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.
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References
Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12:128–152
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 21:12–22
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):cox042
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
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 26:641–648
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 67:803–809
Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562
Bischoff HW, Bold HC (1963) Some soil algae from Enchanted Rock and related algal species. Phycological Studies, University of Texas 4:1–95
Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117
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 51:817–823
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 225:2231
Chen CY, Lin JH (2006) Toxicity of chlorophenols to Pseudokirchneriella subcapitata under air-tight test environment. Chemosphere 62:503–509
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 46:2615–2626
Cullimoke D (1975) The in vitro sensitivity of some species of Chlorophyceae to a selected range of herbicides. Weed Res 15:401–406
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 22:127–132
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 155:348–359
Fairchild J, Ruessler D, Haverland P, Carlson A (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32:353–357
Fassett RG, Coombes JS (2012) Astaxanthin in cardiovascular health and disease. Molecules 17:2030–2048
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 75:259–275
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 40:427–438
Guo J, Selby K, Boxall A (2016) Comparing the sensitivity of chlorophytes, cyanobacteria, and diatoms to major-use antibiotics. Environ Toxicol Chem 35:2587–2596
Hughes EO, Gorham PR, Zehnder A (1958) Toxicity of a unialgal culture of Microcystis aeruginosa. Can J Microbiol 4:225–236
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 29:893–901
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 44:541–550
Johnson EA, An GH (1991) Astaxanthin from microbial sources. Crit Rev Biotechnol 11:297–326
Kwak HS, Kim JYH, Sim SJ (2015) A microreactor system for cultivation of Haematococcus pluvialis and astaxanthin production. J Nanosci Nanotechnol 15:1618–1623
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 286:883–898
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 59:200–207
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 29:568–574
Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167
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 110:127–141
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 27:805–813
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
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 38:693–699
Murphy SD (1967) Malathion inhibition of esterases as a determinant of malathion toxicity. J Pharmacol Exp Ther 156:352–365
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: 173–176
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 15:592–599
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 34:1524–1532
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 37:2039–2047
Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10
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 75:515–522
Proctor VW (1957a) Some controlling factors in the distribution of Haematococcus pluvialis. Ecology 38:457–462
Proctor VW (1957b) Studies of algal antibiosis using Haematococcus and Chlamydomonas. Limnol Oceanogr 2:125–139
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: 15–27
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 46:89–97
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 111:1–61
Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41
Rodgher S, Espindola ELG, Simoes FCF, Tonietto AE (2012) Cadmium and chromium toxicity to Pseudokirchneriella subcapitata and Microcystis aeruginosa. Braz Arch Biol Technol 55:161–169
Rzymski P, Poniedzialek B, Niedzielski P, Tabaczewski P, Wiktorowicz K (2014) Cadmium and lead toxicity and bioaccumulation in Microcystis aeruginosa. Front Env Sci Eng 8:427–432
Saha R, Nandi R, Saha B (2011) Sources and toxicity of hexavalent chromium. J Coord Chem 64:1782–1806
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 42:7010–7017
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 60:291–299
US EPA (2003) Ambient aquatic life water quality criteria for atrazine. U.S. EPA Office of Water: Washington, DC
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 30:495–506
Wang SB, Hu Q, Sommerfeld M, Chen F (2004) Cell wall proteomics of the green alga Haematococcus pluvialis (Chlorophyceae). Proteomics 4:692–708
Weiner JA, DeLorenzo ME, Fulton MH (2004) Relationship between uptake capacity and differential toxicity of the herbicide atrazine in selected microalgal species. Aquat Toxicol 68:121–128
Yeh HJ, Chen CY (2006) Toxicity assessment of pesticides to Pseudokirchneriella subcapitata under air-tight test environment. J Hazard Mater 131:6–12
Zeng J, Yang LY, Wang WX (2010) High sensitivity of cyanobacterium Microcystis aeruginosa to copper and the prediction of copper toxicity. Environ Toxicol Chem 29:2260–2268
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
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).
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Peng, S., Long, M., Zheng, L. et al. Physiological sensitivity of Haematococcus pluvialis (Chlorophyta) to environmental pollutants: a comparison with Microcystis wesenbergii (cyanobacteria) and Pseudokirchneriella subcapitata (Chlorophyta). J Appl Phycol 31, 365–374 (2019). https://doi.org/10.1007/s10811-018-1557-4
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DOI: https://doi.org/10.1007/s10811-018-1557-4