Single and interactive effects of the antifouling booster herbicides diuron and Irgarol 1051 on photosynthesis in the marine cyanobacterium, Arthrospira maxima

Toxicology and Environmental Health Sciences

Volumn 5, Issue 2, 2013, Pages 71-81

  Kottuparambil, Sreejith ^a   Lee, Sulah ^a   Han, Taejun ^a  

^a SolarLight Ltd   (South Korea)

Author keywords

Arthrospira maxima; Chlorophyll a fluorescence; Diuron; Irgarol 1051; Mixture toxicity

Indexed keywords

2 TERT BUTYLAMINO 4 CYCLOPROPYLAMINO 6 METHYLTHIO 1, 3, 5 TRIAZINE; DIURON; PLASTOQUINONE; UNCLASSIFIED DRUG;

ALGAL CELL CULTURE; ARTHROSPIRA MAXIMA; ARTICLE; CHLOROPHYLL FLUORESCENCE; CONTROLLED STUDY; ELECTRON TRANSPORT; FOULING CONTROL; MARINE BACTERIUM; MICROALGA; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; TOXICITY TESTING;

EID: 84880987213     PISSN: 20059752     EISSN: 22337784     Source Type: Journal    
DOI: 10.1007/s13530-013-0157-6     Document Type: Article

References (50)

1. Evans, S. M., Birchenough, A. C. & Brancato, M. S. The TBT ban: Out of the frying pan into the fire? Mar. Poll. Bull. 40, 204-211 (2000).
2. Schultz, M. P., Bendick, J. A., Holm, E. R. & Hertel, W. M. Economic impact of biofouling on a naval surface ship. Biofouling27, 87-98 (2011).
3. Manzo, S., Buono, S. & Cremisini, C. Toxic effects of Irgarol and Diuron on sea urchin Paracentrotus lividus early development, fertilization, and offspring quality. Arch. Environ. Contam. Toxicol. 51, 61-68 (2006).
4. Thomas, K. V., McHugh, M. & Waldock, M. Antifouling paint booster biocides in UK coastal waters: inputs, occurrence, and environmental fate. Sci. Tot. Environ. 293, 117-127 (2002).
5. Kostantinou, I. K. & Albanis, T. A. Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ. Int. 30, 248-253 (2004).
6. Voulvoulis, N., Scrimshaw, M. D. & Lester, J. N. Alternative antifouling biocides. Appl. Organomet. Chem. 13, 135-143 (1999).
7. Thomas, K. V., Blake, S. J. & Waldock, M. J. Antifouling paint booster biocide contamination in UK marine sediments. Mar. Poll. Bull. 40, 739-745 (2000).
8. Koutsaftis, A. & Aoyama, I. The interactive effects of binary mixtures of three antifouling biocides and three heavy metals against marine algae Chaetoceros gracilis. Environ. Toxicol. 21, 432-439 (2006).
9. Fernández-Alba, A. R., Hernando, M. D., Piedra, L. & Chisti, Y. Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal. Chim. Acta456, 303-312 (2002).
10. Bao, V. W. W., Leung, K. M. Y., Qiu, J. W. & Lam, M. H. W. Acute toxicities of five commonly used antifouling booster biocides to selected subtropical and cosmopolitan marine species. Mar. Pollut. Bull. 62, 1147-1151 (2011).
11. Magnusson, M., Heimann, K. & Negri, A. P. Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar. Pollut. Bull. 56, 1545-1552 (2008).
12. Magnusson, M., Heimann, K., Quayle, P. & Negri, A. P. Additive toxicity of herbicide mixtures and comparative sensitivity of tropical benthic microalgae. Mar. Pollut. Bull. 60, 1978-1987 (2010).
13. Seery, C. R., Gunthorpe, L. & Ralph, P. J. Herbicide impact on Hormosira banksii gametes measured by fluorescence and germination bioassays. Environ. Pollut. 140, 43-51 (2006).
14. Schreiber, U., Quayle, P., Schmidt, S., Escher, B. I. & Mueller, J. F. Methodology and evaluation of a highly sensitive algae toxicity test based on multiwall chlorophyll fluorescence imaging. Biosens. Bioelectron. 22, 2554-2563 (2007).
15. Gatidou, G. & Thomaidis, N. Evaluation of single and joint toxic effects of two antifouling biocides, their main metabolites and copper using phytoplankton bioassays. Aquat. Toxicol. 85, 184-191 (2007).
16. Küster, A. & Altenburger, R. Development and validation of a new fluorescence based bioassay for aquatic macrophyte species. Chemosphere67, 194-201 (2007).
17. Chesworth, J. C., Donkin, M. E. & Brown, M. T. The interactive effects of the antifouling herbicides Irgarol 1051 and Diuron on the seagrass Zostera marina (L). Aquat. Toxicol. 66, 293-305 (2004).
18. Campbell, D., Hurry, V., Clarke, A., Gustafsson, P. & Öquist, G. Chlorophyll fluorescence analysis of cyanoacterial photosynthesis and acclimation. Microbiol. Mol. Biol. Rev. 6, 667-683 (1998).
19. Belay, A. in Spirulina: Physiology, cell-biology and biotechnology (ed Vonshak, A.) 131-158 (Taylor and Francis, London, 2004).
20. Yamaguchi, K. Recent advances in microalgal bioscience in Japan, with special reference to utilization of biomass and metabolites: a review. J. Appl. Phycol. 8, 487-502 (1997).
21. Ciferri, O. Spirulina, the edible microorganism. Microbiol. Rev. 47, 551-578 (1983).
22. Becker, W. Microalgae in human and animal nutrition. In Handbook of microalgal culture (ed Richmond, A.) 312-351 (Blackwell, Oxford, 2004).
23. Misra, S. & Kaushik, B. D. Growth promoting substances of cyanobacteria. I. Vitamins and their influences on rice plants. Proc. Ind. Natl. Sci. Acad. B55, 295-300 (1989).
24. Torres-Duran, P. V., Ferreira-Hermosillo, A. & Juarez-Oropeza, M. A. Anti-hyperlipemic and anti-hypertensive effects of Spirulina maxima in an open sample of Mexican population: a preliminary report. Lipids Health Dis. 6, 33-40 (2007).
25. Devilla, R. A. et al. Impact of antifouling booster biocides on single microalgal species and on a natural marine phytoplankton community. Mar. Ecol. Prog. Ser. 286, 1-12 (2005).
26. Backhaus, T. et al. Joint algal toxicity of phenylurea herbicides is equally predictable by concentration addition and independent action. Environ. Toxicol. Chem. 23, 258-264 (2004).
27. Brack, W. & Frank, H. Chlorophyll a fluorescence: a tool for the investigation of toxic effects in the photosynthetic apparatus. Ecotox. Environ. Safe. 40, 34-41 (1998).
28. Kumar, K. S. & Han, T. Toxicity of single and combined herbicides on PSII maximum efficiency of an aquatic higher plant, Lemna sp. Toxicol. Environ. Health Sci. 3, 97-105 (2011).
29. Fai, P. B., Grant, A. & Reid, B. Chlorophyll a fluorescence as a biomarker for rapid toxicity assessment. Environ. Toxicol. Chem. 26, 1520-1531 (2007).
30. Muller, R. et al. Rapid exposure assessment of PSII herbicides in surface water using a novel chlorophyll a fluorescence imaging assay. Sci. Tot. Environ. 401, 51-59 (2008).
31. Pollet, B., Steppe, K., van Labeke, M.-C. & Lemeur, R. Diurnal cycle of chlorophyll fluorescence in Phalaenopsis. Photosynthetica47, 309-312 (2009).
32. Lu, C. M., Chau, C. W. & Zhang, J. H. Acute toxicity of excess mercury on the photosynthetic performance of cyanobacterium, S. platensis-assessment by chlorophyll fluorescence analysis. Chemosphere41, 191-196 (2000).
33. Kirilovsky, D. Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical quenching mechanism. Photosynth. Res. 93, 7-16 (2007).
34. Deng, X., Gao, K. & Sun, J. Physiological and biochemical responses of Synechococcus sp. PCC7942 to Irgarol 1051 and Diuron. Aquat. Toxicol. 122-123, 113-119 (2012).
35. Zhang, A. Q., Leung, K. M. Y., Kwok, K. W. H., Bao, V. W. W. & Lam, M. H. W. Toxicities of antifouling biocide Irgarol 1051 and its major degraded product to marine primary producers. Mar. Pollut. Bull. 57, 575-586 (2008).
36. Podola, B. & Melkonian, M. Selective real-time herbicides monitoring by an array chip biosensor employing diverse microalgae. J. Appl. Phycol. 17, 261-271 (2005).
37. Bednarz, T. The effect of pesticides on the growth of green and blue-green algae cultures. Acta Hydrobiol (Krakow)23, 155-172 (1981).
38. Ma, J. et al. Toxicity of 40 herbicides to the green algae Chlorella vulgaris. Ecotoxicol. Environ. Safe. 51, 128-132 (2002).
39. Spurgeon, D. J. et al. Systems toxicology approaches for understanding the joint effects of environmental chemical mixtures. Sci. Tot. Environ. 408, 3725-3734 (2010).
40. Faust, M., Altenburger, R., Boedeker, W. & Grimme, L. H. Additive effects of herbicide combinations on aquatic non target organisms. Sci. Tot. Environ. 134, 941-952 (1993).
41. Dahl, B. & Blanck, H. Toxic effects of the antifouling agent Irgarol 1051 on periphyton communities in coastal water microcosms. Mar. Poll. Bull. 32, 342-350 (1996).
42. Faust, M. et al. Predicting the joint algal toxicity of multi-component s-triazine mixtures at low-effect concentrations of individual toxicants. Aquat. Toxicol. 56, 13-32 (2001).
43. Zamora-Ley, I. M., Gardinali, P. R., Jochem, F. J. Assessing the effects of Irgarol 1051 on marine phytoplankton populations in Key Largo Harbor, Florida. Mar. Poll. Bull. 52, 935-941 (2006).
44. Schlösser, U. G. SAG-Sammlung von Algenkulturen at the University of Göttingen. Catalogue of strains. Bot. Acta107, 111-186 (1994).
45. Schreiber, U., Hormann, H., Neubauer, C. & Klughammer, C. Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust. J. Plant Physiol. 22, 209-220 (1995).
46. Gisi, U. Synergistic interaction of fungicides in mixtures. Phytopathology86, 1273-1279 (1996).
47. Mayer, F. L. in Acute Toxicity Handbook of Chemicals to Estuarine Organisms (US Environmental Protection Agency, Gulf Breeze, FL, 274 1987).
48. Jones, R. J. & Kerswell, A. P. Phytotoxicity of Photosystem II (PSII) herbicides to coral. Mar. Ecol. Prog. Ser. 261, 149-159 (2003).
49. Sanchez-Ferandin, S., Leroy, F., Bouget, F.-Y. & Joux, F. A new, sensitive marine microalgal recombinant biosensor using luminescence monitoring for the toxicity testing of antifouling biocides. Appl. Environ. Microbiol. 79, 631-638 (2013).
50. Buma, A. G. J., Sjollema, S. B., van de Poll, W. H., Klamer, H. J. C. & Bakker, J. C. Impact of the antifouling agent Irgarol 1051 on marine phytoplankton species. J. Sea Res. 61, 133-139 (2009).