3 Biotech

, 9:315 | Cite as

Physiological and metabolic responses of Scenedesmus quadricauda (Chlorophyceae) to nickel toxicity and warming

  • Wai-Kuan Yong
  • Kae-Shin Sim
  • Sze-Wan Poong
  • Dong Wei
  • Siew-Moi Phang
  • Phaik-Eem LimEmail author
Original Article


An ecologically important tropical freshwater microalga, Scenedesmus quadricauda, was exposed to Ni toxicity under two temperature regimes, 25 and 35 °C to investigate the interactive effects of warming and different Ni concentrations (0.1, 1.0 and 10.0 ppm). The stress responses were assessed from the growth, photosynthesis, reactive oxygen species (ROS) generation and metabolomics aspects to understand the effects at both the physiological and biochemical levels. The results showed that the cell densities of the cultures were higher at 35 °C compared to 25 °C, but decreased with increasing Ni concentrations at 35 °C. In terms of photosynthetic efficiency, the maximum quantum yield of photosystem II (Fv/Fm) of S. quadricauda remained consistent across different conditions. Nickel concentration at 10.0 ppm affected the maximum rate of relative electron transport (rETRm) and saturation irradiance for electron transport (Ek) in photosynthesis. At 25 °C, the increase of non-photochemical quenching (NPQ) values in cells exposed to 10.0 ppm Ni might indicate the onset of thermal dissipation process as a self-protection mechanism against Ni toxicity. The combination of warming and Ni toxicity induced a strong oxidative stress response in the cells. The ROS level increased significantly by 40% after exposure to 10.0 ppm of Ni at 35 °C. The amount of Ni accumulated in the biomass was higher at 25 °C compared to 35 °C. Based on the metabolic profile, temperature contributed the most significant differentiation among the samples compared to Ni treatment and the interaction between the two factors. Amino acids, sugars and organic acids were significantly regulated by the combined factors to restore homeostasis. The most affected pathways include sulphur, amino acids, and nitrogen metabolisms. Overall, the results suggest that the inhibitory effect of Ni was lower at 35 °C compared to 25 °C probably due to lower metal uptake and primary metabolism restructuring. The ability of S. quadricauda to accumulate substantial amount of Ni and thrive at 35 °C suggests the potential use of this strain for phycoremediation and outdoor wastewater treatment.


Nickel toxicity Global warming Scenedesmus Microalgae Photosynthesis Metabolomics 



We appreciate financial support from Ministry of 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 (RU009H-2015 and TU001C-2018).

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

13205_2019_1848_MOESM1_ESM.tif (6.7 mb)
Fig. S1 Relative electron transport rate (rETR) vs irradiance (PAR) for Scenedesmus quadricauda (mean ± SD, n = 3) exposed to various nickel concentrations at 25 and 35 °C (TIFF 6899 kb)
13205_2019_1848_MOESM2_ESM.tif (12.7 mb)
Fig. S2 Results of ANOVA simultaneous component analysis (ASCA) showing the major patterns associated with temperature, concentration of nickel, and their interaction for (A) GCMS, (B) LC-positive and (C) LC-negative data set (TIFF 12956 kb)
13205_2019_1848_MOESM3_ESM.docx (12 kb)
Supplementary material 3 (DOCX 13 kb)
13205_2019_1848_MOESM4_ESM.docx (13 kb)
Supplementary material 4 (DOCX 12 kb)
13205_2019_1848_MOESM5_ESM.docx (16 kb)
Supplementary material 5 (DOCX 15 kb)


  1. 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 50:8827–8839CrossRefGoogle Scholar
  2. Ahmed H, Häder DP (2010) Rapid ecotoxicological bioassay of nickel and cadmium using motility and photosynthetic parameters of Euglena gracilis. Environ Exp Bot 69:68–75CrossRefGoogle Scholar
  3. Aksu Z (2002) Determination of the equilibrium, kinetic and thermodynamic parameters of the batch biosorption of nickel(II) ions onto Chlorella vulgaris. Process Biochem 38:89–99CrossRefGoogle Scholar
  4. 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 30:1–13CrossRefGoogle Scholar
  5. Binet MT, Adams MS, Gissi F, Golding LA, Schlekat CE, Garman ER, Merrington G, Stauber JL (2018) Toxicity of nickel to tropical freshwater and sediment biota: a critical literature review and gap analysis. Environ Toxicol Chem 37(2):293–317CrossRefGoogle Scholar
  6. Booth SC, Workentine ML, Weljie AM, Turner RJ (2011) Metabolomics and its application to studying metal toxicity. Metallomics 3:1142–1152CrossRefGoogle Scholar
  7. Cempel M, Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15(3):375–382Google Scholar
  8. Chong AMY, Wong YS, Tam NFY (2000) Performance of different microalgal species in removing nickel and zinc from industrial wastewater. Chemosphere 41(1–2):251–257CrossRefGoogle Scholar
  9. Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46(Web Server Issue):W486–W494CrossRefGoogle Scholar
  10. Dao LHT, Beardall J (2016) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429CrossRefGoogle Scholar
  11. Fanesi A, Wagner H, Becker A, Wilhelm C (2016) Temperature affects the partitioning of absorbed light energy in freshwater phytoplankton. Freshw Biol 61:1365–1378CrossRefGoogle Scholar
  12. Gong N, Shao K, Feng W, Lin Z, Liang C, Sun Y (2011) Biotoxicity of nickel oxide nanoparticles and bio-remediation by microalgae Chlorella vulgaris. Chemosphere 83(4):510–516CrossRefGoogle Scholar
  13. Hanagata N, Takeuchia T, Fukuju Y, Barnesa DJ, Karube I (1992) Tolerance of microalgae to high CO2 and high temperature. Phytochemistry 31(10):3345–3348CrossRefGoogle Scholar
  14. Huang XG, Sx Li, Liu FJ, Lan WR (2018) Regulated effects of Prorocentrum donghaiense Lu exudate on nickel bioavailability when cultured with different nitrogen sources. Chemosphere 197:57–64CrossRefGoogle Scholar
  15. Kaplan DL (2013) Absorption and adsorption of heavy metals by microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, New York, pp 602–611CrossRefGoogle Scholar
  16. Kaur S, Srivastava A, Kumar S, Srivastava V (2019) Biochemical and proteomic analysis reveals oxidative stress tolerance strategies of Scenedesmus abundans against allelochemicals released by Microcystis aeruginosa. Algal Res 41:101525CrossRefGoogle Scholar
  17. Koppel DJ, Gissi F, Adams MS, King CK, Jolley DF (2017) Chronic toxicity of five metals to the polar marine microalga Cryothecomonas armigera—application of a new bioassay. Environ Pollut 228:211–221CrossRefGoogle Scholar
  18. 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. J Oceanol Limnol 36(4):1266–1279CrossRefGoogle Scholar
  19. Levy JL, Stauber JL, Jolley DF (2007) Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci Total Environ 387:141–154CrossRefGoogle Scholar
  20. Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow QA, Jones DP, Pulendran B (2013) Predicting network activity from high throughput metabolomics. PLoS Comput Biol 9(7):e1003123CrossRefGoogle Scholar
  21. Martínez-Ruiz EB, Martínez-Jerónimo F (2015) Nickel has biochemical, physiological, and structural effects on the green microalga Ankistrodesmus falcatus: an integrative study. Aquat Toxicol 169:27–36CrossRefGoogle Scholar
  22. Miazek K, Iwanek W, Remacle C, Richel A, Goffin D (2015) Effect of metals, metalloids and metallic nanoparticles on microalgae growth and industrial product biosynthesis: a review. Int J Mol Sci 16:23929–23969CrossRefGoogle Scholar
  23. Mohd Udaiyappan AF, Abu Hasan H, Takriff MS, Sheikh Abdullah SR (2017) A review of the potentials, challenges and current status of microalgae biomass applications in industrial wastewater treatment. J Water Process Eng 20:8–21CrossRefGoogle Scholar
  24. Mondal M, Halder G, Oinam G, Indrama T, Tiwari ON (2019) Bioremediation of organic and inorganic pollutants using microalgae. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Amsterdam, Elsevier, pp 223–235CrossRefGoogle Scholar
  25. Muyssen BTA, Brix KV, DeForest DK, Janssen CR (2004) Nickel essentiality and homeostasis in aquatic organisms. Environ Rev 12(2):113–131CrossRefGoogle Scholar
  26. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  27. Nikinmaa M (2013) Climate change and ocean acidification—interactions with aquatic toxicology. Aquat Toxicol 126:365–372CrossRefGoogle Scholar
  28. Oukarroum A, Polchtchikov S, Perreault F, Popovic R (2012) Temperature influence on silver nanoparticles inhibitory effect on photosystem II photochemistry in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Environ Sci Pollut Res 19:1755–1762CrossRefGoogle Scholar
  29. Oukarroum A, Zaidi W, Samadani M, Dewez D (2017) Toxicity of nickel oxide nanoparticles on a freshwater green algal strain of Chlorella vulgaris. Biomed Res Int 2017:8CrossRefGoogle Scholar
  30. 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 LumpurGoogle Scholar
  31. Rodriguez IB, Ho T-Y (2014) Diel nitrogen fixation pattern of Trichodesmium: the interactive control of light and Ni. Sci Rep 4(4445):1–5Google Scholar
  32. Santos FM, Mazur LP, Mayer DA, Vilar VJP, Pires JCM (2019) Inhibition effect of zinc, cadmium, and nickel ions in microalgal growth and nutrient uptake from water: an experimental approach. Chem Eng J 366:358–367CrossRefGoogle Scholar
  33. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53(2):257–277CrossRefGoogle Scholar
  34. Singh V, Verma K (2018) Metals from cell to environment: connecting metallomics with other omics. Open J Plant Sci 3(1):1–14Google Scholar
  35. Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics and ionomics. Front Plant Sci 6:1143PubMedPubMedCentralGoogle Scholar
  36. Strejckova A, Dvorak M, Klejdus B, Krystofova O, Hedbavny J, Adam V, Huska D (2019) The strong reaction of simple phenolic acids during oxidative stress caused by nickel, cadmium and copper in the microalga Scenedesmus quadricauda. N Biotechnol 48:66–75CrossRefGoogle Scholar
  37. Suresh Kumar K, Dahms HU, Won EJ, Lee JS, Shin KH (2015) Microalgae—a promising tool for heavy metal remediation. Ecotoxicol Environ Saf 113:329–352CrossRefGoogle Scholar
  38. Tripathi R, Gupta A, Thakur IS (2019) An integrated approach for phycoremediation of wastewater and sustainable biodiesel production by green microalgae, Scenedesmus sp. ISTGA1. Renew Energy 135:617–625CrossRefGoogle Scholar
  39. Väänänen K, Leppänen MT, Chen X, Akkanen J (2018) Metal bioavailability in ecological risk assessment of freshwater ecosystems: from science to environmental management. Ecotoxicol Environ Saf 147:430–446CrossRefGoogle Scholar
  40. Van Ginneken M, Blust R, Bervoets L (2019) The impact of temperature on metal mixture stress: sublethal effects on the freshwater isopod Asellus aquaticus. Environ Res 169:52–61CrossRefGoogle Scholar
  41. Walz H (2000) WinControl—Windows software for PAM Fluorometers users manualGoogle Scholar
  42. Wang L, Huang X, Lim DJ, Laserna AKC, Fong SYL (2019a) Uptake and toxic effects of triphenyl phosphate on freshwater microalgae Chlorella vulgaris and Scenedesmus obliquus: insights from untargeted metabolomics. Sci Total Environ 650:1239–1249CrossRefGoogle Scholar
  43. Wang P, Zhang B, Zhang H, He Y, Ong CN, Yang J (2019b) Metabolites change of Scenedesmus obliquus exerted by AgNPs. J Environ Sci 76:310–318CrossRefGoogle Scholar
  44. WWAP (United Nations World Water Assessment Programme) (2018) The United Nations World Water Development Report 2018: nature-based solutions for water. UNESCO, ParisGoogle Scholar
  45. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40(W1):W127–W133CrossRefGoogle Scholar
  46. Yong WK, Sim KS, Poong SW, Wei D, Phang SM, Lim PE (2018) Interactive effects of temperature and copper toxicity on photosynthetic efficiency and metabolic plasticity in Scenedesmus quadricauda (Chlorophyceae). J Appl Phycol 30:1–13CrossRefGoogle Scholar
  47. Yusuf M, Fariduddin Q, Hayat S, Ahmad AL (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86(1):1–17CrossRefGoogle Scholar
  48. Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry MP (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manag 181:817–831CrossRefGoogle Scholar
  49. Zhang B, Zhang H, Du C, Xiang Q, Hu C, He Y, Nam C (2017) Metabolic responses of the growing Daphnia similis to chronic AgNPs exposure as revealed by GC-Q-TOF/MS and LC-Q-TOF/MS. Water Res 114:135–143CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Wai-Kuan Yong
    • 1
    • 2
  • Kae-Shin Sim
    • 3
  • Sze-Wan Poong
    • 1
  • Dong Wei
    • 4
  • Siew-Moi Phang
    • 1
    • 3
  • Phaik-Eem Lim
    • 1
    Email author
  1. 1.Institute of Ocean and Earth SciencesUniversity of MalayaKuala LumpurMalaysia
  2. 2.Institute for Advanced StudiesUniversity of MalayaKuala LumpurMalaysia
  3. 3.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  4. 4.School of Food Sciences and EngineeringSouth China University of TechnologyGuangzhouChina

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