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Acclimation and adaptation to elevated pCO2 increase arsenic resilience in marine diatoms

Abstract

Arsenic pollution is a widespread threat to marine life, but the ongoing rise pCO2 levels is predicted to decrease bio-toxicity of arsenic. However, the effects of arsenic toxicity on marine primary producers under elevated pCO2 are not well characterized. Here, we studied the effects of arsenic toxicity in three globally distributed diatom species (Phaeodactylum tricornutum, Thalassiosira pseudonana, and Chaetoceros mulleri) after short-term acclimation (ST, 30 days), medium-term exposure (MT, 750 days), and long-term (LT, 1460 days) selection under ambient (400 µatm) and elevated (1000 and 2000 µatm) pCO2. We found that elevated pCO2 alleviated arsenic toxicity even after short acclimation times but the magnitude of the response decreased after mid and long-term adaptation. When fed with these elevated pCO2 selected diatoms, the scallop Patinopecten yessoensis had significantly lower arsenic content (3.26–52.83%). Transcriptomic and biochemical analysis indicated that the diatoms rapidly developed arsenic detoxification strategies, which included upregulation of transporters associated with shuttling harmful compounds out of the cell to reduce arsenic accumulation, and upregulation of proteins involved in synthesizing glutathione (GSH) to chelate intracellular arsenic to reduce arsenic toxicity. Thus, our results will expand our knowledge to fully understand the ecological risk of trace metal pollution under increasing human activity induced ocean acidification.

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Fig. 1: Growth rates of P. tricornutum, T. pseudonana, and C. mulleri selected under ambient and elevated pCO2 without arsenic exposure (Control), and with AsIII (low AsIII at 0.5 μmol L−1 and high AsIII at IC50, 96 h) or AsV (low AsV at 0.5 μmol L–1; high AV at IC50, 96 h; when IC50, 96 h > 30 μmol L−1, 30 μmol L−1 is used) exposure.
Fig. 2: Intracellular arsenic concentration ([As]intra) of P. tricornutum, T. pseudonana, and C. mulleri selected under ambient and elevated pCO2 without arsenic exposure (Control), and with AsIII (low AsIII at 0.5 μmol L−1 and high AsIII at IC50, 96 h) or AsV (low AsV at 0.5 μmol L−1; high AV at IC50, 96 h; when IC50, 96 h > 30 μmol L−1, 30 μmol L−1 is used).
Fig. 3: Relative change of growth rates of the long-term selected P. tricornutum, T. pseudonana, and C. mulleri assayed at 400 µatm, 1000 µatm, and 2000 µatm pCO2 to growth rate of ambient selected samples assayed at 400 µatm in a reciprocal transplant experiment.
Fig. 4: Comparison of relative change of carbon-use efficiency (CUE) in P. tricornutum, T. pseudonana, and C. mulleri after long-term selection between indoor and outdoor experiments.
Fig. 5: Changes in arsenic concentration in scallop P. yessoensis fed with diatoms selected under ambient and elevated pCO2 with or without additive arsenic exposure in outdoor culture system.
Fig. 6: Diagram representing an altered arsenic pathway of P. tricornutum under elevated pCO2.

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Acknowledgements

This work was supported by National key research and development program of China (2018YFD0900703), National Natural Science Foundation of China (41976110); Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022019006, 2020TD27); Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (NO. 2018SDKJ0406-3); Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program (2019JZZY020706); Financial Fund of the Ministry of Agriculture and Rural Affairs, P.R. of China (NFZX2018); China Agriculture Research System (CARS-50); Taishan Scholars Funding and Talent Projects of Distinguished Scientific Scholars in Agriculture; Shandong Provincial Natural Science Foundation, China (ZR2017MD025); U.S. National Science Foundation grants (OCE 1638804, OCE 1538525).

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Correspondence to Naihao Ye.

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Xu, D., Schaum, CE., Li, B. et al. Acclimation and adaptation to elevated pCO2 increase arsenic resilience in marine diatoms. ISME J 15, 1599–1613 (2021). https://doi.org/10.1038/s41396-020-00873-y

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