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.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
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.
Ivanina AV, Sokolova IM. Interactive effects of metal pollution and ocean acidification on physiology of marine organisms. Curr Zool. 2015;61:653–68.
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.
Murcott S. Arsenic contamination in the world. London, New York: IWA publishing; 2012.
Pan K, Wang WX. Trace metal contamination in estuarine and coastal environments in China. Sci Total Environ. 2012;421:3–16.
NBSC. National Bureau of Statistics of China. Beijing: China Statistical Yearbook; 2001–2009.
Nordstrom DK. Worldwide occurrences of arsenic in ground water. Science. 2002;296:2143–5.
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.
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.
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.
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.
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.
Saunders JK, Rocap G. Genomic potential for arsenic efflux and methylation varies among global Prochlorococcus populations. ISME J. 2016;10:197–209.
Zhao FJ, Ma JF, Meharg AA, McGrath SP. Arsenic uptake and metabolism in plants. N Phytol. 2009;181:777–94.
Ye J, Rensing C, Rosen BP, Zhu YG. Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci. 2012;17:155–62.
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.
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.
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.
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.
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.
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.
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.
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.
Armbrust EV. The life of diatoms in the world’s oceans. Nature. 2009;459:185–92.
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.
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.
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.
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.
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.
Hirata S, Toshimitsu H. Determination of arsenic species and arsenosugars in marine samples by HPLC-ICP-MS. Appl Organomet Chem. 2007;21:447–54.
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.
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.
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.
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.
R Core Development Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014. https://www.R-project.org/.
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.
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.
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.
Collins S. Growth rate evolution in improved environments under Prodigal Son dynamics. Evol Appl. 2016;9:1179–88.
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.
Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.
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.
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.
MillerO FJ, Woosley R, Ditrolio B, Waters J. Effect of ocean acidification on the speciation of metals in seawater. Oceanography. 2009;22:72–85.
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.
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.
Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.
Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. Proc Biol Sci. 2014;281:20141486.
Spalding MH, Van K, Wang Y, Nakamura Y. Acclimation of Chlamydomonas to changing carbon availability. Funct Plant Biol. 2002;29:221–30.
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.
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.
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.
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.
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.
Huang JH. Arsenic trophodynamics along the food chains/webs of different ecosystems: a review. Chem Ecol. 2016;32:803–28.
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.
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.
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.
Milligan AJ, Morel FM. A proton buffering role for silica in diatoms. Science. 2002;297:1848–50.
Collins S, Rost B, Rynearson TA. Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl. 2014;7:140–55.
Reusch TBH, Boyd PW. Experimental evolution meets marine phytoplankton. Evolution. 2013;67:1849–59.
Hutchins DA, Fu FX. Microorganisms and ocean global change. Nat Microbiol. 2017;2:17508.
Lohbeck KT, Riebesell U, Reusch TBH. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci. 2012;5:346–51.
Conover DO, Schultz ET. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol. 1995;10:248–52.
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.
Sültemeyer D. Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot. 1998;76:962–72.
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-020-00873-y
This article is cited by
-
Phytoplankton community shift in response to experimental Cu addition at the elevated CO2 levels (Arabian Sea, winter monsoon)
Environmental Science and Pollution Research (2023)
