viscous populations: The effect of the timing of dispersal," Theoretical Population Biology, Elsevier, vol. 80(4), pages 298-316.
    17. Andreas Wagner, 2006. "Cooperation is Fleeting in the World of Transposable Elements," PLOS Computational Biology, Public Library of Science, vol. 2(12), pages 1-8, December.
    18. Elhanati, Yuval & Schuster, Stefan & Brenner, Naama, 2011. "Dynamic modeling of cooperative protein secretion in microorganism populations," Theoretical Population Biology, Elsevier, vol. 80(1), pages 49-63.
    19. Cazzolla Gatti, Roberto, 2021. "A multi-armed bandit algorithm speeds up the evolution of cooperation," Ecological Modelling, Elsevier, vol. 439(C).
    20. David V McLeod & Troy Day, 2019. "Social evolution under demographic stochasticity," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-13, February.

    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_s41467-023-41704-w. 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.