Abstract
The use of delayed fluorescence intensity as an endpoint for rapid estimation of the effective concentration (ECx) has been reported as an alternative to standard growth inhibition (at 72 h after exposure) in some algal species including Pseudokirchneriella subcapitata. In marine algae, although an approach of bioassaying using delayed fluorescence measurements has not been performed yet, its development would provide many benefits for marine environmental risk assessment. In this study, we selected marine cyanobacterium Cyanobium sp. (NIES-981) as our test algal species and demonstrated that this species is valid for the standard growth inhibition test based on criteria provide by Organization for Economic Co-operation and Development guidelines. Furthermore, standard inhibition tests and shorter period test using DF were performed in NIES-981 using five chemicals (3,5-DCP, simazine, diflufenican, K2Cr2O7, and CuSO4), and their EC50 and low-toxic-effect values (EC10, EC5, and NOEC) were determined from two dose-response curves. Based on comparisons of the two dose-response curves and the EC50 values, we conclude that DF intensity is useful as an endpoint for rapid estimation of EC50 in NIES-981.
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References
Arnold W, Davidson JB (1954) The identity of the fluorescent and delayed light emission spectra in Chlorella. J Gen Physiol 37:677–684
Berden-Zrimec M, Drinovec L, Zrimec A (2010) Delayed fluorescence. In: Sugget, DJ, Prasil O, Borowitzka M (eds) Chlorophyll a fluorescence in aquatic sciences: Methods and applications. Springer, Dordrecht, pp 293–309
Burda K, Kruk J, Strzalka K, Schmid GH (2002) Stimulation of oxygene evolution in photosystem II by copper (II) ions. Z Naturforsch 57:853–857
Comber MHI, Smyth DV, Thompson RS (1995) Assessment of the toxicity to algae of colored substances. Bull Environ Contam Toxicol 55:922–928
Conrad R, Büchel C, Wilhelm C, Arsalane W, Berkaloff C et al. (1993) Changes in yield of in-vivo fluorescence of chlorophyll a as a tool for selective herbicide monitoring. J Appl Phycol 5:505–516
Drinovec L, Drobne D, Jerman I, Zrimec A (2004) Delayed fluorescence of Lemna minor: a biomarker of the effects of copper, cadmium, and zinc. Bull Environ Contam Toxicol 72:896–902
Ebenezer V, Ki J (2013) Quantification of the sub-toxicity of metals and endocrine-disrupting chemicals to the marine green microalga Tetraselmis suecica. Fish Aquat Sci 16:187–194
Escher BI, Bramaz N, Quayle P, Rutishauser S, Vermeirssen ELM (2008) Monitoring of the ecotoxicological hazard potential by polar organic micropolutants in sewage treatment plants and surface waters using a mode-of-action based test battery. J Environ Monit 10:622–631
Franklin NM, Stauber JL, Apte SC, Lim RP (2002) Effect of initial cell density of the bioavailability and toxicity of copper in microalgal bioassays. Environ Toxicol Chem 21:742–751
Gerhardt V, Kretsch G (1989) Development of a delayed fluorescence based biotest for detection of water pollutants. Dortmunder Beiträge zur Wasserforschung, Grundlagen und Anwendungsbereiche der Chlorophyllfluoreszenz; Veröffentlichungen des Instituts für Wassersforschung GmbH Dortmund und der Hydrobiologischen Abteilung der Dortmunder Stadtwerke AG 37:87–95
International Standard (ISO 10253:2006)(2006) Water quality–Marine algal growth inhibition test with Skeletonema costatum and Phaeodactylum tricornutum.
Joliot P, Joliot A, Bouges B, Barbieri G (1971) Studies of system-II photocenters by comparative measurements of luminescence, fluorescence, and oxygen emission. Photochem Photobiol 14:287–305
Jursinic PA (1986) Delayed fluorescence: current concepts and status. In: Govindjee JA, Fork DC (eds) Light emission by plants and bacteria. Academic Press, New York, pp 291–328
Kallqvist T, Romstad R (1994) Effects of agricultural pesticides on planktonic algae and cyanobacteria: examples of interspecies sensitivity variations. Norway J Agric Sci Suppl 13:117–131
Kasai K, Kawachi M, Erata M, Mori F, Yumoto K, Ishimoto M (2009) NIES-Collection, List of strains, 8th edn. Jpn J Phycol 57:220
Katsumata M, Koike T, Kazumura K, Takeuchi A, Sugaya Y (2009) Utility of delayed fluorescence as endpoint for rapid estimation of effect concentration on the green alga Pseudokirchneriella subcapitata. Bull Environ Contam Toxicol 83:484–487
Katsumata M, Koike T, Nishikawa M, Kazumura K, Tsuchiya H (2006) Rapid ecotoxicological bioassay using delayed fluorescence in the green alga Pseudokirchneriella subcapitata. Water Res 40:3393–3400
Kooijman SALM, Hanstveit AO, Nyholm N (1996) No-effect concentrations in algal growth inhibition tests. Water Res 30:1625–1632
Leunert F, Grossart HP, Gerhardt V, Eckert W (2013) Toxicant induced changes on delayed fluorescence decay kinetics of cyanobacteria and green algae: a rapid and sensitive biotest. Plos One 8:e63127
Mayer P, Frickmann J, Christensen ER, Nyholm N (1998) Influence of growth conditions on the results obtained in algal toxicity tests. Environ Toxicol Chem 1091–1098
Millán de Kuhn R, Streb C, Breiter R, Richter P, Neeβe T, Häber DP (2006) Screening for unicellular algae as possible bioassay organisms for monitoring marine water samples. Water Res 40:2695–2703
Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL (2000) Fate and ecotoxicity of the new antifouling compound irgarol 1051 in the aquatic environment. Water Res 34:3523–3530
Organization for Economic Cooperation and Development (OECD) (1984) Guideline for testing of chemicals no. 201. Alga growth inhibition test, Pairs
Pérez J, Domingues I, Soares AMVM, Loureiro S (2011) Growth rate of Pseudokirchneriella subcapitata exposed to herbicides found in surface waters in the alqueva reservoir (Portugal): a bottom-up approach using binary mixtures. Ecotoxicology 20:1167–1175
Radix P, Léonard M, Papantoniou C, Roman G, Saouter E, Gallotti-Schmitt S, Thébaud H, Vasseur P (2000) Comparison of four chronic toxicity tests using algae, bacteria, and invertebrates assessed with sixteen chemicals. Ecotoxicol Environ Safety 47:186–194
Sbrilli G, Bimbi B, Cioni F, Pagliai L, Luchi F, Lanciotti E (2005) Surface and ground waters characterization in Tuscany (Italy) by using algal bioassay and pesticide determinations: comparative evaluation of the results and hazard assessment of the pesticides impact on primary productivity. Chemosphere 58:571–578
Schmidt W, Senger H (1987a) Long-term delayed luminescence in Scenedesmus obliquus I. Spectral and kinetics properties. Biochem Biophys 890:15–22
Schmidt W, Senger H (1987b) Long-term delayed luminescence in Scenedesmus obliquus II. Influence of exogenous factors. Biochem Biophys 981:22–27
Schreiber U, Muller JF, Haugg A, Gademann R (2002) New type of dual channel PAM chlorophyll fluorometer for highly sensitive water toxicity biotests. Photosynth Res 74:317–330
Shigeoka T, Sato Y, Takeda Y, Yoshida K, Yamauchi F (1988) Acute toxicity of chlorophenols to green algae, Selenastrum capricornutum and Chlorella vulgaris, and quantitative structure-activity relationships. Environ Toxicol Chem 7:847–854
Strehler BL, Arnold W (1951) Light production by green plants. J Gen Physiol 34:809–820
Thompson JA (1997) Cellular fluorescence capacity as an endpoint in algal toxicity testing. Chemosphere 35:2027–2037
Vallotton N, Iida R, Eggen L, Escher BI, Krayenbuhl J et al. (2008) Effect of pulse herbicidal exposure on Scenedesmus vacuoleatus: a comparison of two photosystem II inhibitors. Environ Toxicol Chem 27:1399–1407
Van der Hoeven N (1997) How to measure no effect. Part 1: towards a new measure of chronic toxicity. Environmentrics 8:241–248
Vignati DAL, Dominik J, Beye ML, Pettine M, Ferrari BJD (2010) Chromiumu (VI) is more toxic than chromium(III) to freshwater algae: a paradigm to revise. Ecotoxicol Environ Safety 73:743–749
Wang W, Gorsuch JW, Lower WR (eds) (1990) Plants for toxicity assessment. ASTM STP 1091, Philadelphia, PA, pp 40–48
Warne MJ, Dam R (2008) NOEC and LOEC data should no longer be generated or used. Australasian J Ecotoxicol 14:1–5
Weyman GS, Rufli H, Eltje L, Salinas ER, Hamitou M (2012) Aquatic toxicity tests with substances that are poorly soluble in water and consequences for environmental risk assessment. Environ Toxicol Chem 31:1662–1669
Wyman M, Gregory RPF, Carr NG (1985) Novel role phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Nature 230:818–820
Yamaguchi H, Shimura Y, Suzuki S, Yamagishi T, Tatarazako N, Kawachi M (2016) Complete genome sequence of Cyanobium sp. NIES-981, a potentially useful marine strain for ecotoxicological bioassay. Genome Announc 4:e00736–16
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This work was partially supported by Council for Science, Technology and innovation (CSTI), Cross-ministerial Strategic Innovation Promotion Program (SIP), “Next-generation technology for ocean resources exploration”.
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Yamagishi, T., Katsumata, M., Yamaguchi, H. et al. Rapid ecotoxicological bioassay using delayed fluorescence in the marine cyanobacterium Cyanobium sp. (NIES-981). Ecotoxicology 25, 1751–1758 (2016). https://doi.org/10.1007/s10646-016-1718-7
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DOI: https://doi.org/10.1007/s10646-016-1718-7