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Physiological sensitivity of Haematococcus pluvialis (Chlorophyta) to environmental pollutants: a comparison with Microcystis wesenbergii (cyanobacteria) and Pseudokirchneriella subcapitata (Chlorophyta)

  • Shuiping Peng
  • Min Long
  • Lingling Zheng
  • Lirong Song
  • Jie Li
Article

Abstract

Haematococcus pluvialis is beneficial to human health and is important for commercial use. However, it seldom prevails in permanent freshwater bodies. Increasing environmental pollutants from anthropogenic activity may threaten the wide distribution of H. pluvialis. Here, we quantified and compared the adverse effects of the common pesticides atrazine, pentachlorophenol, malathion, and 3,5-dichlorophenol and the heavy metals Cu(II), Cr(VI), and Cd(II) on H. pluvialis, Microcystis wesenbergii (a freshwater bloom-forming cyanobacterium), and Pseudokirchneriella subcapitata (a standard toxicity test species). We found that H. pluvialis was the species most sensitive to 3,5-dichlorophenol and Cr(VI) exposure and the most tolerant to pentachlorophenol exposure according to IC50, changes in chlorophyll a content, maximum electron transport rates (ETRmax), the quantum efficiency of photosystem II (Fv/Fm), and esterase activity. Haematococcus pluvialis was also the species most sensitive to atrazine according to IC50, chlorophyll a, and ETRmax. Overall, our findings suggest that atrazine, 3,5-dichlorophenol, and Cr(VI) are potential factors limiting the distribution of H. pluvialis. We suggest that H. pluvialis can be a potentially useful bioindicator for evaluating pollutants. Furthermore, ETRmax, FDA assay, and flow cytometry can be combined with Haematococcus to test for toxicity.

Keywords

Fluorescein diacetate Haematococcus pluvialis Heavy metals Microcystis wesenbergii Pesticide Pseudokirchneriella subcapitata 

Notes

Acknowledgements

We thank Chenlin Hu of the University of Houston and Dongbo Ding of the The Hong Kong University of Science and Technology for useful suggestions on paper preparation. We also thank Dr. Michael A. Borowitzka and two anonymous referees for critical suggestions.

Funding information

This work was financially supported by China Agriculture Research System (CARS-50), the National Natural Science Foundation of China (31000179), and Teachers Research Funding of Central South University (2014JSJJ035).

References

  1. Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12:128–152CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aptula AO, Netzeva TI, Valkova IV, Cronin MTD, Schultz TW, Kühne R, Schüürmann G (2002) Multivariate discrimination between modes of toxic action of phenols. Quant Struct Act Rel 21:12–22CrossRefGoogle Scholar
  3. Arroyo-Pérez E, Flores J, González-Salvatierra C, Matías-Palafox ML, Jiménez-Sierra C (2017) High tolerance to high-light conditions for the protected species Ariocarpus kotschoubeyanus (Cactaceae). Conserv Physiol 5(1):cox042Google Scholar
  4. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefPubMedGoogle Scholar
  5. Bártová K, Hilscherová K, Babica P, Maršálek B, Bláha L (2011) Effects of microcystin and complex cyanobacterial samples on the growth and oxidative stress parameters in green alga Pseudokirchneriella subcapitata and comparison with the model oxidative stressor—herbicide paraquat. Environ Toxicol 26:641–648CrossRefPubMedGoogle Scholar
  6. Bi XD, Zhang SL, Dai W, Xing KZ, Yang F (2013) Effects of lead (II) on the extracellular polysaccharide (EPS) production and colony formation of cultured Microcystis aeruginosa. Water Sci Technol 67:803–809CrossRefPubMedGoogle Scholar
  7. Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562CrossRefPubMedGoogle Scholar
  8. Bischoff HW, Bold HC (1963) Some soil algae from Enchanted Rock and related algal species. Phycological Studies, University of Texas 4:1–95Google Scholar
  9. Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117CrossRefGoogle Scholar
  10. Brookes JD, Geary SM, Ganf GG, Burch MD (2000) Use of FDA and flow cytometry to assess metabolic activity as an indicator of nutrient status in phytoplankton. Mar Freshw Res 51:817–823CrossRefGoogle Scholar
  11. Calomeni A, Rodgers JH, Kinley CM (2014) Responses of Planktothrix agardhii and Pseudokirchneriella subcapitata to copper sulfate (CuSO4·5H2O) and a chelated copper compound (Cutrine®-Ultra). Water Air Soil Pollut 225:2231CrossRefGoogle Scholar
  12. Chen CY, Lin JH (2006) Toxicity of chlorophenols to Pseudokirchneriella subcapitata under air-tight test environment. Chemosphere 62:503–509CrossRefPubMedGoogle Scholar
  13. Choi CJ, Berges JA, Young EB (2012) Rapid effects of diverse toxic water pollutants on chlorophyll a fluorescence: variable responses among freshwater microalgae. Water Res 46:2615–2626CrossRefPubMedGoogle Scholar
  14. Cullimoke D (1975) The in vitro sensitivity of some species of Chlorophyceae to a selected range of herbicides. Weed Res 15:401–406CrossRefGoogle Scholar
  15. Cvetkovic AD, Samson G, Couture P, Popovic R (1991) Study of dependency between culture growth and photosynthetic efficiency measured by fluorescence induction in Selenastrum capricornutum inhibited by copper. Ecotox Environ Safe 22:127–132CrossRefGoogle Scholar
  16. de Schamphelaere K, Nys C, Janssen C (2014) Toxicity of lead (Pb) to freshwater green algae: development and validation of a bioavailability model and inter-species sensitivity comparison. Aquat Toxicol 155:348–359CrossRefPubMedGoogle Scholar
  17. Fairchild J, Ruessler D, Haverland P, Carlson A (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32:353–357CrossRefPubMedGoogle Scholar
  18. Fassett RG, Coombes JS (2012) Astaxanthin in cardiovascular health and disease. Molecules 17:2030–2048CrossRefPubMedGoogle Scholar
  19. Figueroa FL, Conde-Álvarez R, Gómez I (2003) Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth Res 75:259–275CrossRefPubMedGoogle Scholar
  20. Genitsaris S, Stefanidou N, Katsiapi M, Vardaka E, Kormas KA, Sommer U, Moustaka-Gouni M (2016) Haematococcus: a successful air-dispersed colonist in ephemeral waters is rarely found in phytoplankton communities. Turk J Bot 40:427–438CrossRefGoogle Scholar
  21. Guo J, Selby K, Boxall A (2016) Comparing the sensitivity of chlorophytes, cyanobacteria, and diatoms to major-use antibiotics. Environ Toxicol Chem 35:2587–2596CrossRefPubMedGoogle Scholar
  22. Hughes EO, Gorham PR, Zehnder A (1958) Toxicity of a unialgal culture of Microcystis aeruginosa. Can J Microbiol 4:225–236CrossRefPubMedGoogle Scholar
  23. Jamers A, de Coen W (2010) Effect assessment of the herbicide paraquat on a green alga using differential gene expression and biochemical biomarkers. Environ Toxicol Chem 29:893–901CrossRefPubMedGoogle Scholar
  24. Jamers A, Lenjou M, Deraedt P, Bockstaele DV, Blust R, Wd C (2009) Flow cytometric analysis of the cadmium-exposed green alga Chlamydomonas reinhardtii (Chlorophyceae). Eur J Phycol 44:541–550CrossRefGoogle Scholar
  25. Johnson EA, An GH (1991) Astaxanthin from microbial sources. Crit Rev Biotechnol 11:297–326CrossRefGoogle Scholar
  26. Kwak HS, Kim JYH, Sim SJ (2015) A microreactor system for cultivation of Haematococcus pluvialis and astaxanthin production. J Nanosci Nanotechnol 15:1618–1623CrossRefPubMedGoogle Scholar
  27. Lancaster CR, Michel H (1999) Refined crystal structures of reaction centres from Rhodopseudomonas viridis in complexes with the herbicide atrazine and two chiral atrazine derivatives also lead to a new model of the bound carotenoid. J Mol Biol 286:883–898CrossRefPubMedGoogle Scholar
  28. Li J, Ou D, Zheng L, Gan N, Song L (2011a) Applicability of the fluorescein diacetate assay for metabolic activity measurement of Microcystis aeruginosa (Chroococcales, cyanobacteria). Phycol Res 59:200–207CrossRefGoogle Scholar
  29. Li J, Zhu D, Niu J, Shen S, Wang G (2011b) An economic assessment of astaxanthin production by large scale cultivation of Haematococcus pluvialis. Biotechnol Adv 29:568–574CrossRefPubMedGoogle Scholar
  30. Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167CrossRefPubMedGoogle Scholar
  31. Lukavský J, Furnadjieva S, Cepák V (2003) Toxicity of metals, Al, Cd, Co, Cr, Cu, Fe, Ni, Pb and Zn on microalgae, using microplate bioassay 1: Chlorella kessleri, Scenedesmus quadricauda, Sc. subspicatus and Raphidocelis subcapitata (Selenastrum capricornutum). Algol Stud 110:127–141CrossRefGoogle Scholar
  32. Machado MD, Soares EV (2015) Use of a fluorescence-based approach to assess short-term responses of the alga Pseudokirchneriella subcapitata to metal stress. J Appl Phycol 27:805–813CrossRefGoogle Scholar
  33. Machado MD, Soares EV (2018) Sensitivity of freshwater and marine green algae to three compounds of emerging concern. J Appl Phycol.  https://doi.org/10.1007/s10811-018-1511-5
  34. Martins RJ, Pardo R, Boaventura RA (2004) Cadmium (II) and zinc (II) adsorption by the aquatic moss Fontinalis antipyretica: effect of temperature, pH and water hardness. Water Res 38:693–699CrossRefPubMedGoogle Scholar
  35. Murphy SD (1967) Malathion inhibition of esterases as a determinant of malathion toxicity. J Pharmacol Exp Ther 156:352–365PubMedGoogle Scholar
  36. Ohkawa H, Imaishi H, Shiota N, Yamada T, Inui H And Ohkawa Y (1998) Molecular mechanisms of herbicide resistance with special emphasis on cytochrome p450 monooxygenases. Plant Biotechnol 15: 173–176CrossRefGoogle Scholar
  37. Pambrun V, Marquot A, Racault Y (2008) Characterization of the toxic effects of cadmium and 3.5-dichlorophenol on nitrifying activity and mortality in biologically activated sludge systems - effect of low temperature. Environ Sci Pollut Res 15:592–599CrossRefGoogle Scholar
  38. Paquet N, Lavoie M, Maloney F, Duval JF, Campbell PG, Fortin C (2015) Cadmium accumulation and toxicity in the unicellular alga Pseudokirchneriella subcapitata: influence of metal-binding exudates and exposure time. Environ Toxicol Chem 34:1524–1532CrossRefPubMedGoogle Scholar
  39. Park JC, Choi SP, Hong M-E, Sim SJ (2014) Enhanced astaxanthin production from microalga, Haematococcus pluvialis by two-stage perfusion culture with stepwise light irradiation. Bioprocess Biosyst Eng 37:2039–2047CrossRefPubMedGoogle Scholar
  40. Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10CrossRefPubMedGoogle Scholar
  41. Pereira M, Resende P, Azeiteiro U, Oliveira J, Figueiredo D (2005) Differences in the effects of metals on growth of two freshwater green algae (Pseudokirchneriella subcapitata (Korshikov) Hindak and Gonium pectorale Müller). Bull Environ Contam Toxicol 75:515–522CrossRefPubMedGoogle Scholar
  42. Proctor VW (1957a) Some controlling factors in the distribution of Haematococcus pluvialis. Ecology 38:457–462CrossRefGoogle Scholar
  43. Proctor VW (1957b) Studies of algal antibiosis using Haematococcus and Chlamydomonas. Limnol Oceanogr 2:125–139CrossRefGoogle Scholar
  44. Rhoades MG, Meza JL, Beseler CL, Shea PJ, Kahle A, Vose JM, Eskridge KM, Spalding RF (2013) Atrazine and nitrate in public drinking water supplies and non-Hodgkin lymphoma in Nebraska, USA. Environ Health Insights 7: 15–27Google Scholar
  45. Rioboo C, González-Barreiro Ó, Abalde J, Cid Á (2011) Flow cytometric analysis of the encystment process induced by paraquat exposure in Haematococcus pluvialis (Chlorophyceae). Eur J Phycol 46:89–97CrossRefGoogle Scholar
  46. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  47. Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41CrossRefPubMedGoogle Scholar
  48. Rodgher S, Espindola ELG, Simoes FCF, Tonietto AE (2012) Cadmium and chromium toxicity to Pseudokirchneriella subcapitata and Microcystis aeruginosa. Braz Arch Biol Technol 55:161–169CrossRefGoogle Scholar
  49. Rzymski P, Poniedzialek B, Niedzielski P, Tabaczewski P, Wiktorowicz K (2014) Cadmium and lead toxicity and bioaccumulation in Microcystis aeruginosa. Front Env Sci Eng 8:427–432CrossRefGoogle Scholar
  50. Saha R, Nandi R, Saha B (2011) Sources and toxicity of hexavalent chromium. J Coord Chem 64:1782–1806CrossRefGoogle Scholar
  51. Sanchez BC, Ochoa-AcuÑa H, Porterfield DM, Sepúlveda MS (2008) Oxygen flux as an indicator of physiological stress in fathead minnow (Pimephales promelas) embryos: a real-time biomonitoring system of water quality. Environ Sci Technol 42:7010–7017CrossRefPubMedGoogle Scholar
  52. Tukaj Z, Baścik-Remisiewicz A, Skowroński T, Tukaj C (2007) Cadmium effect on the growth, photosynthesis, ultrastructure and phytochelatin content of green microalga Scenedesmus armatus: a study at low and elevated CO2 concentration. Environ Exp Bot 60:291–299CrossRefGoogle Scholar
  53. US EPA (2003) Ambient aquatic life water quality criteria for atrazine. U.S. EPA Office of Water: Washington, DCGoogle Scholar
  54. Wang C, Feng B, Tian C, Tian Y, Chen D, Wu X, Li G, Xiao B (2018) Quantitative study on the survivability of Microcystis colonies in lake sediments. J Appl Phycol 30:495–506CrossRefGoogle Scholar
  55. Wang SB, Hu Q, Sommerfeld M, Chen F (2004) Cell wall proteomics of the green alga Haematococcus pluvialis (Chlorophyceae). Proteomics 4:692–708CrossRefPubMedGoogle Scholar
  56. Weiner JA, DeLorenzo ME, Fulton MH (2004) Relationship between uptake capacity and differential toxicity of the herbicide atrazine in selected microalgal species. Aquat Toxicol 68:121–128CrossRefPubMedGoogle Scholar
  57. Yeh HJ, Chen CY (2006) Toxicity assessment of pesticides to Pseudokirchneriella subcapitata under air-tight test environment. J Hazard Mater 131:6–12CrossRefPubMedGoogle Scholar
  58. Zeng J, Yang LY, Wang WX (2010) High sensitivity of cyanobacterium Microcystis aeruginosa to copper and the prediction of copper toxicity. Environ Toxicol Chem 29:2260–2268CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.School of Life SciencesCentral South UniversityChangshaChina
  2. 2.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina

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