Toxicity response of Chlorella microalgae to glyphosate herbicide exposure based on biomass, pigment contents and photosynthetic efficiency
DOI:
https://doi.org/10.14719/pst.2021.8.2.1068Keywords:
Phytoplankton, Green algae, photosynthesis, Environment, Aquatic pollutionAbstract
The extensive use of glyphosate (N-(phosphonomethyl) glycine) herbicide in agriculture is accompanied by the risk of environmental contamination of aquatic ecosystems. In this study, the effects of glyphosate at different concentrations (50–500 µg ml-1) on three Chlorella species including Chlorella ellipsoidea, Chlorella sorokiniana and Chlorella vulgaris especially in relation to the biomass, pigment contents and photosynthetic efficiency were assessed. After treatment for 24 hr, the acute toxicity results showed that C. vulgaris (IC50 = 449.34 ± 6.20 µg ml-1) was more tolerant to glyphosate than C. ellipsoidea (IC50 = 288.23 ± 23.53 µg ml-1) and C. sorokiniana (IC50 = 174.28 ± 0.50 µg ml-1). After a 72-hr chronic toxicity treatment with glyphosate, glyphosate concentrations decreased to 400–500 µg ml-1 in C. ellipsoidea, 200–300 µg ml-1 in C. sorokiniana and 200–500 µg ml-1 in C. vulgaris respectively. During 24-hr acute toxicity exposure to glyphosate, the pigment contents and maximum quantum efficiency of photosystem II (Fv/Fm) decreased as the concentration of glyphosate increased. Overall, the biomass, pigment contents and photosynthetic efficiency presented a high positive correlation. It is worthwhile to mention that our study provides detailed information on the toxicity and sensitivity of these Chlorella species to glyphosate.
Downloads
References
Nwani CD, Nagpure NS, Kumar R, Kushwaha B, Kumar P, Lakra WS. Mutagenic and genotoxic assessment of atrazine-based herbicide to freshwater fish Channa puntatus (Bloch) using micronucleus test and single cell gel electrophoresis. Environ Toxicol Pharmacol. 2011;31:314-22. https://doi.org/10.1016/j.etap.2010.12.001
Rimet F, Cauchie HM, Hoffmann L, Ector L. Response of diatom indices to simulated water quality improvements in a river. J Appl Phycol. 2005;17:119–28. https://doi.org/10.1007/s10811-005-4801-7
Ghosh M, Gaur JP. Current velocity and the establishment of stream algal periphyton communities. Aquat Bot. 1998;60:1–10. https://doi.org/10.1016/S0304-3770(97)00073-9
Stoemer EF, Smol JP. The diatoms: applications for the environmental and earth sciences. Nordic J Bot. 1999;19:384. https://doi.org/10.1002/jqs.632
Debenest T, Silvestre J, Coste M, Delmas F, Pinelli E. Herbicide effects on freshwater benthic diatoms: induction of nucleus alterations and silica cell wall abnormalities. Aquat Toxicol. 2008;88:88–94. https://doi.org/10.1016/j.aquatox.2008.03.011
Halstead NT, Mcmahon TA, Johnson SA, Raffel TR, Romansic JM, Crumrine PW, Rohr JR. Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecol Lett. 2014;17:932–41. https://doi.org/10.1111/ele.12295
Posthuma L, Suter GW, Traas TP. Environmental and ecological risk assessment: species sensitivity distributions in ecotoxicology. United States of America: Lewis publishers; 2002.
Oukarroum A, Bras B, Perreault F, Popovic R. Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf. 2012;78: 80–85. http://doi.org/10.1016/j.ecoenv.2011.11.012.
Durrieu C, Badreddine I, Daix C. A dialysis system with phytoplankton for monitoring chemical pollution in freshwater ecosystems by alkaline phosphatase assay. J Appl Phycol. 2003;15:289–95. https://doi.org/10.1023/A:1025165727616
Luna LM, Carmenate Z. Microalgas como biomonitores de contaminación. Revista Cubana de Química 2004;16:34–48.
Omar WMW. Perspectives on the use of algae as biological indicators for monitoring and protecting aquatic environments, with special reference to Malaysian freshwater. Ecosystems Trop Life Sci Res. 2010;21(2):51–67.
Safi C, Zebib B, Merah O, Pontalier PY, Vaca-Garcia C. Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renewable Sustainable Energy Rev. 2014;35:265–78. https://doi.org/10.1016/j.rser.2014.04.007
Shaaban M. Green microalgae water extracts as foliar feeding to wheat plants. Pak J Biol Sci. 2001;4:628–32. https://doi.org/10.3923/pjbs.2001.628.632
Faheed F, Abd el Fattah Z. Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of lettuce plant. J Agric Soc Sci. 2008;4:165–69.
Chacón-Lee TL, González-Mariño GE. Microalgae for “Healthy” foods – possibilities and challenges. Compr Rev Food Sci Saf. 2010;9:655–75. https://doi.org/10.1111/j.1541-4337.2010.00132.x
Fernandes B, Dragone G, Abreu A, Geada P, Teixeira J, Vicente A. Starch determination in Chlorella vulgaris – a comparison between acid and enzymatic methods. J Appl Phycol. 2012;24:1203–08. https://doi.org/10.1007/s10811-011-9761-5
Gouveia L, Veloso V, Reis A, Fernandes H, Novais J, Empis J. Chlorella vulgaris used to colour egg yolk. J Sci Food Agric. 1996;70:167–72. https://doi.org/10.1002/(SICI)1097-0010(199602)70:2<167::AID-JSFA472>3.0.CO;2-2
Wang K, Brown RC, Homsy S, Martinez L, Sidhu SS. Fast pyrolysis of microalgae remnants in a fluidized bed reactor for bio-oil and biochar production. Bioresour Technol. 2013;127:494–99. https://doi.org/10.1016/j.biortech.2012.08.016
Francisco ÉC, Neves DB, Jacob-Lopes E, Franco TT. Microalgae as feedstock for biodiesel production: carbon dioxide sequestration, lipid production and biofuel quality. J Chem Technol Biotechnol. 2010;85:395–403. https://doi.org/10.1002/jctb.2338
Reno U, Regaldo L, Vidal E, Mariani M, Zalazar C, Gagneten AM. Water polluted with glyphosate formulations: effectiveness of a decontamination process using Chlorella vulgaris growing as bioindicator. J Appl Phycol. 2016;28:2279–86. https://doi.org/10.1007/s10811-015-0755-6
Ma J, Lin F, Zhang R, Yu W, Lu N. Differential sensitivity of two green algae, Scenedesmus quadricauda and Chlorella vulgaris, to 14 pesticide adjuvants. Ecotoxicol Environ Saf. 2004;58:61-67. https://doi.org/10.1016/j.ecoenv.2003.08.023
Grobbelaar JU. Quality Control and Assurance: crucial for the sustainability of the applied phycology industry. J Appl Phycol. 2003;15:209–15. https://doi.org/10.1023/A:1023820711706
Gulati OP, Ottaway PB. Legislation relating to nutraceuticals in the European Union with a particular focus on botanical-sourced products. Toxicology 2006;221:75–87. https://doi.org/10.1016/j.tox.2006.01.014
Rodriguez-Garcia I, Guil-Guerrero JL. Evaluation of the antioxidant activity of three microalgal species for use as dietary supplements and in the preservation of foods. Food Chem. 2008;108:1023–26. https://doi.org/10.1016/j.foodchem.2007.11.059
Becker EW. Micro-algae as a source of protein. Biotechnol Adv. 2007; 25:207?10. https://doi.org/10.1016/j.biotechadv.2006.11.002
Keffer JE, Kleinheinz GT. Use of Chlorella vulgaris for CO2 mitigation in a photobioreactor. J Ind Microbiol Biotechnol. 2002;29:275–80. https://doi.org/10.1038/sj.jim.7000313
de-Bashan LE, Moreno M, Hernandez JP, Bashan Y. Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth promoting bacterium Azospirillum brasilense. Water Res. 2002;36:2941–48. https://doi.org/10.1016/S0043-1354(01)00522-X
González LE, Cañizares RO, Baena S. Efficiency of ammonia and phosphorusremoval from a Colombian agroindustrial wastewater by the microalgae Chlorella vulgaris and Scenedesmus dimorphus. Bioresour Technol. 1997;60:259–62. https://doi.org/10.1016/S0960-8524(97)00029-1
Vries T, Duling V, Anders A. Detection of herbicides in water and their interactions with Chlorella kessleri. Environmental Sensing and Applications 1999;3821. https://doi.org/10.1117/12.364194
Mensah PK, Palmer CG, Muller WJ. Derivation of South African water quality guidelines for roundup using species sensitivity distribution. Ecotoxicol Environ Saf. 2013;96:24–31. https://doi.org/10.1016/j.ecoenv.2013.06.009
Ma J. Differential sensitivity to 30 herbicides among populations of two green algae Scenedesmus obliquus and Chlorella pyrenoidosa. Bull Environ Contam Toxicol. 2002;68:275–81. https://doi.org/10.1007/s001280249
Kataoka H, Ryu S, Sakiyama N, Makita M. Simple and rapid determination of the herbicides glyphosate and glufosinate in river water, soil and carrot samples by gas chromatography with flame photometric detection. J Chromatogr A. 1996;726:253–58. https://doi.org/10.1016/0021-9673(95)01071-8
Forlani G, Mangiagalli A, Nielsen E, Suardi CM. Degradation of the phosphonate herbicide glyphosate in soil: Evidence for a possible involvement of unculturable microorganisms. Soil Biol Biochem. 1999;31:991-97. https://doi.org/10.1016/S0038-0717(99)00010-3
Gravena R, Filho RV, Alves PL, Mazzafera P, Gravena AR. Glyphosate has low toxicity to citrus plants growing in the field. Can J Plant Sci. 2012;92:119–27. https://doi.org/10.4141/cjps2011-055
Maršálek B, Rojí?kovâ R. Stress factors enhancing production of algal exudates: A potential self-protective mechanism?. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 1996;51(9-10):646-50. https://doi.org/10.1515/znc-1996-9-1008
Romero DM, Ríos de Molina MC, Juárez ÁB. Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri Ecotoxicol Environ Saf. 2011;74(4):741-47. https://doi.org/10.1016/j.ecoenv.2010.10.034
Hernando F, Royuela M, Muñoz-Rueda A, Gonzalez-Murua C. Effect of glyphosate on the greening process and photosynthetic metabolism in Chlorella pyrenoidosa. J Plant Physiol. 1989;134(1):26?31. https://doi.org/10.1016/S0176-1617(89)80197-X
Anton FA, Ariz M, Alia M. Ecotoxic effects of four herbicides (glyphosate, alachlor, chlortoluron and isoproturon) on the algae Chlorella pyrenoidosa Chick. Sci Total Environ. 1993;134 (Suppl.2):845?51. https://doi.org/10.1016/S0048-9697(05)80090-7
Shao Y, Jiang L, Pan J, He Y. Identification of glyphosate and butachlor by detecting Chlorella pyrenoidosa with raman microspectroscopy. Gaodeng Xuexiao Huaxue Xuebao/Chemical Journal of Chinese Universities 2015;36(6):1082-86. https://doi.org/10.7503/cjcu20140938
Shao Y, Li Y, Jiang L, Pan J, He Y, Dou X. Identification of pesticide varieties by detecting characteristics of Chlorella pyrenoidosa using visible/near infrared hyperspectral imaging and raman microspectroscopy technology. Water Res. 2016b;104:432-40. https://doi.org/10.1016/j.watres.2016.08.042
Shao Y, Jiang L, Zhou H, Pan J, He Y. Identification of pesticide varieties by testing microalgae using visible/Near infrared hyperspectral imaging technology. Sci Rep. 2016a;6:2422. https://doi.org/10.1038/srep24221
Vendrell E, Ferraz DGB, Sabater C, Carrasco JM. Effect of glyphosate on growth of four freshwater species of phytoplankton: A microplate bioassay. Bull Environ Contam Toxicol. 2009;82(5):538?42. https://doi.org/10.1007/s00128-009-9674-z
Jaiswal KK, Kumar V, Vlaskin MS, Nanda M. Impact of glyphosate herbicide stress on metabolic growth and lipid inducement in Chlorella sorokiniana UUIND6 for biodiesel production. Algal Res. 2020;51: 102071. https://doi.org/10.1016/j.algal.2020.102071
Sáenz ME, Marzio WD. Ecotoxicity of herbicide Glyphosate to four chlorophyceaen freshwater algae. Limnetica. 2009;28(1):149?58. https://doi.org/10.1007/s00128-009-9674-z
Lipok J, Studnik H, Gruyaert S. The toxicity of Roundup® 360 SL formulation and its main constituents: glyphosate and isopropylamine towards non-target water photoautotrophs. Ecotoxicol Environ Saf. 2010;73(7):1681-88. https://doi.org/10.1016/j.ecoenv.2010.08.017
Reno U, Gutierrez MF, Regaldo L, Gagneten AM. The impact of Eskoba®, a glyphosate formulation, on the freshwater plankton community. Water Environ Res. 2014;86(12):2294-300. https://doi.org/10.2175/106143014x13896437493580
Shaker BK, Alsalman IMA, Al-Attabi MS. Effect of exposure to glyphosate pesticide, cadimum and chromium on biomass of algae (Chlorococcum humicola and Chlorella vulgaris) in polluted aqueous culture. Indian J Public Health Res Dev. 2018;9(10):708?13. https://doi.org/10.5958/0976-5506.2018.01219.6
Hernández-García CI, Martínez-Jeronimo F. Multistressor negative effects on an experimental phytoplankton community. The case of glyphosate and one toxigenic cyanobacterium on Chlorophycean microalgae. Sci Total Environ. 2020:137186. https://doi.org/10.1016/j.scitotenv.2020.137186
Ostera JM, Malanga G, Puntarulo S. Assessment of oxidative balance in hydrophilic cellular environment in Chlorella vulgaris exposed to glyphosate. Chemosphere. 2020; 248:125955. https://doi.org/10.1016/j.chemosphere.2020.125955
Rizzo L. Bioassays as a tool for evaluating advanced oxidation processes in water and wastewater treatment. Water Res. 2011;45:4311–40. https://doi.org/10.1016/j.watres.2011.05.035
Gonçalves BB, Giaquinto PC, Silva DS, Neto CNS, Lima AA, Darosci AAB, et al. Ecotoxicology of glyphosate-based herbicides on aquatic environment. IntechOpen. 2019. https://doi.org/10.5772/intechopen.85157
Andersen RA. Algal culturing techniques. 1st ed. London: Elsevier Academic Press; 2005.
International Organization for Standardization (IOS). Water quality: fresh water algal growth inhibition test with Scenedesmus subspicatus and Selenastrum capricornutum. International Organization for Standardization. 1989;8692:1-6.
Nielsen SL, Hansen BW. Evaluation of the robustness of optical density as a tool for estimation of biomass in microalgal cultivation: The effects of growth conditions and physiological state. Aquac Res. 2019;50(9):2698-06. https://doi.org/10.1111/are.14227
Martínez-Ruiz EB, Martínez-Jerónimo F. Exposure to the herbicide 2,4-D produces different toxic effects in two different phytoplankters: A green microalga (Ankistrodesmus falcatus) and a toxigenic cyanobacterium (Microcystis aeruginosa). Sci Total Environ. 2018;1:619-20:1566-78. https://doi.org/10.1016/j.scitotenv.2017.10.145
Wellburn AR. The spectral determination of chlorophyll a and chlorophyll b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol. 1994;144:307–13. https://doi.org/10.1016/S0176-1617(11)81192-2
Magnusson M, Heimann K, Negri AP. Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar Pollut Bull. 2008;56(9):1545–52. https://doi.org/10.1016/j.marpolbul.2008.05.023
Christy SL, Karlander E, Parochetti JV. Effects of glyphosate on the growth rate of Chlorella. Weed Sci. 1981;29(1):5-7. https://doi.org/10.1017/S0043174500025728
EL-Sheekh MM. Effect of glyphosate herbicide on growth, photosynthesis and some metabolic activities of the green alga Chlorella kessleri (Chlorophyta). Egypt J Phycol. 2000; 1(1):87-97. https://doi.org/10.21608/egyjs.2000.113224
Wong PK. Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll–a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere. 2000;41(1-2):177–82. https://doi.org/10.1016/s0045-6535(99)00408-7
Reddy KN, Rimando AM, Duke SO. Aminomethylphosphonic acid, a metabolite of glyphosate, causes injury in glyphosate reated, glyphosate-resistant soybean. J Agric Food Chem. 2004;52:5139–43. https://doi.org/10.1021/jf049605v
Mateos-Naranjo E, Redondo-Gómez S, Cox L, Cornejo J, Figueroa ME. Effectiveness of glyphosate and imazamox on the control of the invasive cordgrass Spartina densiflora. Ecotoxicol Environ Saf. 2009;72:1694–700. https://doi.org/10.1016/j.ecoenv.2009.06.003
Zobiole LHS, Kremer RJ, Oliveira RS, Jr. Constantin J, Oliveira RS. Glyphosate affects chlorophyll, nodulation and nutrient accumulation of “second generation” glyphosate-resistant soybean (Glycine max L.). Pestic Biochem Physiol. 2011b;99:53–60. https://doi.org/10.1016/j.pestbp.2010.10.005
Huang J, Silva EN, Shen Z, Jiang B, Lu H. Effects of glyphosate on photosynthesis, chlorophyll fluorescence and physicochemical properties of cogongrass (Imperata cylindrica L.). Plant Omics Journal 2012;5:177–83.
Gomes MP, Le Manac'h SG, Hénault-Ethier L, Labrecque M, Lucotte M, Juneau P. Glyphosate-dependent inhibition of photosynthesis in willow. Front. Plant Sci. 2017;8:1–13. https://doi.org/10.3389/fpls.2017.00207
Cakmak I, Yazici A, Tutus Y, Ozturk L. Glyphosate reduced seed and leaf concentrations of calcium, manganese, magnesium and iron in non-glyphosate resistant soybean. Eur J Agron. 2009;31:114?19. https://doi.org/10.1016/j.eja.2009.07.001
Tanaka R, Tanaka A. Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol. 2007;58:321–46. https://doi.org/10.1146/annurev.arplant.57.032905.105448
Marsh HVJ, Evans HJ, Matrone G. Investigations of the role of iron in chlorophyll metabolism II. Effect of iron deficiency on chlorophyll synthesis. Plant Physiol. 1963;38:638–42. https://doi.org/10.1104/pp.38.6.638
Vivancos PD, Driscoll SP, Bulman CA, Ying L, Emami K, Treumann A, et al. Perturbations of amino acid metabolism associated with glyphosate-dependent inhibition of shikimic acid metabolism affect cellular redox homeostasis and alter the abundance of proteins involved in photosynthesis and photorespiration. Plant Physiol. 2011;157:256–68. https://doi.org/10.1104/pp.111.181024
Yanniccari M, Tambussi E, Istilart C, Castro AM. Glyphosate effects on gas exchange and chlorophyll fluorescence responses of two Lolium perenne L. biotypes with differential herbicide sensitivity. Plant Physiol Biochem. 2012;57:210–17. https://doi.org/10.1016/j.plaphy.2012.05.027
Choi CJ, Berges JA, Young EB. Rapid effects of diverse toxic water pollutants on chlorophyll a fluorescence: variable responses among freshwater microalgae. Water Res. 2012;46:2615?26. https://doi.org/10.1016/j.watres.2012.02.027
Muñoz-Rueda A, Gonzalez-Murua C, Becerril JM, Sánchez-Díaz MF. Effects of glyphosate [N-(phosphonomethyl)glycine] on photosynthetic pigments, stomatal response and photosynthetic electron transport in Medicago sativa and Trifolium pratense. Physiol Plant. 1986;66:63–68. https://doi.org/10.1111/j.1399-3054.1986.tb01234.x
Mukaka MM. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Medical Journal: the Journal of Medical Association of Malawi. 2012;24(3):69-71.
Descy JP, Métens A. Biomass-pigment relationships in potamoplankton. J Plankton Res. 1996;18(9):1557–66. https://doi.org/10.1093/plankt/18.9.1557
Borghini F, Colacevich A, Caruso T, Bargagli R. Algal biomass and pigments along a latitudinal gradient in Victoria Land lakes, East Antarctica. Polar Research. 2016;35. https://doi.org/10.3402/polar.v35.20703
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Somruthai Kaeoboon, Rungcharn Suksungworn, Nuttha Sanevas
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright and Licence details of published articles
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Open Access Policy
Plant Science Today is an open access journal. There is no registration required to read any article. All published articles are distributed under the terms of the Creative Commons Attribution License (CC Attribution 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited (https://creativecommons.org/licenses/by/4.0/). Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
