Abstract
In the present study, physiological and biochemical responses of Dunaliella salina exposed to acrylamide were investigated. The indicators were as follows: the growth, photosynthetic pigments, the contents of carbohydrate and protein, antioxidant system of Dunaliella salina. Besides, the ultrastructure and cell cycle distribution were also analyzed. The results showed that acrylamide could significantly inhibit the growth of D. salina (P < 0.05 or P < 0.01), and reduce the contents of photosynthetic pigments, carbohydrate and protein in D. salina cells. In addition, according to transmission electron microcopy (TEM) and flow cytometry (FCM), acrylamide could change cell ultrastructure and induce G1 phase arrest in D. salina cells. With the increase of acrylamide concentrations, the activities of superoxide dismutase (SOD) and catalase (CAT) in D. salina showed a rise first followed by a decline, whereas malondialdehyde (MDA) content increased sharply (P < 0.05 or P < 0.01). The results suggested that acrylamide was slightly toxic to Dunaliella salina and cause the physiological and biochemical changes. Anti-oxidation and cell cycle arrest may be the defense mechanism of algae responding to acrylamide.
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Abbreviations
- AM:
-
Acrylamide
- PAMs:
-
Polyacrylamides
- TU:
-
Toxicity unit
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalase
- GPx:
-
Glutathione peroxidase
- MDA:
-
Malondialdehyde
- IR:
-
Inhibitory rate
- EC50 :
-
Median effective concentration
- TEM:
-
Transmission electron microcopy
- FCM:
-
Flow cytometry
- PI:
-
Propidium iodide
- SD:
-
Standard deviation
- HSPs:
-
Heat stock proteins
- PCD:
-
Programmed cell death.
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Ahmed F, Schenk PM (2017) UV-C radiation increases sterol production in the microalga Pavlova lutheri. Phytochemistry 139:25–32. https://doi.org/10.1016/j.phytochem.2017.04.002
Albalasmeh AA, Berhe AA, Ghezzehei TA (2013) A new method for rapid determination of carbohydrate and total carbon concentrations using UV spectrophotometry. Carbohydr Polym 97:253–261. https://doi.org/10.1016/j.carbpol.2013.04.072
Almeida AC, Gomes T, Langford K, Thomas KV, Tollefsen KE (2017) Oxidative stress in the algae Chlamydomonas reinhardtii exposed to biocides. Aquat Toxicol 189:50–59. https://doi.org/10.1016/j.aquatox.2017.05.014
Babu MY, Palanikumar L, Nagarani N, Devi VJ, Kumar SR, Ramakritinan CM, Kumaraguru AK (2014) Cadmium and copper toxicity in three marine macroalgae: evaluation of the biochemical responses and DNA damage. Environ Sci Pollut Res 21:9604–9616. https://doi.org/10.1007/s11356-014-2999-0
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Belhaj D, Athmouni K, Frikha D, Kallel M, El Feki A, Maalej S, Zhou JL, Ayadi H (2017) Biochemical and physiological responses of halophilic nanophytoplankton (Dunaliella salina) from exposure to xeno-estrogen 17α-ethinylestradiol. Environ Sci Pollut Res Int 24:7392–7402. https://doi.org/10.1007/s11356-017-8415-9
Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendía ANA, Massart A, Poschenrieder C, Hariadi Y, Shabala S (2014) Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. Plant Cell Environ 37:589–600. https://doi.org/10.1111/pce.12180
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brandão F, Cappello T, Raimundo J, Santos MA, MaisanoM MA, Pacheco M, Pereira P (2015) Unravelling the mechanisms of mercury hepatotoxicity in wild fish (Liza aurata) through a triad approach: bioaccumulation, metabolomic profiles and oxidative stress. Metallomics 7:1352–1363. https://doi.org/10.1039/c5mt00090d
Cao DJ, Xie PP, Deng JW, Zhang HM, Ma RX, Liu C, Liu RJ, Liang YG, Li H, Shi XD (2015) Effects of Cu2+ and Zn2+ on growth and physiological characteristics of green algae, Cladophora. Environ Sci Pollut Res Int 22:16535–16541. https://doi.org/10.1007/s11356-015-4847-2
Duan WY, Meng FP, Lin YF, Wang GS (2017) Toxicological effects of phenol on four marine microalgae. EnvironToxicol Pharmacol 52:170–176. https://doi.org/10.1016/j.etap.2017.04.006
Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70. https://doi.org/10.1016/j.ecoenv.2016.11.029
Gao CF, Zhai Y, Ding Y, Wu QY (2010) Application of sweet sorghum for biodiesel production by heterotrophic microalga Chlorella protothecoides. Appl Energy 87:756–761. https://doi.org/10.1016/j.apenergy.2009.09.006
Gerashchenko BI, Takahashi T, Kosaka T, Hosoya H (2010) Life cycle analysis of unicellular algae. Curr Protoc Cytom, Chapter 11: Unit 11.19.1–6. https://doi.org/10.1002/0471142956.cy1119s52
Golubev AA, Prilepskii AY, Dykman LA, Khlebtsov NG, Bogatyrev VA (2016) Colorimetric evaluation of the viability of the microalga Dunaliella Salina as a test tool for nanomaterial toxicity. Toxicol Sci 151:115–125. https://doi.org/10.1093/toxsci/kfw023
Gorelova O, Baulina O, Ismagulova T, Kokabi K, Lobakova E, Selyakh I (2018) Stress-induced changes in the ultrastructure of the photosynthetic apparatus of green microalgae. Protoplasma 256:261–277. https://doi.org/10.1007/s00709-018-1294-1
Isidori M, Parella A, Piazza CML, Strada R (2000) Toxicity screening of surface waters in southern Italy and Toxkit microbiotests. In: Persoone G, Janssen C, De Coen W (eds) New Microbiotests for routine toxicity screening and biomonitoring. Kluwer Academic/ Plenum Publishers, New York, pp 289–293. https://doi.org/10.1007/978-1-4615-4289-6_33
Jaskowiak J, Tkaczyk O, Slota M, Kwasniewska J, Szarejko I (2018) Analysis of aluminum toxicity in Hordeum vulgare roots with an emphasis on DNA integrity and cell cycle. PLoS One 13:e0193156. https://doi.org/10.1371/journal.pone.0193156
Jia L, Raghupathy RK, Albalawi A, Zhao Z, Reilly J, Xiao Q, Shu X (2017) A colour preference technique to evaluate acrylamide-induced toxicity in zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 199:11–19. https://doi.org/10.1016/j.cbpc.2017.01.004
Kasson TM, Barry BA (2012) Reactive oxygen and oxidative stress: N-formyl kynurenine in photosystem II and non-photosynthetic proteins. Photosynth Res 114:97–110. https://doi.org/10.1007/s11120-012-9784-z
Khaskheli GB, Zuo F, Yu R, Chen S (2015) Overexpression of small heat shock protein enhances heat- and salt-stress tolerance of Bifidobacterium longum NCC2705. Curr Microbiol 71:8–15. https://doi.org/10.1007/s00284-015-0811-0
Kim SM, Baek JM, Lim SM, Kim JY, Kim J, Choi I, Cho KH (2015) Modified lipoproteins by acrylamide showed more Atherogenic properties and exposure of acrylamide induces acute hyperlipidemia and fatty liver changes in zebrafish. Cardiovasc Toxicol 15:300–308. https://doi.org/10.1007/s12012-014-9294-7
Larguinho M, Cordeiro A, Diniz MS, Costa PM, Baptista PV (2014) Metabolic and histopathological alterations in the marine bivalve Mytilus galloprovincialis induced by chronic exposure to acrylamide. Environ Res 135:55–62. https://doi.org/10.1016/j.envres.2014.09.004
Liu J, Chen F (2014) Biology and industrial applications of Chlorella: advances and prospects. Adv Biochem Eng Biotechnol 153:1–35. https://doi.org/10.1007/10_2014_286
Liu YJ, Zhao ZG, Si J, Di CX, Han J, An LZ (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. J Plant Growth Regul 59:207–214. https://doi.org/10.1007/s10725-009-9405-9
Liu Y, Tam NFY, Guan Y, Gao B (2012) Influence of a marine diatom on the embryonic toxicity of 17α-ethynylestradiol to the abalone Haliotis diversicolor Supertexta. Water Air Soil Pollut 223:4383–4395. https://doi.org/10.1007/s11270-012-1202-9
Liu Y, Wang F, Chen X, Zhang J, Gao BY (2015) Cellular responses and biodegradation of amoxicillin in Microcystis aeruginosa at different nitrogen levels. Ecotoxicol Environ Saf 111:138–145. https://doi.org/10.1016/j.ecoenv.2014.10.011
Machado MD, Lopes AR, Soares EV (2015) Responses of the alga Pseudokirchneriella subcapitata to long-term exposure to metal stress. J Hazard Mater 296:82–92. https://doi.org/10.1016/j.jhazmat.2015.04.022
Masyuk NP (1973) Morphology, Systematics, Ecology, Geographical Distribution of Dunaliella Teod. Genius and Trends of its Practical Application. Naukova Dumka, Kiev, Ukraine (in Russian)
Nie X, Wang X, Chen J, Zitko V, An T (2008) Response of the freshwater alga Chlorella vulgaris to trichloroisocyanuric acid and ciprofloxacin. Environ Toxicol Chem 27:168–173. https://doi.org/10.1897/07-028.1
Pichrtová M, Remias D, Lewis LA, Holzinger A (2013) Changes in phenolic compounds and cellular ultrastructure of arctic and antarctic strains of Zygnema (Zygnematophyceae, Streptophyta) after exposure to experimentally enhanced UV to PAR ratio. Microb Ecol 65:68–83. https://doi.org/10.1007/s00248-012-0096-9
Pingot D, Pyrzanowski K, Michałowicz J, Bukowska B (2013) Toxicity of acrylamide and its metabolite - glicydamide. Med Pr 64:259–271. https://doi.org/10.13075/mp.5893/2013/0022
Semla M, Goc Z, Martiniaková M, Omelka R, Formicki G (2017) Acrylamide: a common food toxin related to physiological functions and health. Physiol Res 66:205–217
Smith EA, Oeheme FW (1991) Acrylamide and polyacrylamide: a review of production, use, environmental fate and neurotoxicity. Rev Environ Health 9:215–228. https://doi.org/10.1515/REVEH.1991.9.4.215
Sousa CA, Soares HMVM, Soares EV (2018) Toxic effects of nickel oxide (NiO) nanoparticles on the freshwater alga Pseudokirchneriella subcapitata. Aquat Toxicol 204:80–90. https://doi.org/10.1016/j.aquatox.2018.08.022
Takahashi T, Yoshii M, Kawano T, Kosaka T, Hosoya H (2005) A new approach for the assessment of acrylamide toxicity using a green paramecium. Toxicol in Vitro 19(1):99–105. https://doi.org/10.1016/j.tiv.2004.06.012
Touzé S, Guerin V, Guezennec AG, Binet S, Togola A (2015) Dissemination of acrylamide monomer from polyacrylamide-based flocculant use-sand and gravel quarry case study. Environ Sci Pollut Res Int 22:6423–6430. https://doi.org/10.1007/s11356-014-3177-0
Wang Y, Zhang C, Zheng Y, Ge Y (2017) Phytochelatin synthesis in Dunaliella salina induced by arsenite and arsenate under various phosphate regimes. Ecotoxicol Environ Saf 136:150–160. https://doi.org/10.1016/j.ecoenv.2016.11.002
Xia B, Chen B, Sun X, Qu K, Ma F, Du M (2015) Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533. https://doi.org/10.1016/j.scitotenv.2014.11.066
Xu Y, Ibrahim IM, Harvey PJ (2016) The influence of photoperiod and light intensity on the growth and photosynthesis of Dunaliella salina (chlorophyta) CCAP 19/30. Plant Physiol Biochem 106:305–315. https://doi.org/10.1016/j.plaphy.2016.05.021
Zovko M, Vidaković-Cifrek Ž, Cvetković Ž, Bošnir J, Šikić S (2015) Assessment of acrylamide toxicity using a battery of standardised bioassays. Arh Hig Rada Toksikol 66:315–321. https://doi.org/10.1515/aiht-2015-66-2715
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This work was supported by the Natural Science Foundation of HeiLongJiang (No. C2018037), (No. C201123).
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Ling, N., Li, HX., Guo, HS. et al. Physiological and biochemical responses of Dunaliella salina exposed to acrylamide. Biologia 74, 1045–1053 (2019). https://doi.org/10.2478/s11756-019-00260-9
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DOI: https://doi.org/10.2478/s11756-019-00260-9