Skip to main content
SpringerLink
Log in

Interactive effects of temperature and copper toxicity on photosynthetic efficiency and metabolic plasticity in Scenedesmus quadricauda (Chlorophyceae)

  • 8th Asian Pacific Phycological Forum
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Warming and copper (Cu) toxicity are two key abiotic stressors that strongly affect cell growth, photosynthetic rate, and metabolism in microalgae. In this study, a freshwater chlorophyte, Scenedesmus quadricauda, was exposed to various concentrations of copper sulfate (300, 600, and 1000 μM nominal concentrations of CuSO4·5H2O) at 25 and 35 °C. The changes in cell density, photosynthetic parameters, in vivo absorption spectra, reactive oxygen species (ROS) levels, and metabolic profile were analyzed. The effects of copper toxicity on the physiology and biochemistry of microalgae were highly dependent on water temperature. The interactive effects of both stressors induced significant impact on the photosynthetic parameters such as maximum quantum yield (Fv/Fm), saturation irradiance (Ek), and non-photochemical quenching (NPQ). Temperature induced significant impact on cell density, Ek and NPQ, while the Cu toxicity significantly affected the Fv/Fm and NPQ. Changes in the in vivo absorption spectra and high levels of reactive oxygen species (ROS) were observed across different treatments. Overall, S. quadricauda adapted to the two abiotic stresses via NPQ and metabolic restructuring. Key metabolites including glycine, proline, hexadecanoic acid, propanoic acid, octadecanoic acid, galactose, lactose, and sucrose were involved in the microalgal response. The synergistic effects of temperature and Cu stresses on microalgae might affect community tolerance and species distribution in the long run.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adams MS, Dillon CT, Vogt S, Lai B, Stauber J, Jolley DF (2016) Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy. Environ Sci Technol 50:8827–8839

    Article  CAS  Google Scholar 

  • Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-ur-Rehman M, Irshad MK, Bharwana SA (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    Article  CAS  Google Scholar 

  • Barati B, Lim P-E, Gan S-Y, Poong S-W, Phang S-M, Beardall J (2018) Effect of elevated temperature on the physiological responses of marine Chlorella strains from different latitudes. J Appl Phycol 30:1–13

    Article  Google Scholar 

  • Boyce DG, Lewis MR, Worm B (2010) Global phytoplankton decline over the past century. Nature 466:591–596

    Article  CAS  Google Scholar 

  • Cairns JJ, Heath AG, Parker BC (1975) Temperature influence on chemical toxicity to aquatic organisms. J Water Pollut Control Fed 47:267–280

    CAS  PubMed  Google Scholar 

  • Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C, Pellegrini M, Merchant SS (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23:1273–1292

    Article  CAS  Google Scholar 

  • Chen Y, Jiang X, Wang Y, Zhuang D (2017) Spatial characteristics of heavy metal pollution and the potential ecological risk of a typical mining area : a case study in China. Process Saf Environ Prot 113:204–219

    Article  Google Scholar 

  • Dai D, Gao Y, Chen J, Huang Y, Zhang Z, Xu F (2016) Time-resolved metabolomics analysis of individual differences during the early stage of lipopolysaccharide-treated rats. Sci Rep 6:34136

    Article  CAS  Google Scholar 

  • Dao LHT, Beardall J (2016) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429

    Article  CAS  Google Scholar 

  • Dewez D, Geoffroy L, Vernet G, Popovic R (2005) Determination of photosynthetic and enzymatic biomarkers sensitivity used to evaluate toxic effects of copper and fludioxonil in alga Scenedesmus obliquus. Aquat Toxicol 74:150–159

    Article  CAS  Google Scholar 

  • El-Sheekh M, Abomohra AE-F, El-Azim MA (2017) Effect of temperature on growth and fatty acids profile of the biodiesel producing microalga Scenedesmus acutus. Biotechnol Agron Soc Environ 21:233–239

    CAS  Google Scholar 

  • Fanesi A, Wagner H, Becker A, Wilhelm C (2016) Temperature affects the partitioning of absorbed light energy in freshwater phytoplankton. Freshw Biol 61:1365–1378

    Article  CAS  Google Scholar 

  • Fiehn O, Kopka J, Trethewey RN, Willmitzer L (2000) Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal Chem 72:3573–3580

    Article  CAS  Google Scholar 

  • Gowda H, Ivanisevic J, Johnson CH, Kurczy ME, Benton HP, Rinehart D, Nguyen T, Ray J, Kuehl J, Arevalo B, Westenskow PD, Wang J, Arkin AP, Deutschbauer AM, Patti GJ, Siuzdak G (2014) Interactive XCMS online: simplifying advanced metabolomic data processing and subsequent statistical analyses. Anal Chem 86:6931–6939

    Article  CAS  Google Scholar 

  • Häder D, Villafañe VE, Helbling EW (2014) Productivity of aquatic primary producers under global climate change. Photochem Photobiol Sci 13:1370–1392

    Article  Google Scholar 

  • Hamed SM, Selim S, Klöck G, AbdElgawad H (2017) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotoxicol Environ Saf 144:19–25

    Article  CAS  Google Scholar 

  • Harvey PJ, Handley HK, Taylor MP (2016) Widespread copper and lead contamination of household drinking water, New South Wales, Australia. Environ Res 151:275–285

    Article  CAS  Google Scholar 

  • He H, Chen F, Li H, Xiang W, Li Y, Jiang Y (2010) Effect of iron on growth, biochemical composition and paralytic shellfish poisoning toxins production of Alexandrium tamarense. Harmful Algae 9:98–104

    Article  CAS  Google Scholar 

  • Jamers A, Van der Ven K, Moens L, Robbens J, Potters G, Guisez Y, Blust R, De Con W (2006) Effect of copper exposure on gene expression profiles in Chlamydomonas reinhardtii based on microarray analysis. Aquat Toxicol 80:249–260

    Article  CAS  Google Scholar 

  • Jamers A, Blust R, De Coen W, Griffin JL, Jones OAH (2013a) Copper toxicity in the microalga Chlamydomonas reinhardtii: an integrated approach. Biometals 26:731–740

    Article  CAS  Google Scholar 

  • Jamers A, Blust R, De Coen W, Griffin JL, Jones OAH (2013b) An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 126:355–364

    Article  CAS  Google Scholar 

  • Jiang Y, Zhu Y, Hu Z, Lei A, Wang J (2016) Towards elucidation of the toxic mechanism of copper on the model green alga Chlamydomonas reinhardtii. Ecotoxicology 25:1417–1425

    Article  CAS  Google Scholar 

  • Khodami S, Surif M, Wan Maznah WO, Daryanabard R (2017) Assessment of heavy metal pollution in surface sediments of the Bayan Lepas area, Penang, Malaysia. Mar Pollut Bull 114:615–622

    Article  CAS  Google Scholar 

  • Kluender C, Sans-Piché F, Riedl J, Altenburger R, Härtig C, Laue G, Schmitt-Jansen M (2008) A metabolomics approach to assessing phytotoxic effects on the green alga Scenedesmus vacuolatus. Metabolomics 5:59–71

    Article  Google Scholar 

  • Knauer K, Behra R, Sigg L (1997) Effects of free Cu2+ and Zn2+ ions on growth and metal accumulation in freshwater algae. Environ Toxicol Chem 16:220–229

    Article  CAS  Google Scholar 

  • Knauert S, Knauer K (2008) The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Phycol 44:311–319

    Article  CAS  Google Scholar 

  • Kováčik J, Klejdus B, Babula P, Hedbavny J (2016) Age affects not only metabolome but also metal toxicity in Scenedesmus quadricauda cultures. J Hazard Mater 306:58–66

    Article  Google Scholar 

  • Kropat J, Gallaher SD, Urzica EI, Nakamoto SS, Strenkert D, Tottey S, Mason AZ, Merchant SS (2015) Copper economy in Chlamydomonas: prioritized allocation and reallocation of copper to respiration vs. photosynthesis. Proc Natl Acad Sci U S A 112:2644–2651

    Article  CAS  Google Scholar 

  • Küpper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133

    Article  Google Scholar 

  • Küpper H, Šetlík I, Šetliková E, Ferimazova N, Spiller M, Küpper FC (2003) Copper-induced inhibition of photosynthesis: limiting steps of in vivo copper chlorophyll formation in Scenedesmus quadricauda. Funct Plant Biol 30:1187–1196

    Article  Google Scholar 

  • Lambert AS, Dabrin A, Foulquier A, Morin S, Rosy C, Coquery M, Pesce S (2017) Influence of temperature in pollution-induced community tolerance approaches used to assess effects of copper on freshwater phototrophic periphyton. Sci Total Environ 607–608:1018–1025

    Article  Google Scholar 

  • Lee K-K, Lim P-E, Poong S-W, Wong C-Y, Phang S-M, Beardall J (2017) Growth and photosynthesis of Chlorella strains from polar, temperate and tropical freshwater environments under temperature stress. Chin J Oceanol Limnol

  • Leung PTY, Yi AX, Ip JCH, Mak SST, Leung KMY (2017) Photosynthetic and transcriptional responses of the marine diatom Thalassiosira pseudonana to the combined effect of temperature stress and copper exposure. Mar Pollut Bull 124:938–945

    Article  CAS  Google Scholar 

  • Li W, Xu X, Fujibayashi M, Niu Q, Tanaka N, Nishimura O (2016) Response of microalgae to elevated CO2 and temperature: impact of climate change on freshwater ecosystems. Environ Sci Pollut Res 23:19847–19860

    Article  CAS  Google Scholar 

  • Lozano P, Trombini C, Crespo E, Blasco J, Moreno-Garrido I (2014) ROI-scavenging enzyme activities as toxicity biomarkers in three species of marine microalgae exposed to model contaminants (copper, Irgarol and atrazine). Ecotoxicol Environ Saf 104:294–301

    Article  CAS  Google Scholar 

  • Malapascua J, Jerez C, Sergejevová M, Figueroa F, Masojídek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Biol 22:123–140

    Article  Google Scholar 

  • Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61

    Article  CAS  Google Scholar 

  • Morin S, Lambert AS, Rodriguez EP, Dabrin A, Coquery M, Pesce S (2017) Changes in copper toxicity towards diatom communities with experimental warming. J Hazard Mater 334:223–232

    Article  CAS  Google Scholar 

  • Müller E, Behra R, Sigg L (2016) Toxicity of engineered copper (Cu0) nanoparticles to the green alga Chlamydomonas reinhardtii. Environ Chem 13:457–463

    Article  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  Google Scholar 

  • Nalewajko C, Colman B, Olaveson M (1997) Effects of pH on growth, photosynthesis, respiration, and copper tolerance of three Scenedesmus strains. Environ Exp Bot 37:153–160

    Article  CAS  Google Scholar 

  • Nikinmaa M (2013) Climate change and ocean acidification—interactions with aquatic toxicology. Aquat Toxicol 126:365–372

    Article  CAS  Google Scholar 

  • Nowicka B, Pluciński B, Kuczyńska P, Kruk J (2016) Physiological characterization of Chlamydomonas reinhardtii acclimated to chronic stress induced by Ag, Cd, Cr, Cu and Hg ions. Ecotoxicol Environ Saf 130:133–145

    Article  CAS  Google Scholar 

  • Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986

    Article  CAS  Google Scholar 

  • OECD (2002) OECD guidelines for the testing of chemicals. 1–21

  • Olsson S, Puente-Sánchez F, Gómez MJ, Aguilera A (2015) Transcriptional response to copper excess and identification of genes involved in heavy metal tolerance in the extremophilic microalga Chlamydomonas acidophila. Extremophiles 19:657–672

    Article  CAS  Google Scholar 

  • Oukarroum A (2016) Alleviation of metal-induced toxicity in aquatic plants by exogenous compounds: a mini-review. Water Air Soil Pollut 227:204

    Article  Google Scholar 

  • Oukarroum A, Perreault F, Popovic R (2012) Interactive effects of temperature and copper on photosystem II photochemistry in Chlorella vulgaris. J Photochem Photobiol B 110:9–14

    Article  CAS  Google Scholar 

  • Perales-Vela HV, González-Moreno S, Montes-Horcasitas C, Cañizares-Villanueva RO (2007) Growth, photosynthetic and respiratory responses to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). Chemosphere 67:2274–2281

    Article  CAS  Google Scholar 

  • Phang S-M, Chu W-L (1999) University of Malaya Algae Culture Collection (UMACC). Catalogue of strains. Institute of Postgraduate Studies and Research, University of Malaya, Kuala Lumpur

  • Piotrowska-Niczyporuk A, Bajguz A, Talarek M, Bralska M, Zambrzycka E (2015) The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environ Sci Pollut Res 22:19112–19123

    Article  CAS  Google Scholar 

  • Sibi G, Anuraag TS, Bafila G (2014) Copper stress on cellular contents and fatty acid profiles in Chlorella species. Online J Biol Sci 14:209–217

    Article  Google Scholar 

  • Sunda W, Guillard RRL (1976) The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J Mar Res 34:511–529

    CAS  Google Scholar 

  • Suresh Kumar K, Dahms H-U, Lee J-S, Kim HC, Lee WC, Shin K-H (2014) Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotoxicol Environ Saf 104:51–71

    Article  CAS  Google Scholar 

  • Suresh Kumar K, Dahms HU, Won EJ, Lee JS, Shin KH (2015) Microalgae—a promising tool for heavy metal remediation. Ecotoxicol Environ Saf 113:329–352

    Article  CAS  Google Scholar 

  • Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539–544

    Article  Google Scholar 

  • Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544

    Article  CAS  Google Scholar 

  • Vavilin DV, Ducruet JM, Matorin DN, Venediktov PS, Rubin AB (1998) Membrane lipid peroxidation, cell viability and photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions. J Photochem Photobiol B 42:233–239

    Article  CAS  Google Scholar 

  • Walz H (2000) WinControl—Windows software for PAM Fluorometers user’s manual. Heinz Walz GmbH, Effeltrich

    Google Scholar 

  • Wang M-J, Wang W-X (2008) Temperature-dependent sensitivity of a marine diatom to cadmium stress explained by subcelluar distribution and thiol synthesis. Environ Sci Technol 42:8603–8608

    Article  CAS  Google Scholar 

  • Wang Y, Xu L, Shen H et al (2015) Metabolomic analysis with GC-MS to reveal potential metabolites and biological pathways involved in Pb &Cd stress response of radish roots. Sci Rep 5:18296

    Article  CAS  Google Scholar 

  • Wang H, Sathasivam R, Ki J (2017) Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments. Algae 32:131–137

    Article  CAS  Google Scholar 

  • Winder M, Sommer U (2012) Phytoplankton response to a changing climate. Hydrobiologia 698:5–16

    Article  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0––making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257

    Article  CAS  Google Scholar 

  • Xia L, Song S, Hu C (2016) High temperature enhances lipid accumulation in nitrogen-deprived Scenedesmus obtusus XJ-15. J Appl Phycol 28:831–837

    Article  CAS  Google Scholar 

  • Yong W-K, Tan Y-H, Poong S-W, Lim P-E (2016) Response of microalgae in a changing climate and environment. Malays J Sci 35:167–187

    Google Scholar 

  • Zhang W, Tan NGJ, Li SFY (2014) NMR-based metabolomics and LC-MS/MS quantification reveal metal-specific tolerance and redox homeostasis in Chlorella vulgaris. Mol BioSyst 10:149–160

    Article  CAS  Google Scholar 

  • Zhang W, Tan NGJ, Fua B, Li SFY (2015) Metallomics and NMR-based metabolomics of Chlorella sp. reveal synergistic role of copper and cadmium in multi-metal toxicity and oxidative stress. Metallomics 7:426–438

    Article  CAS  Google Scholar 

Download references

Acknowledgements

It is partly supported by Prof. Dong Wei from the Science and Technology Program in Marine and Fishery of Guangdong (Grant No. A201401C01) and the Science and Technology Program of Guangdong (Grant No. 2015A020216003, 2016A010105001), P.R. China.

Funding

Financial support from Ministry of Higher Education’s HICOE grant (IOES-2014H), Fundamental Research Grant Scheme (FP048-2016), University of Malaya PPP Grant (PG267-2016A), and University of Malaya Research University Grants (RU009F-2015 and RU009H-2015).

Author information

Authors and Affiliations

  1. Institute of Ocean and Earth Sciences, University of Malaya, Kuala Lumpur, Malaysia

    Wai-Kuan Yong, Sze-Wan Poong, Siew-Moi Phang & Phaik-Eem Lim

  2. Institute of Graduate Studies, University of Malaya, Kuala Lumpur, Malaysia

    Wai-Kuan Yong

  3. Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia

    Kae-Shin Sim & Siew-Moi Phang

  4. School of Food Sciences and Engineering, South China University of Technology, Guangzhou, 510640, People’s Republic of China

    Dong Wei

Authors
  1. Wai-Kuan Yong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kae-Shin Sim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sze-Wan Poong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Siew-Moi Phang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Phaik-Eem Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Phaik-Eem Lim.

Electronic supplementary material

Fig. S1

(PDF 219 kb)

Table S1

(PDF 82 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yong, WK., Sim, KS., Poong, SW. et al. Interactive effects of temperature and copper toxicity on photosynthetic efficiency and metabolic plasticity in Scenedesmus quadricauda (Chlorophyceae). J Appl Phycol 30, 3029–3041 (2018). https://doi.org/10.1007/s10811-018-1574-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1574-3

Keywords

Search

Navigation