Toxicity induced by three antibiotics commonly used in aquaculture on the marine microalga Tetraselmis suecica (Kylin) Butch

Marine Environmental Research

Volumn 101, Issue 1, 2014, Pages 1-7

  Seoane, Marta ^a   Rioboo, Carmen ^a   Herrero, Concepción ^a   Cid, Ángeles ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

Antibiotics; Cell activity; Cell viability; Growth inhibition; Microalga; Photosynthesis; Toxicity

Indexed keywords

ALGAE; AQUACULTURE; AQUATIC ECOSYSTEMS; AQUATIC ORGANISMS; CELLS; CYTOLOGY; MOBILE SECURITY; PHOTOSYNTHESIS; PHYSIOLOGICAL MODELS; TOXICITY;

AQUACULTURE FACILITY; BIOCHEMICAL PARAMETERS; BIOLOGICAL INDICATORS; CELL ACTIVITY; CELL VIABILITY; GROWTH INHIBITION; MICROALGA; OXYTETRACYCLINES (OTC);

ANTIBIOTICS;

CHLORAMPHENICOL; CHLOROPHYLL A; ESTERASE; FLORFENICOL; OXYTETRACYCLINE; ANTIINFECTIVE AGENT; CHLOROPHYLL; THIAMPHENICOL; WATER POLLUTANT;

ANTIBIOTICS; AQUACULTURE; CELL ORGANELLE; GROWTH; INHIBITION; MICROALGA; PHOTOSYNTHESIS; TOXICITY;

ALGAL GROWTH; ANTIBIOTIC SENSITIVITY; AQUACULTURE; ARTICLE; AUTOFLUORESCENCE; CELL ACTIVITY; CELL SIZE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; EXPOSURE; GROWTH INHIBITION; GROWTH RATE; IC50; MICROALGA; MITOSIS INHIBITION; NONHUMAN; TETRASELMIS SUECICA; ANALOGS AND DERIVATIVES; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROCEDURES; TOXICITY; TOXICITY TESTING; WATER POLLUTANT;

TETRASELMIS SUECICA;

ANTI-BACTERIAL AGENTS; AQUACULTURE; CELL PROLIFERATION; CELL SURVIVAL; CHLORAMPHENICOL; CHLOROPHYLL; MICROALGAE; OXYTETRACYCLINE; THIAMPHENICOL; TOXICITY TESTS; WATER POLLUTANTS, CHEMICAL;

EID: 84924712739     PISSN: 01411136     EISSN: 18790291     Source Type: Journal    
DOI: 10.1016/j.marenvres.2014.07.011     Document Type: Article

References (66)

1. Aminov, R.I., 2010. A brief history of the antibiotic era: lessons learned and challenges for the future. Front. Microbiol. 1, 134.
2. Blaise, C., Ménard, L., 1998. A micro-algal solid phase test to assess the toxic potential of freshwater sediments. Water Qual. Res. J. Can. 33, 133-151.
3. Blanco, M.M., Liébana, P., Gibello, A., Alcalá, C., Fernández-Garayzábal, J.F., Domínguez, L., 2004. Principales patologías bacterianas en la piscicultura española. REDVET e Revista Electrónica de Veterinaria. Available on: http://www.veterinaria.org/revistas/redvet/n020204.html. Viewed: 4 September 2013.
4. Burka, J.F., Hammell, K.L., Horsberg, T.E., Johnson, G.R., Rainnie, D.J., Speare, D.J., 1997. Drugs in salmonid aquaculture e a review. J. Vet. Pharmacol. Ther. 20, 333-349.
5. Cabello, F.C., 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8 (7), 1137-1144.
6. Campanella, L., Cubadda, F., Sammartino, M., Saoncella, A., 2001. An algal biosensor for the monitoring of water toxicity in estuarine environments. Water Res. 35 (1), 69-76.
7. Carballeira, C., Ramos-Gómez, J., Martín-Díaz, M.L., DelValls, T.A., Carballeira, A., 2012. Designing an integrated environmental monitoring plan for land-based marine fish farms located at exposed and hard bottom coastal areas. J. Environ. Monit. 14, 1305-1316.
8. Chalifour, A., Spear, P.A., Boily, M.H., DeBlois, C., Giroux, I., Dassylva, N., Juneau, P., 2009. Assessment of toxic effects of pesticide extracts on different green algal species by using chlorophyll a fluorescence. Toxicol. Environ. Chem. 91, 1315-1329.
9. Chopra, I., Roberts, M., 2001. Tetracycline antibiotics: mode of actions, applications, molecular biology and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65 (2), 232-260.
10. Cid, A., Fidalgo, P., Herrero, C., Abalde, J., 1996b. Toxic action of copper on the membrane system of a marine diatom measured by flow cytometry. Cytometry 25 (1), 32-36.
11. Cid, A., Herrero, C., Abalde, J., 1996a. Functional analysis of phytoplankton by flow cytometry: a study of the effect of copper on a marine diatom. Sci. Mar. 60 (1), 303-308.
12. Cid, A., Herrero, C., Torres, E., Abalde, J., 1995. Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters. Aquat. Toxicol. 31, 165-174.
13. Couderchet, M., Vernet, G., 2003. Pigments as biomarkers of exposure to the vineyard herbicide flazasulfuron in freshwater algae. Ecotoxicol. Environ. Saf. 55, 271-277.
14. De Orte, M.R., Carballeira, C., Viana, I.G., Carballeira, A., 2013. Assessing the toxicity of chemical compounds associated with marine land-based fish farms: the use of mini-scale microalgal toxicity test. Chem. Ecol. 29 (6), 554-563.
15. De Lorenzo, M.E., Fleming, J., 2008. Individual and mixture effects of selected pharmaceuticals and personal care products on the marine phytoplankton species Dunaliella tertiolecta. Arch. Environ. Contam. Toxicol. 54 (2), 203-210.
16. Ebringer, L., 1972. Are plastids derived from prokaryotic microorganisms? Action of antibiotics on chloroplasts of Euglena gracilis. J. Gen. Microbiol. 71 (1), 35-52.
17. Fábregas, J., Otero, A., Domínguez, A., Patiño, M., 2001. Growth rate of the microalga Tetraselmis suecica changes the biochemical composition of Artemia species. J. Mar. Biotechnol. 3, 256-263.
18. Fábregas, J., 1982. Las microalgas como eslabón de infraestructura en la Microbiología Marina: aislamiento, caracterización, ciclo celular y aprovechamiento tecnológico. Universidad de Santiago de Compostela (Tesis Doctoral).
19. Ferreira, C.S.G., Nunes, B.A., Henriques-Almeida, J.M.M., Guilhermino, L., 2007. Acute toxicity of oxytetracycline and florphenicol to the microalgae Tetraselmis chuii and to the crustacean Artemia parthenogenetica. Ecotoxicol. Environ. Saf. 67, 452-458.
20. Franklin, N.M., Stauber, J.L., Lim, R.P., 2001. Development of flow cytometry-based algal bioassays for assessing toxicity of copper in natural waters. Environ. Toxicol. Chem. 13, 160-170.
21. Franqueira, D., Cid, A., Torres, E., Orosa, M., Herrero, C., 1999. A comparison of the relative sensitivity of structural and functional cellular responses in the alga Chlamydomonas eugametos exposed to the herbicide paraquat. Arch. Environ. Contam. Toxicol. 36, 264-269.
22. Geoffroy, L., Gilbin, R., Simon, O., Floriani, M., Adam, C., Pradines, C., Cournac, L., Garnier-Laplace, J., 2007. Effect of selenate on growth and photosynthesis of Chlamydomonas reinhardtii. Aquat. Toxicol. 83 (2), 149-158.
23. González-Barreiro, O., Rioboo, C., Cid, A., Herrero, C., 2004. Atrazine induced chlorosis in Synechococcus elongatus cells. Arch. Environ. Contam. Toxicol. 46, 301-307.
24. González-Pleiter, M., Gonzalo, S., Rodea-Palomares, I., Leganés, F., Rosal, R., Boltes, K., Marco, E., Fernández-Piñas, F., 2013. Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: Implications for environmental risk assessment. Water Res. 47, 2050-2064.
25. Gray, M.W., 1992. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141, 233-357.
26. Gulkowska, A., He, Y., So, M.K., Yeung, L.W.Y., Leung, H.W., Giesy, J.P., Lam, P.K.S., Martin, M., Richardson, B.J., 2007. The occurrence of selected antibiotics in Hong Kong coastal waters. Mar. Pollut. Bull. 54 (8), 1287-1293.
27. Hadjoudja, S., Vignoles, C., Delucht, V., Lenain, J.F., Le Jeune, A.H., Baudu, M., 2009. Short term copper toxicity on Microcystis aeruginosa and Chlorela vulgaris using flow cytometry. Aquat. Toxicol. 94, 255-264.
28. Halling-Sørensen, B., 2000. Algal toxicity of antibacterial agents used in intensive farming. Chemosphere 40, 731-739.
29. Halling-Sørensen, B., Nielsen, S.N., Lanzky, P.F., Ingerslev, F., Lüzhøft, H.C.H., Jørgensen, S.E., 1998. Occurrence, fate and effects of pharmaceutical substance in the environment e a review. Chemosphere 36, 357-393.
30. Hendry, G.A.F., Price, A.H., 1993. Stress indicators: chlorophylls and carotenoids. In: Hendry, G.A.F., y Grime, J.P. (Eds.), Methods in Comparative Plant Ecology. Chapman & Hall, London, pp. 148-152.
31. Hernando, M.D., Mezcua, M., Fernández-Alba, A.R., Barceló, D., 2006. Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69 (2), 334-342.
32. Herrero, C., Cid, A., Fábregas, J., Abalde, J., 1991. Yields in biomass and chemical constituent of four commercially important marine microalgae with different culture media. Aquacult. Eng. 10 (2), 99-110.
33. Huang, Z.Y., Sun, M.Y., Li, S., Huang, G.L., 2006. Pharmacokinetics of chloramphenicol in carp (Cyprinus carpio L.) after drug administration. Aquacult. Res. 37, 1540-1545.
34. Isidori, M., Lavorgna, M., Nardelli, A., Pascarella, L., Parrella, A., 2005. Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci. Total Environ. 346, 87-98.
35. Jeffrey, S.W., Humphrey, G.F., 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191-194.
36. Jochem, F.J., 2000. Probing the physiological state of phytoplankton at the singlecell level. Sci. Mar. 64 (2), 183-195.
37. Kümmerer, K., 2009. Antibiotics in the aquatic environmente a review e Part I. Chemosphere 75, 417-434.
38. Lage, O.M., Sansonetty, F., O'Connor, J.-E., Parente, A.M., 2001. Flow cytometric analysis of chronic and acute toxicity of copper (II) on the marine dinoflagellate Amphidinium carterae. Cytometry 44, 226-235.
39. Lai, H.T., Hou, J.H., Su, C.I., Chen, C.L., 2009. Effects of chloramphenicol, florphenicol, and thiamphenicolon growth of algae Chlorella pyrenoidosa, Isochrysis galbana and Tetraselmis chuii. Ecotoxicol. Environ. Saf. 72, 329-334.
40. Liu, W., Ming, Y., Huang, Z., Li, P., 2012. Impacts of florphenicol on marine diatom Skeletonema costatum through photosynthesis inhibition and oxidative damages. Plant Physiol. Biochem. 60, 165-170.
41. Marconi, R., Lodmell, J., Hill, W., 1990. Identification of a rRNA/Chloramphenicol interaction site within then peptidyltransferase center of the 50S subunit of the Escherichia coli ribosome. J. Biol. Chem. 265 (14), 7894-7899.
42. Mayfield, S.P., Yohn, C.B., Cohen, A., Danon, A., 1995. Regulation of chloroplast gene expression. Annu. Rev. Plant. Biol. 46, 147-166.
43. McCormick, P.V., Cairns, J.J., 1994. Algae as indicators of environmental change. J. Appl. Phycol. 6, 509-526.
44. McFadden, G.I., Roos, D.S., 1999. Apicomplexan plastids as drug targets. Trends Microbiol. 7 (8), 328-333.
45. McKee, E.E., Ferguson, M., Bentley, A.T., Marks, T.A., 2006. Inhibition of mammalian mitocondrial protein synthesis by oxazolidinones. Antimicrob. Agents Chemother. 50 (6), 2042-2049.
46. Migliore, L., Civitareale, C., Brambilla, G., DiDelupis, G.D., 1997. Toxicity of several important agricultural antibiotics to Artemia. Water Res. 31 (7), 1801-1806.
47. Mullaney, P.F., Van Dilla, M.A., Coulter, J.R., 1969. Cell sizing: a light scattering photometer for rapid volume determination. Rev. Sci. Instrum. 40, 1029-1034.
48. Murthy, S.D.S., Bukhov, N.G., Mohanty, P., 1990. Mercury-induced alterations of chlorophyll a fluorescence kinetics in cyanobacteria: multiple effects of mercury on electron transport. J. Photochem. Photobiol. B 6, 373-380.
49. Nestler, H., Groh, K.J., Schönenberger, R., Behra, R., Schirmer, K., Eggen, R.I.L., Suter, M.J.-F., 2012. Multiple-endpoint assay provides a detailed mechanistic view of responses to herbicide exposure in Chlamydomonas reinhardtii. Aquat. Toxicol. 110-111, 214-224.
50. Nicolas, P., 1981. Sensivity of Euglena gracilis to chloroplast e inhibiting antibiotics, and properties of antibiotic e resistant mutants. Plant. Sci. 22, 309-317.
51. Peperzak, L., Brussaard, C.P.D., 2011. Flow cytometric applicability of fluorescent vitality probes on phytoplankton. J. Phycol. 47 (3), 692-702.
52. Prado, R., García, R., Rioboo, C., Herrero, C., Abalde, J., Cid, A., 2009a. Comparison of the sensitivity of different toxicity test endpoints in a microalga exposed to the herbicide paraquat. Environ. Int. 35, 240-247.
53. Prado, R., Rioboo, C., Herrero, C., Cid, A., 2009b. The herbicide paraquat induces alterations in the elemental and biochemical composition of non-target microalgal species. Chemosphere 76, 1440-1444.
54. Prado, R., Rioboo, C., Herrero, C., Cid, A., 2012b. Screening acute cytotoxicity biomarkers using a microalga as test organism. Ecotoxicol. Environ. Saf. 86, 219-226.
55. Prado, R., Rioboo, C., Herrero, C., Suárez-Bregua, P., Cid, A., 2012a. Flow cytometric analysis to evaluate physiological alterations in herbicide-exposed Chlamydomonas moewusii cells. Ecotoxicology 21, 409-420.
56. Rioboo, C., González, O., Herrero, C., Cid, A., 2002. Physiological response of freshwater microalga (Chlorella vulgaris) to triazine and phenylurea herbicides. Aquat. Toxicol. 59, 225-235.
57. Rioboo, C., Prado, R., Herrero, C., Cid, A., 2007. Population growth study of the rotifer Brachionus sp. fed with triazine-exposed microalgae. Aquat. Toxicol. 83, 247-253.
58. Samson, G., Papovic, R., 1988. Use of algal fluorescence for determination of phytotoxicity of heavy metals and pesticides as environmental pollutants. Ecotoxicol. Environ. Saf. 16, 272-278.
59. 2 evolution in Anacystis nidulans. Plant Physiol. 83, 12-14.
60. Tsiaka, P., Tsarpali, V., Ntaikou, I., Kostopoulou, M.N., Lyberatos, G., Dailianis, S., 2013. Carbamazepine-mediated pro-oxidant effects on the unicelular marine algal species Dunaliella tertiolecta and the hemocytes of mussel Mytilus galloprovincialis. Ecotoxicology 22, 1208-1220.
61. Uriarte, I., Farias, A., Castilla, J.C., 2001. Effect of antibiotic treatment during larval development of the Chilean scallop Argopecten purpuratus. Aquacult. Eng. 25, 139-147.
62. Wollenberger, L., Halling-Sørensen, B., Kusk, K.O., 2000. Acute and chronic toxicity of veterinary antibiotics to Daphnia Magna. Chemosphere 40, 723-730.
63. Xu, L.W., Liao, C.R., Liu, G.F., 2005. Security about florphenicol used in aquaculture. J. Fish. Sci. China 12, 512-518.
64. Xu, W., Zhang, G., Zou, S., Li, X., Liu, Y., 2007. Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using high-performance liquid chromatography-electrospray ionization tandem mass spectrometry. Environ. Pollut. 145 (3), 672-679.
65. Yunis, A.A., 1989. Chloramphenicol toxicity: 25 years of research. Am. J. Med. 87, 44-48.
66. Zhang, W., Zhang, M., Lin, K., Sun, W., Xiong, B., Guo, M., Cui, X., Fu, R., 2012. Ecotoxicological effect of carbamazepine on Scenedesmus obliquus and Chlorella pyrenoidosa. Environ. Toxicol. Pharmacol. 33 (2), 344-352.