Skip to main content
Log in

Shifts in photosynthetic parameters and lipid production of the freshwater microalga Selenastrum gracile (Chlorophyceae) under cadmium exposure

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The amount of metals released into the environment can increase with anthropogenic activities and different trophic levels can be affected. In the present study, we evaluated the changes in growth, chlorophyll content, photosynthetic parameters, and lipid and fatty acid (FA) contents of the freshwater microalga Selenastrum gracile (Chlorophyceae) exposed to sublethal concentrations of cadmium for 72 h. Our results show that Cd negatively affected algal growth and chlorophyll a increased per cell under Cd exposure. Photosynthetic parameters (maximum and operational yield, as well as quenching) were affected under Cd exposure, indicating damage to the photosynthetic apparatus. The amount of lipids and fatty acids increased with the increase of Cd in the medium. The most affected lipid classes under metal exposure were aliphatic hydrocarbon (HC), acetone mobile polar lipid (AMPL), and phospholipid (PL). Based on our results, we suggest that the production of algal lipids and fatty acids changed as a response to the amount of metal in the medium, avoiding photosynthetic damage at the lowest Cd concentration with the increase of polyunsaturated fatty acids (PUFA). However, at higher concentrations, the maintenance of the high values of PUFA was not observed and there was a decrease in the unsaturation of FA, resulting in higher amounts of MUFA. In addition, the percentage of structural lipids (sterol—ST—and PL) also decreased at the highest concentration. This, in combination with the decreased unsaturation of FA, suggests changes in membrane conformation and, consequently, damage to the photosynthetic machinery in the presence of Cd.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Datasets are available upon request. Please contact Giseli S. Rocha (swertsbio@gmail.com).

References

  • AFNOR (1980) Association Française de Normalisation. Essais de eaux. Norme experimental T90-304. Determination de l’inhibition de croissance de Scenedesmus subspicatus par une substance. AFNOR, Paris, p 6

    Google Scholar 

  • Alho LOG, Gebara RC, Paina KA, Sarmento H, Melão MGG (2019) Responses of Raphidocelis subcapitata exposed to Cd and Pb: mechanisms of toxicity assessed by multiple endpoints. Ecotoxicol Environ Saf 169:950–959

    CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Los DA, Murata N (2010) Regulatory roles in photosynthesis of unsaturated fatty acids in membrane lipids. In: Wada H, Murata N (eds) Lipids in photosynthesis - essential and regulatory functions. Springer, Dordrecht, pp 373–388

    Google Scholar 

  • Anderson JM, Park YI, Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol Plant 100:214–223

    CAS  Google Scholar 

  • Andresen E, Kappel S, Stärk HJ, Riegger U, Borovec J, Mattusch J, Heinz A, Schmelzer CEH, Matoušková Š, Dickinson B, Küpper H (2016) Cadmium toxicity investigated at the physiological and biophysical levels under environmentally relevant conditions using the aquatic model plant Ceratophyllum demersum. New Phytol 210:1244–1258

    CAS  PubMed  Google Scholar 

  • Benvenuti G, Bosma R, Cuaresma M, Janssen M, Barbosa MJ, Wijffels RH (2015) Selecting microalgae with high lipid productivity and photosynthetic activity under nitrogen starvation. J Appl Phycol 27:1425–1431

    CAS  Google Scholar 

  • Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology. I. Encyclopedia of plant physiology. Springer, Berlin, pp 57–107

    Google Scholar 

  • Bossuyt BTA, Janssen C (2005) Copper regulation and homeostasis of Daphnia magna and Pseudokirchneriella subcapitata: influence of acclimation. Environ Pollut 136:135–144

    CAS  PubMed  Google Scholar 

  • Boudière L, Michaud M, Petroutsos D, Rébeillé F, Dalconet D, Bastien O, Roy S, Finazzi G, Rolland N, Jouhet J, Block MA, Maréchal E (2014) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta 1837:470–480

    PubMed  Google Scholar 

  • Budge SM, Parrish CC (1998) Lipid biogeochemistry of plankton, settling matter and sediments in Trinity Bay, Newfoundland. II. Fatty acids. Org Geochem 29:1547–1559

    CAS  Google Scholar 

  • Carvalho CCR, Caramujo MJ (2018) The various roles of fatty acids. Molecules 23:2583

    PubMed Central  Google Scholar 

  • Çelekli A, Gültekin E, Bozkurt H (2016) Morphological and biochemical responses of Spirogyra setiformis exposed to cadmium. Clean Soil Air Water 44:256–262

    Google Scholar 

  • Chia MA, Lombardi AT, Melão MGG, Parrish CC (2013) Effects of cadmium and nitrogen on lipid composition of Chlorella vulgaris (Trebouxiophyceae, Chlorophyta). Eur J Phycol 48:1–11

    CAS  Google Scholar 

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 1–17

    Google Scholar 

  • Dao LHT, Beardall J (2016) Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Res 16:150–159

    Google Scholar 

  • Dixit S, Singh DP (2015) Differential response of photosynthetic apparatus of cyanobacterium Nostoc muscorum to Pb and Cd toxicity. Photosynthetica 53:223–230

    CAS  Google Scholar 

  • Echeveste P, Silva JC, Lombardi AT (2017) Cu and Cd affect distinctly the physiology of a cosmopolitan tropical freshwater phytoplankton. Ecotoxicol Environ Saf 143:228–235

    CAS  PubMed  Google Scholar 

  • Fernandez-Piñas F, Mateo P, Bonilla I (1995) Cadmium toxicity in Nostoc UAM208: protection by calcium. New Phytol 131:403–407

    Google Scholar 

  • Herlory O, Bonzom JM, Gilbin R (2013) Sensitivity evaluation of the green alga Chlamydomonas reinhardtii to uranium by pulse amplitude modulated (PAM) fluorometry. Aquat Toxicol 140-141:288–294

    CAS  PubMed  Google Scholar 

  • Ivorra N, Hettelaar J, Tubbing G, Kraak MHS, Sabater S, Admiraal W (1999) Translocation of microbenthic algal assemblages used for in situ analysis of metal pollution in rivers. Arch Environ Contam Toxicol 37:19–28

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    CAS  Google Scholar 

  • Juneau P, El Berdey A, Popovic R (2002) PAM fluorometry in the determination of the sensitivity of Chlorella vulgaris, Selenastrum capricornutum and Chlamydomonas reinhardtii to copper. Arch Environ Contam Toxicol 42:155–164

    CAS  PubMed  Google Scholar 

  • Kainz MJ, Fisk AT (2009) Integrating lipids and contaminants in aquatic ecology and ecotoxicology. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Berlin, pp 93–114

    Google Scholar 

  • Kalaji HM, Schansker G, Ladler RJ et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kanervo E, Tasaka Y, Murata N, Aro EM (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures. Plant Physiol 114:841–849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Tiam S, Lavoie I, Doose C, Hamilton PB, Fortin C (2018) Morphological, physiological and molecular responses of Nitzschia palea under cadmium stress. Ecotoxicology 27:675–688

    PubMed  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application Notes 1:27–35

    Google Scholar 

  • Krause GH, Jahns P (2003) Pulse amplitude modulated chlorophyll fluorometry and its application in plant science. In: Green BR, Parson WW (eds) Light harvesting antennas in photosynthesis. Kluwer, Dordrecht, pp 373–399

    Google Scholar 

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

    Google Scholar 

  • Küpper H, Šetlík I, Spiller M, Küpper FC, Prášil O (2002) Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol 38:429–441

    Google Scholar 

  • Landrum PF, Fisher SW (1999) Influence of lipids on the bioaccumulation and trophic transfer of organic contaminants in aquatic organisms. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 203–234

    Google Scholar 

  • Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 435:42

    CAS  PubMed  Google Scholar 

  • Lee JG, Roberts SB, Morel FMM (1995) Cadmium: a nutrient for the marine diatom Thalassiosira weissflogii. Limnol Oceanogr 40:1056–1063

    CAS  Google Scholar 

  • Lombardi AT, Maldonado MT (2011) The effects of copper on the photosynthetic response of Phaeocystis cordata. Photosynth Res 108:77–87

    CAS  PubMed  Google Scholar 

  • Lombardi AT, Vieira AAH (1999) Lead- and copper-complexing extracellular ligands released by Kirchneriella aperta (Chloroccocales, Chlorophyta). Phycologia 38:283–288

    Google Scholar 

  • Lombardi AT, Vieira AAH, Sartori LA (2002) Mucilagenous capsule adsorption and intracellular uptake of copper by Kirchneriella aperta (Chlorococcales). J Phycol 38:332–337

    CAS  Google Scholar 

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

    Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69

    CAS  PubMed  Google Scholar 

  • Marchello AE, Oliveira NL, Lombardi AT, Polpo A (2018) An investigation onto Cd toxicity to freshwater microalga Chlorella sorokiniana in mixotrophy and photoautotrophy: a Bayesian approach. Chemosphere 211:794–803

    CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson G (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Google Scholar 

  • Morrison WR, Smith LM (1964) Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J Lipid Res 5:600–608

    CAS  PubMed  Google Scholar 

  • Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5:802–814

    CAS  PubMed  Google Scholar 

  • Nicklish A, Köhler J (2001) Estimation of primary production with Phyto-PAM fluorometry. Ann Report Inst Freshw Ecol Inland Fish Berlin 13:47–60

    Google Scholar 

  • Parrish CC (1999) Determination of total lipid, lipid classes and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 4–20

    Google Scholar 

  • Pavlaki MD, Morgado RG, Soares AMVM, Calado R, Loureiro S (2018) Toxicokinetics of cadmium in Palaemon varians postlarvae under waterborne and/or dietary exposure. Environ Toxicol Chem 37:1614–1622

    CAS  PubMed  Google Scholar 

  • Peers G, Price NM (2006) Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature 441:341–344

    CAS  PubMed  Google Scholar 

  • Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10

    CAS  PubMed  Google Scholar 

  • Perez P, Estevez-Blanco P, Beiras R, Fernandez E (2006) Effect of copper on the photochemical efficiency, growth, and chlorophyll a biomass of natural phytoplankton assemblages. Environ Toxicol Chem 25:137–143

    CAS  PubMed  Google Scholar 

  • Pinto E, Sigaud-Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal induced oxidative stress in algae. J Phycol 39:1008–1018

    CAS  Google Scholar 

  • Price NM, Morel FMM (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344:658–660

    CAS  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237

    CAS  Google Scholar 

  • Ritter A, Dittami SM, Goulitquer S, Correa JA, Boyen C, Potin P, Tonon T (2014) Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae. BMC Plant Biol 14:116

    PubMed  PubMed Central  Google Scholar 

  • Rocha GS, Pinto FHV, Melão MGG, Lombardi AT (2015) Growing Scenedesmus quadricauda in used cultured media: is it viable? J Appl Phycol 27:171–178

    Google Scholar 

  • Rocha GS, Tonietto AE, Lombardi AT, Melão MGG (2016a) Effect of copper contaminated food on the life cycle and secondary production of Daphnia laevis. Ecotoxicol Environ Saf 133:235–242

    CAS  PubMed  Google Scholar 

  • Rocha GS, Parrish CC, Lombardi AT, Melão MGG (2016b) Copper affects biochemical and physiological responses of Selenastrum gracile (Reinsch). Ecotoxicology 25:1468–1477

    CAS  PubMed  Google Scholar 

  • Rocha GS, Parrish CC, Lombardi AT, Melão MGG (2018) Biochemical and physiological responses of Selenastrum gracile (Chlorophyceae) acclimated to different phosphorus concentrations. J Appl Phycol 30:2167–2177

    CAS  Google Scholar 

  • Ruangsomboon SS, Wongrat L (2006) Bioaccumulation of cadmium in an experimental aquatic food chain involving phytoplankton (Chlorella vulgaris), zooplankton (Moina macrocopa), and the predatory catfish Clarias macrocephalus x C. gariepinus. Aquat Toxicol 78:15–20

    CAS  PubMed  Google Scholar 

  • Sakshaug E (1993) Variability in photosynthetic parameters. Proc. SPIE 2048, Underwater Light Measurements. doi: https://doi.org/10.1117/12.165490

  • Santos D, Duarte B, Caçador I (2015) Biochemical and photochemical feedbacks of acute Cd toxicity in Juneus acutus seedlings: the role of non-functional Cd-chlorophylls. Estuar Coast Shelf Sci 167:228–239

    CAS  Google Scholar 

  • Schmid-Siegert E, Stepushenko O, Glauser G, Farmer EE (2016) Membranes as structural antioxidants: recycling of malondialdehyde to its source in oxidation-sensitive chloroplast fatty acids. J Biol Chem 291:13005–13013

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shanab S, Essa A, Shalaby E (2012) Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal Behav 7:392–399

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553

    CAS  Google Scholar 

  • Shoaf TW, Lium B (1976) Improved extraction of chlorophyll a and b from algae using dimethylsulfoxide. Limnol Oceanogr 21:926–928

    CAS  Google Scholar 

  • Smolders A, Lock R, Van der Velde G et al (2003) Effects of mining activities on heavy metal concentrations in water, sediment, and macroinvertebrates in different reaches of the Pilcomayo River, South America. Arch Environ Contam Toxicol 44:314–323

    CAS  PubMed  Google Scholar 

  • Song L, Qin JG, Su S, Xu J, Clarke S, Shan Y (2012) Micronutrient requirements for growth and hydrocarbon production in the oil producing green alga Botryococcus braunii (Chlorophyta). PLoS One 7:e41459

    CAS  PubMed  PubMed Central  Google Scholar 

  • Souza JP, Melo DC, Lombardi AT, Melão MGG (2014) Effects of diet borne cadmium on life history and secondary production of a tropical freshwater cladoceran. Ecotoxicology 23:1764–1773

    CAS  PubMed  Google Scholar 

  • Suslichenko IS, Thikonov AN (2019) Photo-reducible plastoquinone pools in chloroplasts of Tradescentia plants acclimated to high and low light. FEBS Letters 593:788–798

    CAS  PubMed  Google Scholar 

  • Van Eerden SJ, Jong DH, Vries AH, Wassenaar TA, Marrink SJ (2015) Characterization of lipid thylakoid membranes from cyanobacteria and higher plants by molecular dynamic simulations. Biochim Biophys Acta 1848:1319–1330

    PubMed  Google Scholar 

  • Vinyard DJ, Badshah SL, Riggio MR, Kaur D, Fanguy AR, Gunner MR (2019) Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions. Proc Nat Acad Sci 116:18917–18922

    CAS  PubMed  Google Scholar 

  • Wacker A, Piepho M, Spijkerman E (2015) Photosynthetic and fatty acid acclimation of four phytoplankton species in response to light intensity and phosphorus availability. Eur J Phycol 50:288–300

    CAS  Google Scholar 

  • Wang WX, Dei RCH (2006) Metal stoichiometry in predicting Cd and Cu toxicity to a freshwater green alga Chlamydomonas reinhardtii. Environ Pollut 142:303–312

    CAS  PubMed  Google Scholar 

  • White DA, Rooks PA, Kimmance S, Tait K, Jones M, Tarran GA, Cook C, Llewellyn CA (2019) Modulation of polar lipid profiles in Chlorella sp in response to nutrient limitation. Metabolites 9:E39

    PubMed  Google Scholar 

  • Yadav S, Prajapati R, Atri N (2016) UV-B-heavy metal interaction: comparative evaluation on photosynthetic properties of three cyanobacteria. Curr Microbiol 73:739–746

    CAS  PubMed  Google Scholar 

  • Zhou W, Juneau P, Qiu B (2006) Growth and photosynthetic responses of the bloom forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere 65:1738–1746

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Ana Teresa Lombardi and Maria da Graça Gama Melão for providing the laboratory facilities to develop this study.

Funding

This study was funded by São Paulo Research Foundation (FAPESP, Grant #2015/25436-1 – first author) and Natural Sciences and Engineering Research Council of Canada (NSERC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giseli Swerts Rocha.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rocha, G.S., Parrish, C.C. & Espíndola, E.L.G. Shifts in photosynthetic parameters and lipid production of the freshwater microalga Selenastrum gracile (Chlorophyceae) under cadmium exposure. J Appl Phycol 32, 4047–4055 (2020). https://doi.org/10.1007/s10811-020-02255-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02255-5

Keywords

Navigation