Abstract
In this work, we evaluated the removal efficiency of diclofenac by Chlorella vulgaris OW-01, Nannochloropsis oculata CCAP 849/7, Scenedesmus acutus UTEX 72, and Scenedesmus obliquus CCAP 276/2. Each microalga was grown in media with different concentrations (50 and 100% of the original formulation) of carbon, nitrogen, and phosphorus, to evaluate their effect on the removal of diclofenac. We also evaluated the photodegradation of diclofenac under the same conditions. The diclofenac removed from the media ranged from 59 to 92%, obtaining the highest removal with S. obliquus. The diclofenac adsorbed on the cell walls ranged from 12.2 to 26.5%, obtaining the highest adsorption with S. obliquus. The diclofenac degraded by light ranged from 15 to 28%. The nutrient deficit showed no influence on the removal of diclofenac in any of the microalgae under study. These results indicate that S. obliquus is the best alternative for the bioremediation of diclofenac.
Similar content being viewed by others
Data availability
All data are incorporated into the article and its online supplementary material.
Code availability
Not applicable.
References
Alessandretti I, Toniciolli-Rigueto CV, Torres-Nazari M, Rosseto M, Dettmer A (2021) Removal of diclofenac from wastewater: a comprehensive review of detection, characteristics and tertiary treatment techniques. J Environ Chem Eng 9:106743. https://doi.org/10.1016/j.jece.2021.106743
Alharbi SK, Ansari AJ, Nghiem LD, Price WE (2022) New transformation products from ozonation and photolysis of diclofenac in the aqueous phase. Process Saf Environ 157:106–114. https://doi.org/10.1016/j.psep.2021.10.050
Anne-Marie K, Yee W, Loh SH, Thye AA, Cha S (2020) Effects of excess and limited phosphate on biomass, lipid and fatty acid contents and the expression of four fatty acid desaturase genes in the tropical Selenastraceaen Messastrum gracile SE-MC4. Appl Biochem Biotechol. https://doi.org/10.1007/s12010-019-03182-z
Arnold KE, Boxall ABA, Brown AR, Cuthbert RJ, Gaw S, Hutchinson TH, Jobling S, Madden JC, Metcalfe CD, Naidoo V, Shore RF, Smits JE, Taggart MA, Thompson HM (2013) Assessing the exposure risk and impacts of pharmaceuticals in the environment on individuals and ecosystems. Biol Lett 9:20130492. https://doi.org/10.1098/rsbl.2013.0492
Barsanti L (2006) Algae. Anatomy, biochemistry and biotechnology. CRC Press, Boca Raton
Ben-Ouada S, Ben-Ali R, Cimetiere N, Leboulanger C, Ben-Ouada H, Sayadi S (2019) Biodegradation of diclofenac by two green microalgae: Picocystis sp. y Graesiella sp. Ecotoxicol Environ Saf 186:109769. https://doi.org/10.1016/j.ecoenv.2019.109769
Bonnefille B, Courant F, Gomez E (2018) Diclofenac in the marine environment: a review of its occurrence and effects. Mar Pollut Bull 131(Part A):496–506. https://doi.org/10.1016/j.marpolbul.2018.04.053
Brönmark C, Hansson LA (2005) The biology of lakes and ponds. University Press, Oxford
Cai T, Park SY, Li Y (2013) Nutrient recovery from wastewater streams by microalgae: status and prospects. Renew Sust Energ Rev 19:360–369. https://doi.org/10.1016/j.rser.2012.11.030
Cleuvers M (2004) Mixture toxicity of the anti-Inflammatory drugs diclofenac, ibuprofen, naproxen and acetylsalicylic acid. Ecotoxicol Environ Saf 59:309–315. https://doi.org/10.1016/S0147-6513(03)00141-6
Corcoll N, Acuña V, Barceló D, Casellas M, Guasch H, Huerta B, Petrovic M, Ponsatí L, Rodríguez-Mozaz S, Sabater S (2014) Pollution-induced community tolerance to non-steroidal anti—inflammatory drugs (NSAIDs) in fluvial biofilm communities affected by WWTP effluents. Chemosphere 112:185–193. https://doi.org/10.1016/j.chemosphere.2014.03.128
Croom E (2012) Chapter Three - Metabolism of Xenobiotics of Human Environments. Chapter Three-Metabolism Xenobiotics Human Environ 112:31–88. https://doi.org/10.1016/B978-0-12-415813-9.00003-9
Cuellar-Bermudez SP, Alemán-Nava GS, Chandra R, García-Pérez JS, Contreras-Angulo JR, Markou G, Muylaert K, Rittmann BE, Parra-Saldivar R (2017) Nutrients utilization and contaminants removal. A review of two approaches of algae and cyanobacteria in wastewater. Algal Res 24:438–449. https://doi.org/10.1016/j.algal.2016.08.018
De Oliveira T, Guégan R, Thiebault T, Milbeau CL, Le Milveau C, Muller F, Teixeira V, Giovanela M, Boussafir M (2016) Adsorption of diclofenac onto orgnoclays: effects of surfactant and environmental (pH and temperature) conditions. J Hazar Mater 323:558–566. https://doi.org/10.1016/j.jhazmat.2016.05.001
de Wilt A, Butkovskyi A, Tuantet K, Leal LH, Fernandes TV, Langenhoff A, Zeeman G (2016) Micropollutant removal in an algal treatment system fed with source separated wastewater streams. J Hazar Mater 304:84–92. https://doi.org/10.1016/j.jhazmat.2015.10.033
Dragone G (2022) Challenges and opportunities to increase economic feasibility and sustainability of mixotrophic cultivation of green microalgae of the genus Chlorella. Renew Sustain Energy Rev 160:112284. https://doi.org/10.1016/j.rser.2022.112284
Escher B, Bramaz N, Eggen R, Richter M (2005) In vitro assessment of modes of toxic action of pharmaceuticals in aquatic life. Environ Sci Technol 39(9):3090–3100. https://doi.org/10.1021/ess048590e
Fini A, Bassini G, Monastero A, Cavallari C (2012) Diclofenac salts, VIII. Effect of the counterions on the permeation through porcine membrane from aqueous saturated solutions. Pharmaceutics 4:413–429. https://doi.org/10.3390/pharmaceutics4030413
Goswami RK, Agrawal K, Verma P (2022) Microalgal-based remediation of wastewater: a step towards environment protection and management. Environ Qual Manag. https://doi.org/10.1002/tqem.21850
Gröner F, Höhne C, Kleiner W, Kloas W (2017) Chronic diclofenac exposure affects gill integrity and pituitary gene expression and displays estrogenic activity in nile tilapia (Oreochromis niloticus). Chemosphere 166:473–481. https://doi.org/10.1016/j.chemosphere.2016.09.116
Henriques M, Silva A, Rocha J (2007) Extraction and quantification of pigments from a marine microalga: a simple and reproducible method. Commun Curr Res Educ Topics Trends Appl Microbiol Formatex 2:586–593
Jerez CG, Malapascua JR, Sergejevová M, Figueroa FL, Masojídek J (2016) Effect of nutrient starvation under high irradiance on lipid and starch accumulation in Chlorella fusca (Chlorophyta). Marine Biotechnol 18:24–36. https://doi.org/10.1007/s10126-015-9664-6
Kamal MA, Iimura N, Nabekura T, Kitagawa S (2007) Enhanced skin permeation of diclofenac by ion-pair formation and further enhancement by microemulsion. Chem Pharm Bull 55:368–371. https://doi.org/10.1248/cpb.55.368
Koul B, Sharma K, Shah M (2022) Phycoremediation: a sustainable alternative in wastewater treatment (WWT) regime. Environ Technol Innovation 25:102040. https://doi.org/10.1016/j.eti.2021.102040
Kumar R, Qureshi M, Kumar-Vishwakarma D, Al-Ansari N, Kuriqi A, Elbeltagi A, Saraswat A (2022) A review on emerging water contaminants and the application of sustainable removal technologies. Case Stud Chem Env Eng 6:100219. https://doi.org/10.1016/j.cscee.2022.100219
Kunkel U, Radke M (2012) Fate of pharmaceuticals in rivers: deriving a benchmark dataset at favorable attenuation conditions. Water Res 46:5551–5565. https://doi.org/10.1016/j.watres.2012.07.033
Lee J, Ji K, Lim Kho Y, Kim P, Choi K (2011) Chronic exposure to diclofenac on two freswater cladocerans and Japanese medaka. Ecotoxicol Environ Saf 74:1216–1225. https://doi.org/10.1016/j.ecoenv.2011.03.014
Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177. https://doi.org/10.1007/s11120-010-9583-3
Leong WH, Mohamad-Saman NA, Kiatkittipong W, Assabumrungrat S, Najdanovic-Visak V, Wang J, Shiong-Khoo J, Kee-Lam M, Mohamad M, Wei-Lim J (2022) Photoperiod-induced mixotrophic metabolism in chlorella vulgaris for high biomass and lipid to biodiesel productions using municipal wastewater medium. Fuel 313:123052. https://doi.org/10.1016/j.fuel.2021.123052
Li R, Chen GZ, Tam NFY, Luan TG, Shin PKS, Cheung S, Liu T (2009) Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii. Ecotox Environ Saf 72:321–328. https://doi.org/10.1016/j.ecoenv.2008.05.012
Li F, Gao D, Hu Hanhua H (2014) High-efficiency nuclear transformation of the oleaginous marine Nannochloropsis species using PCR product. Biosci Biotechnol Biochem 78:812–817. https://doi.org/10.1080/09168451.2014.905184
Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049. https://doi.org/10.1007/s10529-009-9975-7
Liu Y, Guan YT, Gao QT, Tam NFY, Zhu WP (2010) Cellular responses, biodegradation and bioaccumulation of endocrine disrupting chemicals in marine diatom Navicula incerta. Chemosphere 80:592–599. https://doi.org/10.1016/j.chemosphere.2010.03.042
Majewska M, Harshkova D, Gucsiora M, Aksmann A (2018) Phytotoxic activity of diclofenac: evaluation using a model green algal Chlamydomonas reinhardtii with atrazine as a reference substance. Chemosphere 209:989–997. https://doi.org/10.1016/j.chemosphere.2018.06.156
Martínez ME, Sánchez S, Jiménez JM, Yousfi FE, Muñoz L (2000) Nitrogen and phosphorus removal from urban wastewater by the microalga Scenedesmus obliquus. Biotechnol Rep 73:263–272. https://doi.org/10.1016/j.btre.2016.04.003
Maryjoseph S, Ketheesan B (2020) Microalgae based wastewater treatment for the removal of emerging contaminants: a review of challenges and opportunities. Case Stud Chem Env Eng 2:100046. https://doi.org/10.1016/j.cscee.2020.100046
Matamoros V, Gutierrez R, Ferrer I, García J, Bayona J (2015) Capability of microalgae-based wastewater treatment systems to remove emerging organic contaminants: a pilot-scale study. J Hazard Mater 288:34–42. https://doi.org/10.1016/j.jhazmat.2015.02.002
Montes JP, Pulido M (2012) Obtención de protocolos para el aislamiento, cultivo y extracción de ADN de Chlorella vulgaris Beyerinck. El Astrolabio 11:47–54
Mullan J, Weston KMBA, Burns P, Mullan J, Rudd R (2017) Con-sumer knowledge about over-the-counter NSAIDs: they don’t know what they don’t know. Aust New Zealand J Public Health 41:210. https://doi.org/10.1111/1753-6405.12589
Nicolaou A, Meric S, Fatta D (2007) Occurrence pattern of pharmaceuticals in water and wastewater environments. Anal Bioanal Chem 387(4):1225–1234. https://doi.org/10.1007/s00216-006-1035-8
Norvill ZN, Shilton A, Guieysse B (2016) Emerging contaminant degradation and removal in algal wastewater treatment ponds: Identifying the research gaps. J Hazard Mater 313:291–309. https://doi.org/10.1016/j.jhazmat.2016.03.085
Pérez O, Escalante FM, de Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36. https://doi.org/10.1016/j.watres.2010.08.037
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA Bioenergetics. 975:384–394. https://doi.org/10.1016/S0005-2728(89)80347-0
Posadas E, Bochon S, Coca M, García-González MC, García-Encina PA, Muñoz R (2014) Microalgae-based agro-industrial wastewater treatment: a preliminary screening of biodegradability. J Appl Phycol 26:2335–2345. https://doi.org/10.1016/j.cscee.2020.100046
Priyadharshini SD, Babu PS, Manikandan S, Subbaiya R, Govarthanan M, Karmegam N (2021) Phycoremediation of wastewater for pollutant removal: a green approach to environmental protection and long-term remediation. Environ Poll 290:117989. https://doi.org/10.1016/j.envpol.2021.117989
Ribeiro H, Rodrigues I, Napoleao L, Lira L, Marques D, Veríssimo M, Andrade JP, Dourado M (2022) Non-steroidal anti-inflammatory drugs (NSAIDs), pain and aging: Adjusting prescription to patient features. Biom Pharm 150:112958. https://doi.org/10.1016/j.biopha.2022.112958
Rivera-Utrilla J, Sanchez-Polo M, Ferro-Garcia MA, Prados-Joya G, Ocampo-Perez R (2013) Pharmaceuticals as emerging contaminants and their removal from water. A Review Chemosphere 93:1268–1287
Round FE (1973) Biologia das Algas. Editora Guanabara Dois S.A, Rio de Janeiro
Ruiz-Marin A, Mendoza-Espinosa LG, Stepherson T (2010) Growth and nutrient removal in free and immobilized green algae in batch and semi-continuous cultures treating real wastewater. Bioresour Technol 101:58–64. https://doi.org/10.1016/j.biortech.2009.02.076
Samal K, Mahapatra S, Hibzur Ali MD (2022) Pharmaceutical wastewater as emerging contaminants (EC): treatment technologies, impact on environment and human health. Energy Nexus 6:100076. https://doi.org/10.1016/j.nexus.2022.100076
Sánchez-Torres H, Juscamaita J, Vargas J (2008) Crecimiento mixotrófico de la microalga Nannochloropsis oculata en ensilado biológico de pescado. The Biologist 6:94–100
Santos CE, de Coimbra NR, Paniagua-Bermejo S, García-Perez AI, Otero-Cabero M (2017) Comparative assessment of pharmaceutical removal from wastewater by the microalgae Chlorella sorokiniana, Chlorella vulgaris y Scenedesmus obliquus. In: Farooq R, Ahmad Z (eds) Biological wastewater treatment and resource recovery. London, IntechOpen. Available from: https://www.intechopen.com/chapters/53770. https://doi.org/10.5772/66772
Scholz MJ, Weiss TL, Jinkerson RE, Jing J, Roth R, Goodenough U, Posewitz MC, Gerken HG (2014) Ultrastructure and composition of the Nannochloropsis gaditana cell wall. Eukaryot Cell 13:1450–1464. https://doi.org/10.1128/EC.00183-14
Sophia AC, Lima EC (2018) Removal of emerging contaminants from the environment by adsorption. Ecotoxicol Environ Saf 150:1–17. https://doi.org/10.1016/j.ecoenv.2017.12.026
Szopinska M, Potapowicz J, Jankowska K, Luczkiewicz A, Svahn O, Björklund E, Nannou C, Lambropoulou D, Polkowska Z (2022) Pharmaceuticals and other contaminants of emerging concern in Admiralty Bay as a result of untreated wastewater discharge: Status and possible environmental consequences. Sci Total Environ 835:155400. https://doi.org/10.1016/j.scitotenv.2022.155400
Wang S, Zheng L, Han X, Yang B, Li J, Sun C (2018) Lipid accumulation and CO2 utilization of two marine oil-rich microalgal strains in response to CO2 aeration. Acta Oceanol Sin 37:119–126. https://doi.org/10.1007/s13131-018-1171-y
Weissmannova HD, Pavlosky J, Fiserova L, Kosarova H (2018) Toxicity of diclofenac: cadmium binary mixtures to algae Desmodesmus subspicatus using nomalization method. Bulletin of Environ Contam Toxicol 101:205–213. https://doi.org/10.1007/s000128-018-2384-7
Wongrakpanich S, Wongrakpanich A, Melhado K, Rangaswami JA (2018) Comprehensive review of non-steroidal anti-inflammatory drug use in the elderly. Aging Dis 9:143–150. https://doi.org/10.14336/AD.2017.0306
Xiong JQ, Kurade MB, Jeon BH (2018) Can microalgae remove pharmaceutical contaminants from water? Trends Biotechnol 36:30–44. https://doi.org/10.1016/j.tibtech.2017.09.003
Xu M, Huang H, Li N, Li F, Wang D, Luo Q (2019) Occurrence and ecological risk of pharmaceuticals and personal care products (PPCPs) and pesticides in typical surface watersheds, China. Ecotoxicol Environ Saf 175:289–298. https://doi.org/10.1016/j.ecoenv.2019.01.131
Yeh K, Chang J (2012) Effects of cultivation conditions and media composition on cell growth and lipid productivity of indigenous microalgae Chlorella vulgaris ESP-31. Bioresour Technol 105:120–127. https://doi.org/10.1016/j.biortech.2011.11.103
Yu SJ, Hu H, Zheng H, Wang YQ, Pan SB, Zeng RJ (2019) Effect of different phosphorus concentrations on biodiesel production from Isochrysis zhangjiangensis under nitrogen sufficiency or deprivation condition. Appl Microbiol Biotechnol 103:5051–5059. https://doi.org/10.1007/s00253-019-09814-y
Zhang Z, Volkman JK (2017) Algaenan structure in the microalga Nannochloropsis oculata characterized from stepwise pyrolysis. Org Geochem 104:1–7. https://doi.org/10.1016/j.orggeochem.2016.11.005
Zhang DQ, Gersberg RM, Hua T, Zhu J, Goyal MK, Ng WJ, Tan SK (2013) Fate of pharmaceutical compounds in hydroponic mesocosms planted with Scirpus validus. Environm Pollut 181:98–106. https://doi.org/10.1016/j.envpol.2013.06.016
Zhang Y, Guo J, Yao T, Zhang Y, Zhou X, Chu H (2019) The influence of four pharmaceuticals on Chlorella pyrenoidosa culture. Sci Rep 9:1624. https://doi.org/10.1038/s41598-018-36609-4
Zhou GJ, Peng FQ, Zhang LJ, Ying GG (2012) Biosorption of zinc and copper from aqueous solutions by two freshwater green microalgae Chlorella pyrenoidosa and Scenedesmus obliquus. Environ Sci Pollut Res 19:2918–2929. https://doi.org/10.1007/s11356-012-0800-9
Zhou GJ, Peng FQ, Zhang LJ, Ying GG (2013) Cellular responses and bioremoval of nonylphenol and octylphenol in the freshwater green microalga Scenedesmus obliquus. Ecotoxicol Environ Saf 87:10–16. https://doi.org/10.1016/j.ecoenv.2012.10.002
Zhu S, Liu B, Chen B, Zhang J, Liu W (2014) Effects of three pharmaceuticals and personal care products on growth and photosystem II in Scenedesmus obliquus. Zhongshan Daxue Xuebao/acta Scientiarum Natralium Universitatis Sunyatseni 53(1):121-126+134
Zuorro A, Maffei G, Lavecchia R (2017) Kinetic modeling of azo dye adsorption on non-living cells of Nannochloropsis oceanica. J Environ Chem Engineer 5:4121–4127. https://doi.org/10.1016/j.jece.2017.07.078
Acknowledgements
Sincere thanks are due to Dr. Roberto Rico Martínez from the Autonomous University of Aguascalientes for kindly providing the microalgae used in this project and to Dra. Luz María Teresita Paz Maldonado from the Bioreactors Engineering Laboratory at the Autonomous University of San Luis Potosí for providing equipment to perform the necessary analyses in this project. Also thanks to the National Council of Science and Technology (CONACyT) for the grant awarded with registration number 252858.
Funding
The authors did not receive support from any organization for the submitted work.
Author information
Authors and Affiliations
Contributions
SS: conceptualization, methodology, formal analysis, investigation, writing-original draft, visualization. GO: resources, formal analysis, writing-review and editing. GC: and VM: resources, writing-review and editing, supervision. SG: conceptualization, validation, resources, writing-review and editing, supervision, project administration, funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Ethics approval
Not applicable.
Consent to participle
Not applicable.
Consent to publication
Not applicable.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sánchez-Sandoval, D.S., González-Ortega, O., Vazquez-Martínez, J. et al. Diclofenac removal by the microalgae species Chlorella vulgaris, Nannochloropsis oculata, Scenedesmus acutus, and Scenedesmus obliquus. 3 Biotech 12, 210 (2022). https://doi.org/10.1007/s13205-022-03268-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-022-03268-2