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Toxicity of marine pollutants on the ascidian oocyte physiology: an electrophysiological approach

Published online by Cambridge University Press:  13 December 2017

Alessandra Gallo
Alessandra Gallo*
Affiliation:
Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.
*
All correspondence to: Alessandra Gallo, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy. Tel: +39 0815833233. Fax +39 0817641355. E-mail: [email protected]
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Summary

In marine animals with external fertilization, gametes are released into seawater where fertilization and embryo development occur. Consequently, pollutants introduced into the marine environment by human activities may affect gametes and embryos. These xenobiotics can alter cell physiology with consequent reduction of fertilization success. Here the adverse effects on the reproductive processes of the marine invertebrate Ciona intestinalis (ascidian) of different xenobiotics: lead, zinc, an organic tin compound and a phenylurea herbicide were evaluated. By using the electrophysiological technique of whole-cell voltage clamping, the effects of these compounds on the mature oocyte plasma membrane electrical properties and the electrical events of fertilization were tested by calculating the concentration that induced 50% normal larval formation (EC50). The results demonstrated that sodium currents in mature oocytes were reduced in a concentration-dependent manner by all tested xenobiotics, with the lowest EC50 value for lead. In contrast, fertilization current frequencies were differently affected by zinc and organic tin compound. Toxicity tests on gametes demonstrated that sperm fertilizing capability and fertilization oocyte competence were not altered by xenobiotics, whereas fertilization was inhibited in zinc solution and underwent a reduction in organic tin compound solution (EC50 value of 1.7 µM). Furthermore, fertilized oocytes resulted in a low percentage of normal larvae with an EC50 value of 0.90 µM. This study shows that reproductive processes of ascidians are highly sensitive to xenobiotics suggesting that they may be considered a reliable biomarker and that ascidians are suitable model organisms to assess marine environmental quality.

Keywords

AscidianFertilizationHeavy metalIon currentOocyteOrganic tinPhenylurea herbicide
Type
Research Article
Information
Zygote , Volume 26 , Issue 1 , February 2018 , pp. 14 - 23
Copyright
Copyright © Cambridge University Press 2017 

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References

Alzieu, C. (2000). Impact of tributyltin on marine invertebrates. Ecotoxicology 9, 71–6.Google Scholar
Au, D. & Chiang, M. (2000). Effects of cadmium and phenol on motility and ultrastructure of sea urchin and mussel spermatozoa. Arch. Environ. Contam. Toxicol. 38, 455–63.CrossRefGoogle ScholarPubMed
Beiras, R. & Albentosa, M. (2004). Inhibition of embryo development of the commercial bivalves Ruditapes decussatus and Mytilus galloprovincialis by trace metals; implications for the implementation of seawater quality criteria. Aquaculture 230, 205–13.Google Scholar
Bellas, J. (2005). Toxicity assessment of the antifouling compound zinc pyrithione using early developmental stages of the ascidian. Ciona intestinalis Biofouling. 21, 289–96.Google Scholar
Bellas, J. (2006). Comparative toxicity of alternative antifouling biocides on embryos and larvae of marine invertebrates. Sci. Total. Environ. 367, 573–85.Google Scholar
Bellas, J. (2007). Toxicity of the booster biocide Sea-Nine to the early developmental stages of the sea urchin Paracentrotus lividus . Aquat. Toxicol. 83, 52–61.Google Scholar
Bellas, J., Vázquez, E. & Beiras, R. (2001). Toxicity of Hg, Cu, Cd, and Cr on early developmental stages of Ciona intestinalis (Chordata, Ascidiacea) with potential application in marine water quality assessment. Water Res. 35, 2905–12.CrossRefGoogle ScholarPubMed
Boni, R., Gallo, A., Montanino, M., Macina, A. & Tosti, E. (2016). Dynamic changes in the sperm quality of Mytilus galloprovincialis under continuous thermal stress. Mol. Reprod. Dev. 83, 162–73.Google Scholar
Brownlee, C. & Dale, B. (1990). Temporal and spatial correlation of fertilization current, calcium waves and cytoplasmic contraction in eggs of Ciona intestinalis . Proc. R. Soc. Lond. B Biol. Sci. 239, 321–8.Google ScholarPubMed
Cima, F., Ballarin, L., Bressa, G., Martinucci, G. & Burighel, P. (1996). Toxicity of organotin compounds on embryos of a marine invertebrate (Styela plicata; tunicata). Ecotoxicol. Environ. Saf. 35, 174–82.CrossRefGoogle ScholarPubMed
Cuomo, A., Silvestre, F., De Santis, R. & Tosti, E. (2006). Ca2+ and Na+ current patterns during oocyte maturation, fertilization, and early developmental stages of Ciona intestinalis . Mol. Reprod. Dev. 73, 501–11.Google Scholar
Dale, B. (1989). Fertilization in ascidians. In Nonmammalian Animal Models for Biomedical Research (eds Woodhead, A. & Vivirito, K.). Boca Raton, FL: CRC Press, 87 pp.Google Scholar
Dale, B. (1994). Oocyte activation in invertebrates and humans. Zygote 2, 373–7.Google Scholar
Dale, B. & De Felice, L. (1984). Sperm-activated channels in ascidian oocytes. Dev. Biol. 101, 235–9.Google Scholar
Danzo, B.J. (1997). Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ. Health Perspect. 105, 294.Google Scholar
Danzo, B.J. (1998). The effects of environmental hormones on reproduction.. Cell. Mol. Life Sci. 54, 1249–64.Google Scholar
Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–8.Google Scholar
Depledge, M., Weeks, J. & Bjerregaard, P. (1994). Heavy metals. In Handbook of Ecotoxicology (ed. Calow, P.), pp. 79–105. Oxford: Blackwell Scientific.Google Scholar
Falchuk, K. H. & Montorzi, M. (2001). Zinc physiology and biochemistry in oocytes and embryos. In Zinc Biochemistry, Physiology, and Homeostasis (ed. W. Maret) pp. 199–209. The Netherlands: Springer .Google Scholar
Fernández, N. & Beiras, R. (2001). Combined toxicity of dissolved mercury with copper, lead and cadmium on embryogenesis and early larval growth of the Paracentrotus lividus sea-urchin. Ecotoxicology 10, 263–71.Google Scholar
Ferrer, L., Andrade, S., Asteasuain, R. & Marcovecchio, J. (2006). Acute toxicities of four metals on the early life stages of the crab Chasmagnathus granulata from Bahia Blanca estuary, Argentina. Ecotoxicol. Environ. Saf. 65, 209–17.Google Scholar
Franchet, C., Goudeau, M. & Goudeau, H. (1999). Tributyltin impedes early sperm-egg interactions at the egg coat level in the ascidian Phallusia mammillata but does not prevent sperm-egg fusion in naked eggs. Aquat. Toxicol. 44, 213–28.Google Scholar
Gallo, A. & Tosti, E. (2013). Adverse effect of antifouling compounds on the reproductive mechanisms of the ascidian Ciona intestinalis . Mar. Drugs 11, 3554–68.CrossRefGoogle ScholarPubMed
Gallo, A. & Tosti, E. (2015a). The ascidian Ciona intestinalis as model organism for ecotoxicological bioassays. J. Marine Sci. Res. Dev. 5, e138.CrossRefGoogle Scholar
Gallo, A. & Tosti, E. (2015b). Ion currents involved in gamete physiology. Int. J. Dev. Biol. 59, 261–70.Google Scholar
Gallo, A. & Tosti, E. (2015c). Reprotoxicity of the antifoulant chlorothalonil in ascidians: an ecological risk assessment. PLoS ONE 10, e0123074.Google Scholar
Gopalakrishnan, S., Thilagam, H. & Raja, P. (2007). Toxicity of heavy metals on embryogenesis and larvae of the marine sedentary polychaete Hydroides elegans . Arch. Environ. Contam. Toxicol. 52, 171–8.Google Scholar
Gallo, A., Silvestre, F., Cuomo, A., Papoff, F. & Tosti, E. (2011). The impact of metals on the reproductive mechanisms of the ascidian Ciona intestinalis. Mar. Ecol. 32, 222–31.Google Scholar
Gallo, A., Boni, R., Buttino, I. & Tosti, E. (2016). Spermiotoxicity of nickel nanoparticles in the marine invertebrate Ciona intestinalis (ascidians). Nanotoxicology 10, 1096–104.Google Scholar
Gallo, A., Boni, R. & Tosti, E. (2018). Sperm viability assessment in marine invertebrates by fluorescent staining and spectrofluorimetry: A promising tool for assessing marine pollution impact. Ecotoxicol. Environ. Saf., 147, 407–12.Google Scholar
Henson, M. C. & Chedrese, P. J. (2004). Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. 229, 383–92.CrossRefGoogle ScholarPubMed
Holt, E. A. & Miller, S. W. (2011). Bioindicators: using organisms to measure environmental impacts. Nature Education Knowledge 3, 8.Google Scholar
Itow, T., Loveland, R. & Botton, M. (1998). Developmental abnormalities in horseshoe crab embryos caused by exposure to heavy metals. Arch. Environ. Contam. Toxicol. 35, 33–40.Google Scholar
Manzo, S. (2004). Sea urchin embryotoxicity test: proposal for a simplified bioassay. Ecotoxicol. Environ. Saf. 57, 123–8.Google Scholar
Martin, M., Osborn, K. E., Billig, P. & Glickstein, N. (1981). Toxicities of ten metals to Crassostrea gigas and Mytilus edulis embryos and Cancer magister larvae. Mar. Poll. Bull. 12, 305–8.Google Scholar
Matranga, V. & Corsi, I. (2012). Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar. Environ. Res. 76, 32–40.Google Scholar
Nacci, D., Jackim, E. & Walsh, R. (1986). Comparative evaluation of three rapid marine toxicity tests: sea urchin early embryo growth test, sea urchin sperm cell toxicity test and Microtox. Environ. Toxicol. Chem. 5, 521–5.Google Scholar
Papadopoulou, C. & Kanias, G. D. (1977). Tunicate species as marine pollution indicators. Mar. Poll. Bull. 8, 229–31.Google Scholar
Patricolo, E., Mansueto, C., D'Agati, P. & Pellerito, L. (2001). Organometallic complexes with biological molecules: XVI. Endocrine disruption effects of tributyltin (IV) chloride on metamorphosis of the ascidian larva. Appl. Organomet. Chem. 15, 916–23.Google Scholar
Pennati, R., Groppelli, S., Zega, G., Biggiogero, M., De Bernardi, F. & Sotgia, C. (2006). Toxic effects of two pesticides, Imazalil and Triadimefon, on the early development of the ascidian Phallusia mammillata (Chordata, Ascidiacea). Aquat. Toxicol. 79, 205–12.CrossRefGoogle ScholarPubMed
Popek, W., Dietrich, G., Glogowski, J., Demska-Zakeś, K., Drag-Kozak, E., Sionkowski, J., Łuszczek-Trojan, E., Epler, P., Demianowicz, W. & Sarosiek, B. (2005). Influence of heavy metals and 4-nonylphenol on reproductive function in fish. Reprod. Biol. 6, 175–88.Google Scholar
Porte, C., Janer, G., Lorusso, L., Ortiz-Zarragoitia, M., Cajaraville, M., Fossi, M. & Canesi, L. (2006). Endocrine disruptors in marine organisms: approaches and perspectives. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 143, 303–15.Google Scholar
Sasakura, Y., Inaba, K., Satoh, N., Kondo, M. & Akasaka, K. (2009). Ciona intestinalis and Oxycomanthus japonicus, representatives of marine invertebrates. Exp. Anim. 58, 459–69.CrossRefGoogle ScholarPubMed
Satoh, N. (1994). Developmental Biology of Ascidians. Cambridge: Cambridge University Press.Google Scholar
Segner, H. (2009). Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 187–95.CrossRefGoogle Scholar
Silvestre, F., Cuomo, A. & Tosti, E. (2009). Ion current activity and molecules modulating maturation and growth stages of ascidian (Ciona intestinalis) oocytes. Mol. Reprod. Dev. 76, 1084–93.Google Scholar
Tosti, E. & Boni, R. (2004). Electrical events during gamete maturation and fertilization in animals and humans. Hum. Reprod. Update 10, 53–65.Google Scholar
Tosti, E., Gallo, A. & Silvestre, F. (2011). Ion currents involved in oocyte maturation, fertilization and early developmental stages of the ascidian Ciona intestinalis . Mol. Reprod. Dev. 78, 854–60.Google Scholar
Tosti, E. & Ménézo, Y. (2016). Gamete activation: basic knowledge and clinical applications. Hum. Reprod. Update 22, 420–39.CrossRefGoogle ScholarPubMed
Villa, L., Agati, P., Mansueto, C., Pellerito, C., Scopelliti, M., Fiore, T., Nagy, L. & Pellerito, L. (2003). Effects of tributyltin (IV) chloride on the gametes and fertilization of Ascidia malaca (Ascidiacea: Tunicata). Appl. Organomet. Chem. 17, 106–12.Google Scholar
Voulvoulis, N., Scrimshaw, M. & Lester, J. (1999). Alternative antifouling biocides. Appl. Organomet. Chem. 13, 135–43.Google Scholar
Wang, Q., Liu, B., Yang, H., Wang, X. & Lin, Z. (2009). Toxicity of lead, cadmium and mercury on embryogenesis, survival, growth and metamorphosis of Meretrix meretrix larvae. Ecotoxicology 18, 829–37.Google Scholar
Waykar, B. & Deshmukh, G. (2012). Evaluation of bivalves as bioindicators of metal pollution in freshwater. Bull. Environ. Contam. Toxicol. 88, 48–53.Google Scholar
Wong, C., Chu, K., Tang, K., Tam, T. & Wong, L. (1993). Effects of chromium, copper and nickel on survival and feeding behaviour of Metapenaeus ensis larvae and postlarvae (Decapoda: Penaeidae). Mar. Environ. Res. 36, 63–78.Google Scholar
Wurl, O. & Obbard, J. P. (2004). A review of pollutants in the sea-surface microlayer (SML): a unique habitat for marine organisms. Mar. Poll. Bull. 48, 1016–30.Google Scholar
Yamada, H. (2007). Behaviour, occurrence, and aquatic toxicity of new antifouling biocides and preliminary assessment of risk to aquatic ecosystems. Bull. Fish. Res. Dev. Agency 21, 31–45.Google Scholar
Zega, G., De Bernardi, F., Groppelli, S. & Pennati, R. (2009a). Effects of the azole fungicide Imazalil on the development of the ascidian Ciona intestinalis (Chordata, Tunicata): morphological and molecular characterization of the induced phenotype. Aquat. Toxicol. 91, 255–61.Google Scholar
Zega, G., Pennati, R., Candiani, S., Pestarino, M. & De Bernardi, F. (2009b). Solitary ascidians embryos (Chordata, Tunicata) as model organisms for testing coastal pollutant toxicity. Invertebr. Surviv. J 6, S29–34.Google Scholar
Zhou, Q., Zhang, J., Fu, J., Shi, J. & Jiang, G. (2008). Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal. Chim. Acta 606, 135–50.Google Scholar