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Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification

The ISME Journal volume 17, pages 525–536 (2023)Cite this article

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Abstract

Ocean warming (OW) and acidification (OA) are recognized as two major climatic conditions influencing phytoplankton growth and nutritional or toxin content. However, there is limited knowledge on the responses of harmful algal bloom species that produce toxins. Here, the study provides quantitative and mechanistic understanding of the acclimation and adaptation responses of the domoic acid (DA) producing diatom Pseudo-nitzschia multiseries to rising temperature and pCO2 using both a one-year in situ bulk culture experiment, and an 800-day laboratory acclimation experiment. Ocean warming showed larger selective effects on growth and DA metabolism than ocean acidification. In a bulk culture experiment, increasing temperature +4 °C above ambient seawater temperature significantly increased DA concentration by up to 11-fold. In laboratory when the long-term warming acclimated samples were assayed under low temperatures, changes in growth rates and DA concentrations indicated that P. multiseries did not adapt to elevated temperature, but could instead rapidly and reversibly acclimate to temperature shifts. However, the warming-acclimated lines showed evidence of adaptation to elevated temperatures in the transcriptome data. Here the core gene expression was not reversed when warming-acclimated lines were moved back to the low temperature environment, which suggested that P. multiseries cells might adapt to rising temperature over longer timescales. The distinct strategies of phenotypic plasticity to rising temperature and pCO2 demonstrate a strong acclimation capacity for this bloom-forming toxic diatom in the future ocean.

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Fig. 1: Growth rates and DA concentrations of P. multiseries under six different temperature and pCO2 combinations in bulk culture experiments during summer and autumn.
Fig. 2: Growth rates and DA concentrations of P. multiseries laboratory cultures over 800 days of acclimation to nine different temperature and pCO2 combinations.
Fig. 3: Combined effects of ocean warming and ocean acidification on traits of P. multiseries after short-term or long-term acclimation.
Fig. 4: Growth rates and DA concentrations of P. multiseries in a shift experiment after long-term acclimation.
Fig. 5: Molecular understanding of altered DA biosynthetic potential of P. multiseries under different acclimation conditions.
Fig. 6: Relative expression of the core genes involed in the DA metabolic pathway of long-term acclimated P. multiseries in shift experiments.

Data availability

Transcriptome sequencing data are available at the National Center for Biotechnology Information (NCBI) with the accession number PRJNA686847.

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Acknowledgements

This work was supported by Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No.2021QNLM050103-1), National Natural Science Foundation of China (41976110; 32072329; 32000404); the Young Taishan Scholars Program to DX, Taishan Scholars Funding; Central Public-interest Scientific Institution Basal Research Fund, CAFS (NO. 2020TD27, 20603022021019); Natural Science Foundation of Shandong Province (ZR2021MD075); Laoshan Laboratory (LSKJ202203204); China Agriculture Research System (CARS-50); U.S. California Urban Ocean Sea Grant and National Science Foundation grants (OCE 1638804, OCE 1538525, OCE 2149837, OCE 2120619).

Author information

Authors and Affiliations

  1. National Key Laboratory of Mariculture Biobreeding and Sustainable Production, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, China

    Dong Xu, Guanchao Zheng, Tao Jiang, Ke Sun, Xiao Fan, Xiaowen Zhang, Yan Zhang, Wei Wang, Yitao Wang, Yan Li, Haiyan Wu, Zhijun Tan & Naihao Ye

  2. Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

    Dong Xu & Naihao Ye

  3. Institute of Marine Sciences, ICM-CSIC, Barcelona, Spain

    Georgina Brennan

  4. School of Forestry and Wildlife Sciences, Auburn University, Auburn, AL, USA

    Zhuonan Wang

  5. Institut de Biologie de l’ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France

    Chris Bowler

  6. Marine Science Research Institute of Shandong Province (National Oceanographic Center), Qingdao, China

    Youxun Li

  7. Department of Biological Sciences, University of Southern California, Los Angeles, CA, 90089, USA

    Fei-Xue Fu & David A. Hutchins

Authors
  1. Dong Xu
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  2. Guanchao Zheng
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Contributions

NY designed the project with contributions from DX. NY, DX, GCZ, ZW, TJ, KS, XF, CB, DAH, and ZJT analyzed the data. DX, NY, GB, ZW, and DAH wrote the manuscript; all authors contributed to editing the manuscript.

Corresponding authors

Correspondence to David A. Hutchins, Zhijun Tan or Naihao Ye.

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Xu, D., Zheng, G., Brennan, G. et al. Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification. ISME J 17, 525–536 (2023). https://doi.org/10.1038/s41396-023-01370-8

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