Elevated CO2 reduces copper accumulation and toxicity in the diatom Thalassiosira pseudonana

The projected ocean acidification (OA) associated with increasing atmospheric CO2 alters seawater chemistry and hence the bio-toxicity of metal ions. However, it is still unclear how OA might affect the long-term resilience of globally important marine microalgae to anthropogenic metal stress. To explore the effect of increasing pCO2 on copper metabolism in the diatom Thalassiosira pseudonana (CCMP 1335), we employed an integrated eco-physiological, analytical chemistry, and transcriptomic approach to clarify the effect of increasing pCO2 on copper metabolism of Thalassiosira pseudonana across different temporal (short-term vs. long-term) and spatial (indoor laboratory experiments vs. outdoor mesocosms experiments) scales. We found that increasing pCO2 (1,000 and 2,000 μatm) promoted growth and photosynthesis, but decreased copper accumulation and alleviated its bio-toxicity to T. pseudonana. Transcriptomics results indicated that T. pseudonana altered the copper detoxification strategy under OA by decreasing copper uptake and enhancing copper-thiol complexation and copper efflux. Biochemical analysis further showed that the activities of the antioxidant enzymes glutathione peroxidase (GPX), catalase (CAT), and phytochelatin synthetase (PCS) were enhanced to mitigate oxidative damage of copper stress under elevated CO2. Our results provide a basis for a better understanding of the bioremediation capacity of marine primary producers, which may have profound effect on the security of seafood quality and marine ecosystem sustainability under further climate change.

[1]  J. Xia,et al.  Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs. , 2021, The Science of the total environment.

[2]  Fei-xue Fu,et al.  Acclimation and adaptation to elevated pCO2 increase arsenic resilience in marine diatoms , 2021, The ISME Journal.

[3]  Jun Sun,et al.  Transcriptomic reprogramming of the oceanic diatom Skeletonema dohrnii under warming ocean and acidification. , 2020, Environmental microbiology.

[4]  Stephen Depuydt,et al.  Assessment of five live-cell characteristics in periphytic diatoms as a measure of copper stress. , 2020, Journal of hazardous materials.

[5]  S. Egan,et al.  The effect of elevated pCO2 on cadmium resistance of a globally important diatom. , 2020, Journal of hazardous materials.

[6]  Hui Wang,et al.  Molecular characterization and expression analysis of copper‐zinc superoxide dismutases from the freshwater alga Closterium ehrenbergii under metal stress , 2020, Environmental toxicology.

[7]  A. Moenne,et al.  Isolation and Characterization of Copper- and Zinc- Binding Metallothioneins from the Marine Alga Ulva compressa (Chlorophyta) , 2019, International journal of molecular sciences.

[8]  Jiangxin Wang,et al.  Mitigation effects of CO2-driven ocean acidification on Cd toxicity to the marine diatom Skeletonema costatum. , 2019, Environmental pollution.

[9]  A. Falciatore,et al.  Diatom Molecular Research Comes of Age: Model Species for Studying Phytoplankton Biology and Diversity[OPEN] , 2019, Plant Cell.

[10]  R. Feely,et al.  Decadal variability in twentieth-century ocean acidification in the California Current Ecosystem , 2019, Nature Geoscience.

[11]  J. Camadro,et al.  Copper and iron metabolism in Ostreococcus tauri - the role of phytotransferrin, plastocyanin and a chloroplast copper-transporting ATPase. , 2019, Metallomics : integrated biometal science.

[12]  N. M. Price,et al.  A reduction‐dependent copper uptake pathway in an oceanic diatom , 2019, Limnology and Oceanography.

[13]  M. Wang,et al.  OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice , 2019, BMC Plant Biology.

[14]  F. Arenas,et al.  Interaction of short-term copper pollution and ocean acidification in seagrass ecosystems: Toxicity, bioconcentration and dietary transfer. , 2019, Marine pollution bulletin.

[15]  G. Lobos,et al.  Copper excess detoxification is mediated by a coordinated and complementary induction of glutathione, phytochelatins and metallothioneins in the green seaweed Ulva compressa. , 2019, Plant physiology and biochemistry : PPB.

[16]  Peter Kúš.  Experimental , 2019, Springer Theses.

[17]  T. Capo,et al.  Physiological responses of corals to ocean acidification and copper exposure. , 2018, Marine pollution bulletin.

[18]  C. Klausmeier,et al.  Rapid thermal adaptation in a marine diatom reveals constraints and trade‐offs , 2018, Global change biology.

[19]  K. Gao,et al.  Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2 , 2018, Global change biology.

[20]  N. Baliga,et al.  Ocean acidification conditions increase resilience of marine diatoms , 2018, Nature Communications.

[21]  Fei-xue Fu,et al.  Responses of the large centric diatom Coscinodiscus sp. to interactions between warming, elevated CO2, and nitrate availability , 2018 .

[22]  H. Küpper,et al.  Trace metal metabolism in plants. , 2018, Journal of experimental botany.

[23]  K. Leung,et al.  Photosynthetic and transcriptional responses of the marine diatom Thalassiosira pseudonana to the combined effect of temperature stress and copper exposure. , 2017, Marine pollution bulletin.

[24]  Fei-xue Fu,et al.  Individual and interactive effects of warming and CO 2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica , two dominant phytoplankton from the Ross Sea, Antarctica , 2017 .

[25]  Brad M. Angel,et al.  Time-averaged concentrations are effective for predicting chronic toxicity of varying copper pulse exposures for two freshwater green algae species. , 2017, Environmental pollution.

[26]  L. Guidi,et al.  The evolution of diatoms and their biogeochemical functions , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  N. Colegrave,et al.  Evolutionary consequences of multidriver environmental change in an aquatic primary producer , 2017, Proceedings of the National Academy of Sciences.

[28]  A. Djurišić,et al.  Influences of temperature and salinity on physicochemical properties and toxicity of zinc oxide nanoparticles to the marine diatom Thalassiosira pseudonana , 2017, Scientific Reports.

[29]  S. Dupont,et al.  Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity , 2017, Nature Ecology &Evolution.

[30]  Guang Gao,et al.  Expected CO2-induced ocean acidification modulates copper toxicity in the green tide alga Ulva prolifera , 2017 .

[31]  K. Gao,et al.  Decreased photosynthesis and growth with reduced respiration in the model diatom Phaeodactylum tricornutum grown under elevated CO2 over 1800 generations , 2017, Global change biology.

[32]  Fei-xue Fu,et al.  Individual and interactive effects of warming and CO 2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica , two dominant phytoplankton from the Ross Sea, Antarctica , 2017 .

[33]  P R Jayachandran,et al.  Toxicity effects of copper on the marine diatom, Chaetoceros calcitrans , 2016 .

[34]  S. Collins.  Growth rate evolution in improved environments under Prodigal Son dynamics , 2016, Evolutionary applications.

[35]  Jiangxin Wang,et al.  Towards elucidation of the toxic mechanism of copper on the model green alga Chlamydomonas reinhardtii , 2016, Ecotoxicology.

[36]  Naoki Yamaji,et al.  A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain , 2016, Nature Communications.

[37]  U. Riebesell,et al.  Long-term dynamics of adaptive evolution in a globally important phytoplankton species to ocean acidification , 2016, Science Advances.

[38]  S. Lofts,et al.  Effect of Ocean Acidification on Organic and Inorganic Speciation of Trace Metals. , 2016, Environmental science & technology.

[39]  T. A. DelValls,et al.  Simulating CO₂ leakages from CCS to determine Zn toxicity using the marine microalgae Pleurochrysis roscoffensis. , 2016, Chemosphere.

[40]  A. Richel,et al.  Effect of Metals, Metalloids and Metallic Nanoparticles on Microalgae Growth and Industrial Product Biosynthesis: A Review , 2015, International journal of molecular sciences.

[41]  A. Ivanina,et al.  Interactive effects of metal pollution and ocean acidification on physiology of marine organisms , 2015 .

[42]  F. Joos,et al.  Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios , 2015, Science.

[43]  M. T. Maldonado,et al.  Sequence analysis and gene expression of potential components of copper transport and homeostasis in Thalassiosira pseudonana. , 2015, Protist.

[44]  U. Riebesell,et al.  Adaptation of a globally important coccolithophore to ocean warming and acidification , 2014 .

[45]  Stephanie Mangan,et al.  Ocean acidification increases copper toxicity to the early life history stages of the polychaete Arenicola marina in artificial seawater. , 2014, Environmental science & technology.

[46]  V. Brotas,et al.  Effects of ultraviolet radiation and CO2 increase on winter phytoplankton assemblages in a temperate coastal lagoon , 2014 .

[47]  A. Irwin,et al.  Ocean acidification enhances the growth rate of larger diatoms , 2014 .

[48]  I. Riba,et al.  Effects on the mobility of metals from acidification caused by possible CO₂ leakage from sub-seabed geological formations. , 2014, The Science of the total environment.

[49]  J. Salisbury,et al.  Ocean acidification in the coastal zone from an organism's perspective: multiple system parameters, frequency domains, and habitats. , 2014, Annual review of marine science.

[50]  P. Boyd,et al.  EXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON , 2013, Evolution; international journal of organic evolution.

[51]  C. Lewis,et al.  Ocean acidification increases the toxicity of contaminated sediments , 2013, Global change biology.

[52]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[53]  Z. Yang,et al.  Alleviation of Copper-Induced Oxidative Damage in Chlamydomonas reinhardtii by Carbon Monoxide , 2011, Archives of environmental contamination and toxicology.

[54]  J. Raven,et al.  Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change , 2011, Photosynthesis Research.

[55]  F. Morel,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Efficiency of the CO2-concentrating mechanism of diatoms , 2011 .

[56]  D. Wallace,et al.  MS Excel Program Developed for CO2 System Calculations , 2011 .

[57]  Brian M. Hopkinson,et al.  Effect of Ocean Acidification on Iron Availability to Marine Phytoplankton , 2010, Science.

[58]  F. Millero,et al.  Effect of ocean acidification on the speciation of metals in seawater , 2009 .

[59]  E. Virginia Armbrust,et al.  The life of diatoms in the world's oceans , 2009, Nature.

[60]  M. Hildebrand,et al.  Gene Expression Induced by Copper Stress in the Diatom Thalassiosira pseudonana , 2006, Eukaryotic Cell.

[61]  Graham Bell,et al.  Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga , 2004, Nature.

[62]  Nicholas H. Putnam,et al.  The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism , 2004, Science.

[63]  Richard A. Feely,et al.  Impact of Anthropogenic CO2 on the CaCO3 System in the Oceans , 2004, Science.