Abstract
The present study demonstrates that the environment play a vital role in the development of tolerance in the local algal isolates towardsalpha-cypermethrin. The isolates collected from rice fields (Scenedesmus ecornis NC-M9 and Tetradesmus dimorphus NC-K2) showed significantly higher tolerance than the isolates collected from freshwater bodies far from the rice fields. Also, significant reduction in Malondialdehyde (MDA) content was noticed in S. ecornis NC-M9 after fourth and seventh day exposure to alpha-cypermethrin compared to first day exposure. However, the Superoxide Dismutase (SOD) and Peroxidase (POD) contents of S. ecornis NC-M9 enhanced at 4th and 7th day exposure to alpha-cypermethrin compared to 1st day exposure. Further, biochemical studies of all isolates show that Graesiella emersonii NC-M1(the isolate from freshwater bodies near to rice field) possesses higher contents of Chlorophyll a (Chl a), carotenoid and lipid (5.59 ± 0.36 mg·L−1, 2.5 ± 0.024 mg·L−1 and 28 ± 2.5% Dry Cell Weight (DCW), respectively) compared to other. This variation in biochemical parameters present in different field areas as collected and tested could be further used as potential substrates for production of bioactive compounds which have many health and environmental benefits.
Similar content being viewed by others
Abbreviations
- MDA:
-
Malondialdehyde
- SOD:
-
Superoxide Dismutase
- POD:
-
Peroxidase
- DCW:
-
Dry Cell Weight
- CAT:
-
Catalase
- DMSO:
-
Dimethylsulphoxide
- TCA:
-
Trichloroacetic acid
- TBA:
-
Thiobarbituric acid
- PVP:
-
Polyvinylpyrrolidone
- EDTA:
-
Ethylenediamine tetraacetic acid
- NBT:
-
Nitro Blue Tetrazolium
- Chl a :
-
Chlorophyll a
- Chl b :
-
Chlorophyll b
- PCR:
-
Polymerase Chain Reaction
- ITS:
-
Internal Transcribed Spacer
- TAG:
-
Triacylglycerols
References
Amamra R, Djebar MR, Grara N, Moumeni O, Otmani H, Alayat A, Berrebbah H (2015) Cypermethrin-induces oxidative stress to the freshwater ciliate model: Paramecium tetraurelia. Annu Res Rev Biol ISSN: 2347–565X. Doi: https://doi.org/10.9734/ARRB/2015/10852
Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12(1):128–152. https://doi.org/10.3390/md12010128
Amorós I, Alonso JL, Romaguera S, Carrasco JM (2007) Assessment of toxicity of a glyphosate-based formulation using bacterial systems in lake water. Chemosphere 67:2221–2228. https://doi.org/10.1016/j.chemosphere.2006.12.020
Apt KE, Behrens PW (1999) Commercial developments in microalgal biotechnology. J Phycol 35(2):215–226. https://doi.org/10.1046/j.1529-8817.1999.3520215.x
Bhatnagar A, Makandar MB, Garg MK, Bhatnagar B (2008) Community structure and diversity of cyanobacteria and green algae in the soils of Thar Desert (India). J Arid Environ 72:73–83. https://doi.org/10.1016/j.jaridenv.2007.05.007
Borowitzka MA, Beardall J, Raven JA (2016) The physiology of microalgae. Dev Appl Phycol 6. https://doi.org/10.1007/978-3-319-24945-2
Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43(1):83–11. https://doi.org/10.1146/annurev.pp.43.060192.000503
Buono S, Langellotti AL, Martello A, Rinna F, Fogliano V (2014) Functional ingredients from microalgae. Food Funct 5(8):1669–1685. https://doi.org/10.1039/C4FO00125G
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods Enzymol 2:764–775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chen Z, Juneau P, Qiu B (2007) Effects of three pesticides on the growth, photosynthesis and photoinhibition of the edible cyanobacterium Ge-Xian-Mi (Nostoc). Aquat Toxicol 81(3):256–265. https://doi.org/10.1016/j.aquatox.2006.12.008
Del Campo JA, Moreno J, Rodrı́guez H, Vargas MA, Rivas J, Guerrero MG (2000) Carotenoid content of Chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotechnol 76:51–59. https://doi.org/10.1016/S0168-1656(99)00178-9
Deng X, Fei X, Li Y (2011) The effects of nutritional restriction on neutral lipid accumulation in Chlamydomonas and Chlorella. Afr J Microbiol Res 5:260–270. https://doi.org/10.5897/AJMR10.557
Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Murthy KNC, Ravishankar GA (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Technol 16(9):389–406. https://doi.org/10.1016/j.tifs.2005.02.006
Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92(4):696–717. https://doi.org/10.1111/j.1399-3054.1994.tb03042.x
Gahagan HE, Holm RE, Abeles FB (1968) Effect of ethylene on peroxidase activity. Physiol Plant 21(6):1270–1279. https://doi.org/10.1111/j.1399-3054.1968.tb07358.x
Galhano V, Santos H, Oliveira MM, Laranjo JG, Peixoto F (2011) Changes in fatty acid profile and antioxidant systems in a Nostoc muscorum strain exposed to the herbicide bentazon. Process Biochem 46:2152–2162. https://doi.org/10.1016/j.procbio.2011.08.015
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Gosetti F, Bolfi B, Chiuminatto U, Manfredi M, Robotti E, Marengo E (2018) Photodegradation of the pure and formulated alpha-cypermethrin insecticide gives different products. Environ Chem Lett 16:581–590. https://doi.org/10.1007/s10311-017-0685-4
Gouveia L, Batista AP, Miranda A, Empis J, Raymundo A (2007) Chlorella vulgaris biomass used as colouring source in traditional butter cookies. Innov Food Sci Emerg Technol 8(3):433–436. https://doi.org/10.1016/j.ifset.2007.03.026
Gu XZ, Zhang GY, Chen L, Dai RL, Yu YC (2008) Persistence and dissipation of synthetic pyrethroid pesticides in red soils from the Yangtze River Delta area. Environ Geochem Health 30:67–77. https://doi.org/10.1007/s10653-007-9108-y
Gür Ö, Özdal M, Algur ÖF (2014) Biodegradation of the synthetic pyrethroid insecticide α-cypermethrin by Stenotrophomonas maltophilia OG2. Turk J Biol 38(5):684–689. https://doi.org/10.3906/biy-1402-10
Gurbuz F, Ciftci H, Akcil A (2009) Biodegradation of cyanide containing effluents by Scenedesmus obliquus. J Hazard Mater 162(1):74–79. https://doi.org/10.1016/j.jhazmat.2008.05.008
Gwak Y, Hwang Y, Wang B, Kim M, Jeong J, Lee CG, Hu Q, Han D, Jin E (2014) Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis. J Exp Bot 65:4317–4334. https://doi.org/10.1093/jxb/eru206
Harun R, Singh M, Gareth MF, Michael KD (2010) Bioprocess engineering of microalgae to produce a variety of consumer products. Renew Sustain Energy Rev 14:1037–1047. https://doi.org/10.1016/j.rser.2009.11.004
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):1891–1898. https://doi.org/10.1016/0003-9861(68)90654-1
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1133. https://doi.org/10.1139/b79-163
Ibrahim WM, Karam MA, El-Shahat RM, Adway AA (2014) Biodegradation and utilization of organophosphorus pesticide malathion by cyanobacteria. Biomed Res Int 2014:1–6. https://doi.org/10.1155/2014/392682
Iummato MM, Fassiano A, Graziano M, dos Santos AM, de Molina MDCR, Juárez ÁB (2019) Effect of glyphosate on the growth, morphology, ultrastructure and metabolism of Scenedesmus vacuolatus. Ecotoxicol Environ Saf 172:471–479. https://doi.org/10.1016/j.ecoenv.2019.01.083
Kaur S, Sarkar M, Srivastava RB, Gogoi HK, Kalita MC (2012) Fatty acid profiling and molecular characterization of some freshwater microalgae from India with potential biodiesel production. New Biotechnol 29(3):332–344. https://doi.org/10.1016/j.nbt.2011.10.009
Kumar MS, Praveenkumar R, Jeon BH, Thajuddin N (2014) Chlorpyrifos induced changes in the antioxidants and fatty acid compositions of Chroococcus turgidus NTMS12. Lett Appl Microbiol 59(5):535–541. https://doi.org/10.1111/lam.12311
Kumar MS, Kabra AN, Min B, El-Dalatony MM, Xiong J, Thajuddin N, Jeon BH (2016) Insecticides induced biochemical changes in freshwater microalga Chlamydomonas Mexicana. Environ Sci Pollut Res 23(2):1091–1099. https://doi.org/10.1007/s11356-015-4681-6
Laskowski DA (2002) Physical and chemical properties of pyrethroids. Rev Environ Contam Toxicol 174:49–170. https://doi.org/10.1007/978-1-4757-4260-2-3
Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33(2):258–278. https://doi.org/10.1111/j.1574-6976.2008.00134.x
Li HZ, Cheng F, Wei YL, Lydy MJ, You J (2017) Global occurrence of pyrethroid insecticides in sediment and the associated toxicological effects on benthic invertebrates: an overview. J Hazard Mater 324:258–271. https://doi.org/10.1111/j.1574-6976.2008.00134.x
Liu F, Pang SJ (2010) Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. J Exp Mar Biol Ecol 382:82–87. https://doi.org/10.1016/j.jembe.2009.11.005
Luis LG, Ferreira P, Fonte E, Oliveira M, Guilhermino L (2015) Does the presence of microplastics influence the acute toxicity of chromium (VI) to early juveniles of the common goby (Pomatoschistus microps)? A study with juveniles from two wild estuarine populations. Aquat Toxicol 164:163–174. https://doi.org/10.1016/j.aquatox.2015.04.018
Mandal MK, Chaurasia N (2018) Molecular characterization of freshwater microalgae and nutritional exploration to enhance their lipid yield. 3 Biotech 8:238–252. https://doi.org/10.1007/s13205-018-1248-5
Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33(5):541–553. https://doi.org/10.1093/oxfordjournals.pcp.a078288
Moon-van der Staay SY, Gerog WM, Guillou L, Vaulot D (2000) Abundance and diversity of prymnesiophytes in the picoplankton community from the equatorial Pacific Ocean inferred from 18S rDNA sequences. Limnol Oceanogr 45:98–109. https://doi.org/10.4319/lo.2000.45.1.0098
Padhy R, Panigrahi A (2014) The secret story of the farmer’s friend: the case of Anabaena cylindrica. Int J Curr Microbiol App Sci 3(12):296–303 http://www.ijcmas.com
Rafique N, Tariq SR, Ahmed D (2016) Monitoring and distribution patterns of pesticide residues in soil from cotton/wheat fields of Pakistan. Environ Monit Assess 188:695. https://doi.org/10.1007/s10661-016-5668-6
Rausch T (1981) The estimation of micro-algal protein content and its meaning to the evaluation of algal biomass I. Comparison of methods for extracting protein. Hydrobiologia 78:237–251. https://doi.org/10.1007/BF00008520
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 111:1–6. https://doi.org/10.1099/00221287-111-1-1
Romero DM, Molina MCR, Juarez AB (2011) Oxidative stress induced by acommercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotoxicol Environ Saf 74:741–747. https://doi.org/10.1016/j.ecoenv.2010.10.034
Safafar H, Nørregaard PU, Ljubic A, Møller P, Holdt SL, Jacobsen C (2016) Enhancement of protein and pigment content in two Chlorella species cultivated on industrial process water. J Mar Sci Eng 4:84–99. https://doi.org/10.3390/jmse4040084
Sarada R, Ranga Rao A, Sandesh BK, Dayananda C, Anila N, Chauhan VS, Ravishankar GA (2012) Influence of different culture conditions on yield of biomass and value added products in microalgae. Dyn Biochem Process Biotechnol Mol Biol 6(2):77–85 http://www.globalsciencebooks.info/Online/GSBOnline/images/2012/DBPBMB_6(SI2)/DBPBMB_6(SI2)77-85o.pdf
Schager M, Muller B (2006) Acclimation of chlorophyll a and carotenoid levels to different irradiances in four freshwater cyanobacteria. J Plant Physiol 163:709–716. https://doi.org/10.1016/j.jplph.2005.09.015
Singh DP, Khattar JI, Kaur M, Kaur G, Gupta M, Singh Y (2013) Anilofos tolerance and its mineralization by the cyanobacterium Synechocystis sp. strain PUPCCC 64. PLoS One 8(1):1–10. https://doi.org/10.1371/journal.pone.0053445
Spiro RG (1966) Analysis of sugars found in glycoproteins. Methods Enzymol 8:3–26. https://doi.org/10.1016/0076-6879(66)08005-4
Srivastava AK, Bhargava P, Rai LC (2005) Salinity and copper-induced oxidative damage and changes in the antioxidative defence systems of Anabaena doliolum. World J Microbiol Biotechnol 21:1291–1298. https://doi.org/10.1007/s11274-005-2442-2
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tiwari B, Singh S, Singh M, Mishra AK (2014) Regulation of organophosphate metabolism in cyanobacteria- a review. Microbiology 84(3):291–302. https://doi.org/10.1134/S0026261715030200
Torres MA, Barros MP, Campos SCG, Pinto E, Rajamani S, Sayre RT, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicol Environ Saf 71:1–15. https://doi.org/10.1016/j.ecoenv.2008.05.009
Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20. https://doi.org/10.1111/j.0022-3646.1991.00014.x
Vendrell E, de Gómez Barreda FD, Sabater C, Carrasco JM (2009) Effectof glyphosate on growth of four fresh water species of phytoplankton:a microplate bioassay. Bull Environ Contam Toxicol 82:538–542. https://doi.org/10.1007/s00128-009-9674-z
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Brawley SH (2016) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29(2):949–982. https://doi.org/10.1007/s10811-016-0974-5
Wu L, Qiu Z, Zhou Y, Du Y, Liu C, Ye J, Hu X (2016) Physiological effects of the herbicide glyphosate on the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 178:72–79. https://doi.org/10.1016/j.aquatox.2016.07.010
Yordanova V, Stoyanova T, Traykov I, Boyanovsky B (2009) Toxicological effects of Fastac insecticide (Alpha – Cypermethrin) to Daphnia magna and Gammarus pulex. Biotechnol Biotechnol Equip 23(1):393–395. https://doi.org/10.1080/13102818.2009.10818447
Yu X, Chen L, Zhang W (2015) Chemicals to enhance microalgal growth and accumulation of high-value bioproducts. Front Microbiol 6:56. https://doi.org/10.3389/fmicb.2015.00056
Yuan NN, Chen SN, Zhai LX, Schnabel G, Yin LF, Luo CX (2013) Baseline sensitivity of Monilia yunnanensis to the DMI fungicides tebuconazole and triadimefon. Eur J Plant Pathol 136:651–655. https://doi.org/10.1007/s10658-013-0200-0
Zhang J, Sun Z, Sun P, Chen T, Chen F (2014) Microalgal carotenoids: beneficial effects and potential in human health. Food Funct 5(3):413–425. https://doi.org/10.1039/C3FO60607D
Zhu F, Massana R, Not F, Marie D, Vaulot D (2005) Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiol Ecol 52:79–92. https://doi.org/10.1016/j.femsec.2004.10.006
Acknowledgments
Authors gratefully acknowledge the financial support of Department of Biotechnology (BT/PR12716/PBD/26/478/2015), DST-SERB (BT/PR12716/PBD/26/478/2015), Council of Scientific & Industrial Research [09/347(222)/2017-EMR-I], Rajiv Gandhi National Fellowship for OBC Students (UGC) (201819-NFO-2018-19-OBC-ASS-76611) DST-FIST, and UGC-SAP, Government of India. Authors are also thankful to the Head of Department, Biotechnology and Bioinformatics, North-Eastern Hill University for providing the necessary facilities.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical approval
The manuscript does not contain experiments on animals and human; hence ethical permission not required.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chanu, N.K., Mandal, M.K. & Chaurasia, N. Correlating the influence of biochemical parameters in environment with pesticide tolerance of non-target algae. Biologia 76, 307–319 (2021). https://doi.org/10.2478/s11756-020-00568-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-020-00568-x