IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46297-6.html
   My bibliography  Save this article

Bet hedging in a unicellular microalga

Author

Listed:
  • Si Tang

    (Tsinghua Shenzhen International Graduate School)

  • Yaqing Liu

    (Tsinghua Shenzhen International Graduate School)

  • Jianming Zhu

    (Tsinghua Shenzhen International Graduate School)

  • Xueyu Cheng

    (Tsinghua Shenzhen International Graduate School)

  • Lu Liu

    (Tsinghua Shenzhen International Graduate School)

  • Katrin Hammerschmidt

    (Kiel University)

  • Jin Zhou

    (Tsinghua Shenzhen International Graduate School)

  • Zhonghua Cai

    (Tsinghua Shenzhen International Graduate School
    Tsinghua Shenzhen International Graduate School)

Abstract

Understanding how organisms have adapted to persist in unpredictable environments is a fundamental goal in biology. Bet hedging, an evolutionary adaptation observed from microbes to humans, facilitates reproduction and population persistence in randomly fluctuating environments. Despite its prevalence, empirical evidence in microalgae, crucial primary producers and carbon sinks, is lacking. Here, we report a bet-hedging strategy in the unicellular microalga Haematococcus pluvialis. We show that isogenic populations reversibly diversify into heterophenotypic mobile and non-mobile cells independently of environmental conditions, likely driven by stochastic gene expression. Mobile cells grow faster but are stress-sensitive, while non-mobile cells prioritise stress resistance over growth. This is due to shifts from growth-promoting activities (cell division, photosynthesis) to resilience-promoting processes (thickened cell wall, cell enlargement, aggregation, accumulation of antioxidant and energy-storing compounds). Our results provide empirical evidence for bet hedging in a microalga, indicating the potential for adaptation to current and future environmental conditions and consequently conservation of ecosystem functions.

Suggested Citation

  • Si Tang & Yaqing Liu & Jianming Zhu & Xueyu Cheng & Lu Liu & Katrin Hammerschmidt & Jin Zhou & Zhonghua Cai, 2024. "Bet hedging in a unicellular microalga," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46297-6
    DOI: 10.1038/s41467-024-46297-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46297-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46297-6?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. Hubertus J. E. Beaumont & Jenna Gallie & Christian Kost & Gayle C. Ferguson & Paul B. Rainey, 2009. "Experimental evolution of bet hedging," Nature, Nature, vol. 462(7269), pages 90-93, November.
    2. Martin Ackermann & Bärbel Stecher & Nikki E. Freed & Pascal Songhet & Wolf-Dietrich Hardt & Michael Doebeli, 2008. "Self-destructive cooperation mediated by phenotypic noise," Nature, Nature, vol. 454(7207), pages 987-990, August.
    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. Peña, Jorge & Nöldeke, Georg & Lehmann, Laurent, 2014. "Relatedness and synergies of kind and scale in the evolution of helping," Working papers 2014/09, Faculty of Business and Economics - University of Basel.
    2. Manalee Vishnu Surve & Smita Bhutda & Akshay Datey & Anjali Anil & Shalini Rawat & Athira Pushpakaran & Dipty Singh & Kwang Sik Kim & Dipshikha Chakravortty & Anirban Banerjee, 2018. "Heterogeneity in pneumolysin expression governs the fate of Streptococcus pneumoniae during blood-brain barrier trafficking," PLOS Pathogens, Public Library of Science, vol. 14(7), pages 1-29, July.
    3. Andrew W. Lo & H. Allen Orr & Ruixun Zhang, 2018. "The growth of relative wealth and the Kelly criterion," Journal of Bioeconomics, Springer, vol. 20(1), pages 49-67, April.
    4. Yann S Dufour & Sébastien Gillet & Nicholas W Frankel & Douglas B Weibel & Thierry Emonet, 2016. "Direct Correlation between Motile Behavior and Protein Abundance in Single Cells," PLOS Computational Biology, Public Library of Science, vol. 12(9), pages 1-25, September.
    5. Gary Friedman & Stephen McCarthy & Dmitrii Rachinskii, 2014. "Hysteresis Can Grant Fitness in Stochastically Varying Environment," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-9, July.
    6. Anne-Stéphanie Rueff & Renske Raaphorst & Surya D. Aggarwal & Javier Santos-Moreno & Géraldine Laloux & Yolanda Schaerli & Jeffrey N. Weiser & Jan-Willem Veening, 2023. "Synthetic genetic oscillators demonstrate the functional importance of phenotypic variation in pneumococcal-host interactions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Jessica A Lee & Siavash Riazi & Shahla Nemati & Jannell V Bazurto & Andreas E Vasdekis & Benjamin J Ridenhour & Christopher H Remien & Christopher J Marx, 2019. "Microbial phenotypic heterogeneity in response to a metabolic toxin: Continuous, dynamically shifting distribution of formaldehyde tolerance in Methylobacterium extorquens populations," PLOS Genetics, Public Library of Science, vol. 15(11), pages 1-38, November.
    8. Sébastien Boyer & Lucas Hérissant & Gavin Sherlock, 2021. "Adaptation is influenced by the complexity of environmental change during evolution in a dynamic environment," PLOS Genetics, Public Library of Science, vol. 17(1), pages 1-27, January.
    9. Jan J. Kreider & Thijs Janzen & Abel Bernadou & Daniel Elsner & Boris H. Kramer & Franz J. Weissing, 2022. "Resource sharing is sufficient for the emergence of division of labour," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    10. Peña, Jorge & Cooper, Guy Alexander & Liu, Ming & West, Stuart Andrew, 2020. "Dividing labour in social microorganisms: coordinated or random specialisation?," IAST Working Papers 20-104, Institute for Advanced Study in Toulouse (IAST).
    11. Terence C. Burnham & Aimee Dunlap & David W. Stephens, 2015. "Experimental Evolution and Economics," SAGE Open, , vol. 5(4), pages 21582440156, November.
    12. Byer, Nathan W. & Reid, Brendan N., 2022. "The emergence of imperfect philopatry and fidelity in spatially and temporally heterogeneous environments," Ecological Modelling, Elsevier, vol. 468(C).
    13. Karl P. Gerhardt & Satyajit D. Rao & Evan J. Olson & Oleg A. Igoshin & Jeffrey J. Tabor, 2021. "Independent control of mean and noise by convolution of gene expression distributions," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    14. Leighton T Izu & Tamás Bányász & Ye Chen-Izu, 2015. "Optimizing Population Variability to Maximize Benefit," PLOS ONE, Public Library of Science, vol. 10(12), pages 1-17, December.
    15. David D. Woods, 2018. "The theory of graceful extensibility: basic rules that govern adaptive systems," Environment Systems and Decisions, Springer, vol. 38(4), pages 433-457, December.
    16. Czuppon, Peter & Gokhale, Chaitanya S., 2018. "Disentangling eco-evolutionary effects on trait fixation," Theoretical Population Biology, Elsevier, vol. 124(C), pages 93-107.
    17. Patrick Kaiser & Emma Slack & Andrew J Grant & Wolf-Dietrich Hardt & Roland R Regoes, 2013. "Lymph Node Colonization Dynamics after Oral Salmonella Typhimurium Infection in Mice," PLOS Pathogens, Public Library of Science, vol. 9(9), pages 1-12, September.
    18. Amandine Nucci & Eduardo P. C. Rocha & Olaya Rendueles, 2022. "Adaptation to novel spatially-structured environments is driven by the capsule and alters virulence-associated traits," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. Te Wu & Long Wang & Feng Fu, 2017. "Coevolutionary dynamics of phenotypic diversity and contingent cooperation," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-16, January.
    20. Chaitanya S. Gokhale & Marcus Frean & Paul B. Rainey, 2023. "Eco-evolutionary Logic of Mutualisms," Dynamic Games and Applications, Springer, vol. 13(4), pages 1066-1087, 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_s41467-024-46297-6. 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.