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


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.


  1. 1.

    Valenzuela JJ, de Lomana ALG, Lee A, Armbrust EV, Orellana MV, Baliga NS. Ocean acidification conditions increase resilience of marine diatoms. Nat Commun. 2018;9:2328.

    PubMed  PubMed Central  Google Scholar 

  2. 2.

    Ivanina AV, Sokolova IM. Interactive effects of metal pollution and ocean acidification on physiology of marine organisms. Curr Zool. 2015;61:653–68.

    Google Scholar 

  3. 3.

    Stockdale A, Tipping E, Lofts S, Mortimer RJ. The effect of ocean acidification on organic and inorganic of trace metals. Environ Sci Technol. 2016;50:1906–13.

    CAS  PubMed  Google Scholar 

  4. 4.

    Murcott S. Arsenic contamination in the world. London, New York: IWA publishing; 2012.

  5. 5.

    Pan K, Wang WX. Trace metal contamination in estuarine and coastal environments in China. Sci Total Environ. 2012;421:3–16.

    PubMed  Google Scholar 

  6. 6.

    NBSC. National Bureau of Statistics of China. Beijing: China Statistical Yearbook; 2001–2009.

  7. 7.

    Nordstrom DK. Worldwide occurrences of arsenic in ground water. Science. 2002;296:2143–5.

    CAS  PubMed  Google Scholar 

  8. 8.

    Cutter GA, Cutter LS, Featherstone AM, Lohrenz SE. Antimony and arsenic biogeochemistry in the western Atlantic Ocean. Deep-Sea Res Pt II. 2001;48:2895–915.

    CAS  Google Scholar 

  9. 9.

    Yunus SM, Hamzah Z, Wood AKH, Saat A. Natural radionuclides and heavy metals pollution in seawater at kuala langat coastal area. Malays J Anal Sci. 2015;19:766–74.

    Google Scholar 

  10. 10.

    Sanders JG. Role of marine phytoplankton in determining the chemical speciation and biogeochemical cycling of arsenic. Can J Fish Aquat Sci. 1983;40:192–6.

    Google Scholar 

  11. 11.

    Wang Y, Zhang C, Zheng Y, Ge Y. Phytochelatin synthesis in Dunaliella salina induced by arsenite and arsenate under various phosphate regimes. Ecotox Environ Safe. 2017;136:150–60.

    CAS  Google Scholar 

  12. 12.

    Fru EC, Arvestål E, Callac N, El Albani A, Kilias S, Argyraki A, et al. Arsenic stress after the Proterozoic glaciations. Sci Rep. 2015;5:17789.

    PubMed  Google Scholar 

  13. 13.

    Saunders JK, Rocap G. Genomic potential for arsenic efflux and methylation varies among global Prochlorococcus populations. ISME J. 2016;10:197–209.

    CAS  PubMed  Google Scholar 

  14. 14.

    Zhao FJ, Ma JF, Meharg AA, McGrath SP. Arsenic uptake and metabolism in plants. N Phytol. 2009;181:777–94.

    CAS  Google Scholar 

  15. 15.

    Ye J, Rensing C, Rosen BP, Zhu YG. Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci. 2012;17:155–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA. 2008;105:9931–5.

    CAS  PubMed  Google Scholar 

  17. 17.

    Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob Biogeochem Cycles. 1995;9:359.

    CAS  Google Scholar 

  18. 18.

    Crawfurd KJ, Raven JA, Wheeler GL, Baxter EJ, Joint I. The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PloS ONE. 2011;6:e26695.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Wu Y, Campbell DA, Irwin AJ, Suggett DJ, Finkel ZV. Ocean acidification enhances the growth rate of larger diatoms. Limnol Oceanogr. 2014;59:1027–34.

    CAS  Google Scholar 

  20. 20.

    Domingues RB, Guerra CC, Barbosa AB, Brotas V, Galvão HM. Effects of ultraviolet radiation and CO2 increase on winter phytoplankton assemblages in a temperate coastal lagoon. J Plankton Res. 2014;36:672–84.

    CAS  Google Scholar 

  21. 21.

    Heydarizadeh P, Boureba W, Zahedi M, Huang B, Moreau B, Lukomska E, et al. Response of CO2-starved diatom Phaeodactylum tricornutum to light intensity transition. Philos Trans R Soc B. 2017;372:20160396.

    Google Scholar 

  22. 22.

    Heydarizadeh P, Veidl B, Huang B, Lukomska E, Wielgosz-Collin G, Couzinet-Mossion A, et al. Carbon orientation in the diatom Phaeodactylum tricornutum: the effects of carbon limitation and photon flux density. Front Plant Sci. 2019;10:471.

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam N, et al. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science. 2004;459:79–86.

    Google Scholar 

  24. 24.

    Armbrust EV. The life of diatoms in the world’s oceans. Nature. 2009;459:185–92.

    CAS  PubMed  Google Scholar 

  25. 25.

    Rastogi A, Vieira FRJ, Deton-Cabanillas A, Veluchamy A, Cantrel C, Wang G, et al. A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum. ISME J. 2020;14:347–63.

    PubMed  Google Scholar 

  26. 26.

    Liang C, Zhang Y, Wang L, Shi L, Xu D, Zhang X, et al. Features of metabolic regulation revealed by transcriptomic adaptions driven by long‐term elevated pCO2 in Chaetoceros muelleri. Phycol Res. 2020;68:236–48.

    CAS  Google Scholar 

  27. 27.

    Uddin S, Bebhehani M, Al-Musallam L, Kumar VV, Sajid S. Po uptake in microalgae at different seawater pH: An experimental study simulating ocean acidification. Mar Pollut Bull. 2020;151:110844.

    CAS  PubMed  Google Scholar 

  28. 28.

    Pierrot D, Lewis E, Wallace D. MS Excel program developed for CO2 system calculations ORNL/CDIAC-105a. Oak Ridge, Tennessee: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy; 2006.

  29. 29.

    Karadjova IB, Slaveykova VI, Tsalev DL. The biouptake and toxicity of arsenic species on the green microalga Chlorella salina in seawater. Aquat Toxicol. 2008;87:264e271.

    Google Scholar 

  30. 30.

    Hirata S, Toshimitsu H. Determination of arsenic species and arsenosugars in marine samples by HPLC-ICP-MS. Appl Organomet Chem. 2007;21:447–54.

    CAS  Google Scholar 

  31. 31.

    Yan Y, Ye J, Xue XM, Zhu YG. Arsenic demethylation by a C·As lyase in cyanobacterium nostoc sp.PCC 7120. Environ Sci Technol. 2015;49:14350–8.

    CAS  PubMed  Google Scholar 

  32. 32.

    Guo YQ, Xue XM, Yan Y, Zhu YG, Yang GD, Ye J, et al. Arsenic methylation by an arsenite s-adenosylmethionine methyltransferase from spirulina platensis. J Environ Sci. 2016;49:162–8.

    CAS  Google Scholar 

  33. 33.

    Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun. 2018;9:1719.

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Li P, Pan Y, Fang Y, Du M, Pei F, Shen F, et al. Concentrations and health risks of inorganic arsenic and methylmercury in shellfish from typical coastal cities in China: a simultaneous analytical method study. Food Chem. 2019;278:587–92.

    CAS  PubMed  Google Scholar 

  35. 35.

    R Core Development Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014.

  36. 36.

    de Orte MR, Sarmiento AM, Basallote MD, Rodríguez-Romero A, Riba I. Effects on the mobility of metals from acidification caused by possible CO2 leakage from sub-seabed geological formations. Sci Total Environ. 2014;470:356–63.

    PubMed  Google Scholar 

  37. 37.

    Qu P, Fu FX, Hutchins DA. Responses of the large centric diatom Coscinodiscus sp to interactions between warming, elevated CO2, and nitrate availability. Limnol Oceanogr. 2018;63:1407–24.

    CAS  Google Scholar 

  38. 38.

    Zhu Z, Qu P, Gale J, Fu FX, Hutchins DA. Individual and interactive effects of warming and CO2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica, two dominant phytoplankton from the Ross Sea, Antarctica. Biogeosciences. 2017;14:1–15.

    Google Scholar 

  39. 39.

    Collins S. Growth rate evolution in improved environments under Prodigal Son dynamics. Evol Appl. 2016;9:1179–88.

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Amin SA, Hmelo LR, Van Tol HM, Durham BP, Carlson LT, Heal K, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.

    CAS  PubMed  Google Scholar 

  41. 41.

    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Zhu YG, Xue XM, Kappler A, Rosen BP, Meharg AA. Linking genes to microbial biogeochemical cycling: lessons from arsenic. Environ Sci Technol. 2017;51:7326–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Lefebvre SC, Benner I, Stillman JH, Parker AE, Drake MK, Rossignol PE, et al. Nitrogen source and pCO2 synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle. Glob Change Biol. 2012;18:493–503.

    Google Scholar 

  44. 44.

    MillerO FJ, Woosley R, Ditrolio B, Waters J. Effect of ocean acidification on the speciation of metals in seawater. Oceanography. 2009;22:72–85.

    Google Scholar 

  45. 45.

    Bautista-Chamizo E, De Orte MR, DelValls TA, Riba I. Simulating CO2 leakages from CCS to determine Zn toxicity using the marine microalgae Pleurochrysis roscoffensis. Chemosphere. 2016;144:955–65.

    CAS  PubMed  Google Scholar 

  46. 46.

    Zhang XS, Xu D, Huang SJ, Wang SH, Han WT, Liang CW, et al. The effect of elevated pCO2 on cadmium resistance of a globally important diatom. J Hazard Mater. 2020;396:122749.

    CAS  PubMed  Google Scholar 

  47. 47.

    Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.

    CAS  PubMed  Google Scholar 

  48. 48.

    Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. Proc Biol Sci. 2014;281:20141486.

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Spalding MH, Van K, Wang Y, Nakamura Y. Acclimation of Chlamydomonas to changing carbon availability. Funct Plant Biol. 2002;29:221–30.

    CAS  PubMed  Google Scholar 

  50. 50.

    Raven JA, Giordano M, Beardall J, Maberly SC. Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res. 2011;109:281–96.

    CAS  PubMed  Google Scholar 

  51. 51.

    IGBP, IOC, SCOR. Ocean acidification summary for policymakers—third symposium on the ocean in a high-CO2 world. Stockholm, Sweden: International Geosphere-Biosphere Programme; 2013.

    Google Scholar 

  52. 52.

    Liu NN, Tong SY, Yi XQ, Li Y, Li ZZ, Miao HB, et al. Carbon assimilation and losses during an ocean acidification mesocosm experiment, with special reference to algal blooms. Mar Environ Res. 2017;129:229–35.

    CAS  PubMed  Google Scholar 

  53. 53.

    D’Amario B, Pérez C, Grelaud M, Pitta P, Krasakopoulou E, Ziveri P. Coccolithophore community response to ocean acidification and warming in the Eastern Mediterranean Sea: results from a mesocosm experiment. Sci Rep. 2020;10:1–14.

    Google Scholar 

  54. 54.

    Hussain MM, Wang J, Bibi I, Shahid M, Niazi NK, Iqbal J, et al. Arsenic speciation and biotransformation pathways in the aquatic ecosystem: the significance of algae. J Hazard Mater. 2020;403:124027.

    PubMed  Google Scholar 

  55. 55.

    Huang JH. Arsenic trophodynamics along the food chains/webs of different ecosystems: a review. Chem Ecol. 2016;32:803–28.

    Google Scholar 

  56. 56.

    Heijne WH, Kienhuis AS, Van Ommen B, Stierum RH, Groten JP. Systems toxicology: applications of toxicogenomics, transcriptomics, proteomics and metabolomics in toxicology. Expert Rev Proteomic. 2005;2:767–80.

    CAS  Google Scholar 

  57. 57.

    Tsai SL, Singh S, Chen W. Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Curr Opin Biotech. 2009;20:659–67.

    CAS  PubMed  Google Scholar 

  58. 58.

    Petrou K, Baker KG, Nielsen DA, Hancock AM, Schulz GK, Davidson AT. Acidification diminishes diatom silica production in the Southern Ocean. Nat Clim Change. 2019;9:781–6.

    CAS  Google Scholar 

  59. 59.

    Milligan AJ, Morel FM. A proton buffering role for silica in diatoms. Science. 2002;297:1848–50.

    CAS  PubMed  Google Scholar 

  60. 60.

    Collins S, Rost B, Rynearson TA. Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl. 2014;7:140–55.

    CAS  PubMed  Google Scholar 

  61. 61.

    Reusch TBH, Boyd PW. Experimental evolution meets marine phytoplankton. Evolution. 2013;67:1849–59.

    PubMed  Google Scholar 

  62. 62.

    Hutchins DA, Fu FX. Microorganisms and ocean global change. Nat Microbiol. 2017;2:17508.

    Google Scholar 

  63. 63.

    Lohbeck KT, Riebesell U, Reusch TBH. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci. 2012;5:346–51.

    CAS  Google Scholar 

  64. 64.

    Conover DO, Schultz ET. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol. 1995;10:248–52.

    CAS  PubMed  Google Scholar 

  65. 65.

    Griffin KL, Anderson OR, Gastrich MD, Lewis JD, Lin G, Schuster W, et al. Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure. Proc Natl Acad Sci USA. 2001;98:2473–8.

    CAS  PubMed  Google Scholar 

  66. 66.

    Sültemeyer D. Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot. 1998;76:962–72.

    Google Scholar 

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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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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).

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