Microsporidia parasites disrupt the responses to cadmium exposure in a gammarid

Environmental Pollution

Volumn 160, Issue 1, 2012, Pages 17-23

  Gismondi, Eric ^a   Rigaud, Thierry ^b   Beisel, Jean Nicolas ^a   Cossu Leguille, Carole ^a  

^a Nancy University   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Biomarkers; Cadmium stress; Confounding factor; Gammarus roeseli; Microsporidian parasites

Indexed keywords

ANTIOXIDANT DEFENCE; CADMIUM EXPOSURE; CADMIUM STRESS; CELLULAR DAMAGE; CONFOUNDING FACTOR; ECO-TOXICOLOGY; ECOTOXICOLOGICAL STUDY; ENERGY RESERVES; GAMMARUS; MALONDIALDEHYDE; MICROSPORIDIA; MICROSPORIDIAN PARASITES; PHYSIOLOGICAL CONDITION;

ALDEHYDES; CADMIUM; DAMAGE DETECTION;

PROTOZOA;

CADMIUM; GLUTATHIONE; GLYCOGEN; MALONALDEHYDE;

AMPHIPOD; BIOMARKER; CADMIUM; ECOTOXICOLOGY; PARASITE; PARASITIC DISEASE; POLLUTION EXPOSURE;

ARTICLE; CELL DAMAGE; CELL STRESS; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ECOTOXICOLOGY; ENERGY RESOURCE; ENVIRONMENTAL EXPOSURE; FEMALE; GAMMARUS; GAMMARUS ROESELI; HOST PARASITE INTERACTION; HOST RESISTANCE; MALE; MICROSPORIDIA; MICROSPORIDIOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; SEASONAL VARIATION; SENSITIVITY ANALYSIS; SEX DIFFERENCE; WATER POLLUTION;

AMPHIPODA; ANIMALS; CADMIUM; ENERGY METABOLISM; FEMALE; HOST-PARASITE INTERACTIONS; MALE; MALONDIALDEHYDE; MICROSPORIDIA; PARASITES; SPECIES SPECIFICITY;

AMPHIPODA; DICTYOCOELA MUELLERI; DICTYOCOELA SP. L11; GAMMARIDAE; GAMMARUS ROESELI; MICROSPORIDIA;

EID: 80053901879     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2011.09.021     Document Type: Article

References (69)

1. N. Akira, M.E. Anderson, and A. Meister Cellular glutathione as a determinant of sensitivity to mercuric chloride toxicity: prevention of toxicity by giving glutathione monoester Biochemical Pharmacology 40 1990 693 697 (Pubitemid 20246572)
2. J. Alhama, A. Romero-Ruiz, and J. Lopez-Barea Metallothionein quantification in clams by reversed-phase high-performance liquid chromatography coupled to fluorescence detection after monobromobimane derivatization Journal of Chromatography A 1107 2006 52 58 (Pubitemid 43184206)
3. C. Bandi, A.M. Dunn, G.D.D. Hurst, and T. Rigaud Inherited microorganisms, sex-specific virulence and reproductive parasitism Trends in Parasitology 17 2001 88 94 (Pubitemid 32416555)
4. C. Barata, I. Varo, J.C. Navarro, S. Arun, and C. Porte Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 140 2005 175 186 (Pubitemid 40720038)
5. I. Barber, H.A. Wright, S.A. Arnott, and R.J. Wootton Growth and energetics in the stickleback Schistocephalus host-parasite system: a review of experimental infection studies Behaviour 145 2008 647 668 (Pubitemid 351445640)
6. W. Behrens, and R. Madre Malonaldehyde determination in tissues and biological fluids by ion-pairing high-performance liquid chromatography Lipids 26 1991 232 236
7. C. Biderre, F. Babin, and C.P. Vivars Fatty acid composition of four Microsporidian species compared to that of their host fishes Journal of Eukaryotic Microbiology 47 2000 7 10 (Pubitemid 30063283)
8. A. Bigot, L. Minguez, L. Giambérini, and F. Rodius Early defense responses in the freshwater bivalve Corbicula fluminea exposed to copper and cadmium: transcriptional and histochemical studies Environmental Toxicology 2010 10.1002/tox.20599
9. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Analytical Biochemistry 72 1976 248 254
10. M.P. Cajaraville, M.J. Bebianno, J. Blasco, C. Porte, C. Sarasquete, and A. Viarengo The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach The Science of the Total Environment 247 2000 295 311 (Pubitemid 30145681)
11. A.S. Cargill, K.W. Cummins, B.J. Hanson, and R.R. Lowry The role of lipids as feeding stimulants for shredding aquatic insects Freshwater Biology 15 1985 455 464 (Pubitemid 16279615)
12. A.D. Correia, D.R. Livingstone, and M.H. Costa Effects of water-borne copper on metallothionein and lipid peroxidation in the marine amphipod Gammarus locusta Marine Environmental Research 54 2002 357 360 (Pubitemid 35286449)
13. S. Dietrich, S. Dammel, F. Ploessl, F. Bracher, and C. Laforsch Effects of a pharmaceutical mixture at environmentally relevant concentrations on the amphipod Gammarus fossarum Marine and Freshwater Research 61 2010 196 203
14. A.M. Dunn, M.J. Hatcher, R.S. Terry, and C. Tofts Evolutionary ecology of vertically transmitted parasites: transovarial transmission of a microsporidian sex ratio distorter in Gammarus duebeni Parasitology 111 Suppl. S1 1995 S91 S109 (Pubitemid 26173656)
15. A.M. Dunn, and J.E. Smith Microsporidian life cycles and diversity: the relationship between virulence and transmission Microbes and Infection 3 2001 381 388 (Pubitemid 32441661)
16. B.K. Dutra, F. Fernandes, A. Lauffer, and G. Oliveira Carbofuran-induced alterations in the energy metabolism and reproductive behaviors of Hyalella castroi (Crustacea, Amphipoda) Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 149 2009 640 646
17. D. Ebert, and E.A. Herre The evolution of parasitic diseases Parasitology Today 12 1996 96 101 (Pubitemid 26069995)
18. A.T. Ford, T.F. Fernandes, C.D. Robinson, I.M. Davies, and P.A. Read Can industrial pollution cause intersexuality in the amphipod, Echinogammarus marinus? Marine Pollution Bulletin 53 2006 100 106
19. D.M. Forrow, and L. Maltby Toward a mechanistic understanding of contaminant-induced changes in detritus processing in streams: direct and indirect effects on detritivore feeding Environmental Toxicology and Chemistry 19 2000 2100 2106 (Pubitemid 30599912)
20. A. Geffard, H. Quéau, O. Dedourge, S. Biagianti-Risboug, and O. Geffard Influence of biotic and abiotic factors on metallothionein level in Gammarus pulex Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 145 2007 632 640 (Pubitemid 46671530)
21. E. Guerlet, K. Ledy, and L. Giambérini Is the freshwater gammarid, Dikerogammarus villosus, a suitable sentinel species for the implementation of histochemical biomarkers? Chemosphere 72 2008 697 702
22. E.R. Haine, E. Brondani, K.D. Hume, M. Perrot-Minnot, M. Gaillard, and T. Rigaud Coexistence of three microsporidia parasites in populations of the freshwater amphipod Gammarus roeseli: evidence for vertical transmission and positive effect on reproduction International Journal for Parasitology 34 2004 1137 1146 (Pubitemid 39222047)
23. E.R. Haine, S. Motreuil, and T. Rigaud Infection by a vertically-transmitted microsporidian parasite is associated with a female-biased sex ratio and survival advantage in the amphipod Gammarus roeseli Parasitology 134 2007 1363 1367 (Pubitemid 47236800)
24. T. Jacobson, K. Holmström, G. Yang, A.T. Ford, U. Berger, and B. Sundelin Perfluorooctane sulfonate accumulation and parasite infestation in a field population of the amphipod Monoporeia affinis after microcosm exposure Aquatic Toxicology 98 2010 99 106
25. T. Jacobson, B. Sundelin, G. Yang, and A.T. Ford Low dose TBT exposure decreases amphipod immunocompetence and reproductive fitness Aquatic Toxicology 101 2011 72 77
26. P.J. Keeling, and N.M. Fast Microsporidia: biology and evolution of highly reduced intracellular parasites Annual Review of Microbiology 56 2002 93 116 (Pubitemid 35217449)
27. A. Kelly, A.M. Dunn, and M.J. Hatcher Population dynamics of a vertically transmitted, parasitic sex ratio distorter and its amphipod host Oikos 94 2001 392 402 (Pubitemid 32913905)
28. A. Kelly, M.J. Hatcher, and A.M. Dunn The impact of a vertically transmitted microsporidian, Nosema granulosis on the fitness of its Gammarus duebeni host under stressful environmental conditions Parasitology 126 2003 119 124 (Pubitemid 36308247)
29. F.R. Khan, N.R. Bury, and C. Hogstrand Cadmium bound to metal rich granules and exoskeleton from Gammarus pulex causes increased gut lipid peroxidation in zebrafish following single dietary exposure Aquatic Toxicology 96 2010 124 129
30. A. Lange, O. Ausseil, and H. Segner Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 131 2002 231 243 (Pubitemid 34241527)
31. W.Y. Lee, S.A. Macko, and J.A.C. Nicol Changes in nesting behavior and lipid content of a marine amphipod (Amphithoe valida) to the toxicity of a no. 2 fuel oil Water, Air, and Soil Pollution 15 1981 185 195 (Pubitemid 11104113)
32. Y.Y. Lee, S.J. Kim, E.H. Park, and C.J. Lim Glutathione content and the activities of glutathione-synthesizing enzymes in fission yeast are modulated by oxidative stress Journal of Microbiology 41 2003 248 251
33. P. Leroy, A. Nicolas, M. Wellmann, F. Michelet, T. Oster, and G. Siest Evaluation of o-phthalaldehyde as bifunctional fluorogenic post-column reagent for glutathione in LC Chromatographia 36 1993 130 134 (Pubitemid 23102641)
34. A. Mathis Microsporidia: emerging advances in understanding the basic biology of these unique organisms International Journal for Parasitology 30 2000 795 804 (Pubitemid 30421125)
35. S. Mautner, K.A. Cool, M.R. Forbes, D.G. McCurdy, and A.M. Dunn Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod Parasitology 134 2007 1567 1573 (Pubitemid 350194882)
36. C.P. McCahon, S.J. Maund, and M.J. Poulton The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex) Freshwater Biology 25 1991 507 513
37. A. Meister Selective modification of glutathione metabolism Science 220 1983 472 477 (Pubitemid 13114104)
38. G. Méténier, and C.P. Vivars Molecular characteristics and physiology of microsporidia Microbes and Infection 3 2001 407 415 (Pubitemid 32441664)
39. L. Minguez, A. Meyer, D.P. Molloy, and L. Giambérini Interactions between parasitism and biological responses in zebra mussels (Dreissena polymorpha): importance in ecotoxicological studies Environmental Research 109 2009 843 850
40. C. Parmentier, P. Leroy, M. Wellman, and A. Nicolas Determination of cellular thiols and glutathione-related enzyme activities: versatility of high-performance liquid chromatography-spectrofluorimetric detection Journal of Chromatography B: Biomedical Sciences and Applications 719 1998 37 46
41. D. Pascoe, T.J. Kedwards, S.J. Blockwell, and E.J. Taylor Gammarus pulex (L.) feeding bioassay - Effects of parasitism Bulletin of Environmental Contamination and Toxicology 55 1995 629 632
42. S.J. Plaistow, J.P. Troussard, and F. Cézilly The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex International Journal for Parasitology 31 2001 346 351 (Pubitemid 32295901)
43. J. Prenter, C. MacNeil, J.T.A. Dick, G.E. Riddell, and A.M. Dunn Lethal and sublethal toxicity of ammonia to native, invasive, and parasitised freshwater amphipods Water Research 38 2004 2847 2850 (Pubitemid 38829575)
44. S. Ray, N.L.A. Misso, J.C. Lenzo, C. Robinson, and P.J. Thompson Gamma-glutamylcysteine synthetase activity in human lung epithelial (A549) cells: factors influencing its measurement Free Radical Biology and Medicine 27 1999 1346 1356 (Pubitemid 30001497)
45. T.P. Rodgers-Gray, J.E. Smith, A.E. Ashcroft, R.E. Isaac, and A.M. Dunn Mechanisms of parasite-induced sex reversal in Gammarus duebeni International Journal for Parasitology 34 2004 747 753 (Pubitemid 38521229)
46. G. Roesijadi Metallothioneins in metal regulation and toxicity in aquatic animals Aquatic Toxicology 22 1992 81 113
47. D. Schlenk, and C.D. Rice Effect of zinc and cadmium treatment on hydrogen peroxide-induced mortality and expression of glutathione and metallothionein in a teleost hepatoma cell line Aquatic Toxicology 43 1998 121 129 (Pubitemid 28544993)
48. R. Siddall, and B. Sures Uptake of lead by Pomphorhynchus laevis cystacanths in Gammarus pulex and immature worms in chub (Leuciscus cephalus) Parasitology Research 84 1998 573 577 (Pubitemid 28323242)
49. R. Singhal, M. Anderson, and A. Meister Glutathione, a first line of defense against cadmium toxicity The FASEB Journal 1 1987 220 223 (Pubitemid 18032626)
50. J.E. Smith The ecology and evolution of microsporidian parasites Parasitology 136 Special Issue 14 2009 1901 1914
51. M. Soussi, K. Ouali, M.W. Hadj, R. Rouachdia, A. Djabouradi, and M. Bensouilah Proportioning of biomarkers (GSH, GST, AchE, catalase) indicator of pollution at Gambusia affinis (Teleostei fish) exposed to cadmium Environmental Research Journal 2 2008 177 181
52. T.C. Sparkes, D.P. Keogh, and R.A. Pary Energetic costs of mate guarding behavior in male stream-dwelling isopods Oecologia 106 1996 166 171
53. S. Sroda, and C. Cossu-Leguille Effects of sublethal copper exposure on two gammarid species: which is the best competitor? Ecotoxicology 20 2011 264 273
54. A. Stuhlbacher, and L. Maltby Cadmium resistance in Gammarus pulex (L.) Archives of Environmental Contamination and Toxicology 22 1992 319 324
55. B. Sures, and H. Taraschewski Cadmium concentrations in two adult acanthocephalans, Pomphorhynchus laevis and Acanthocephalus lucii, as compared with their fish hosts and cadmium and lead levels in larvae of A. lucii as compared with their crustacean host Parasitology Research 81 1995 494 497
56. B. Sures, R. Siddall, and H. Taraschewski Parasites as accumulation indicators of heavy metal pollution Parasitology Today 15 1999 16 21 (Pubitemid 29246040)
57. B. Sures, G. Scheef, B. Klar, W. Kloas, and H. Taraschewski Interaction between cadmium exposure and infection with the intestinal parasite Moniliformis moniliformis (Acanthocephala) on the stress hormone levels in rats Environmental Pollution 119 2002 333 340 (Pubitemid 34327227)
58. B. Sures Environmental parasitology: relevancy of parasites in monitoring environmental pollution Trends in Parasitology 20 2004 170 177 (Pubitemid 38526131)
59. B. Sures, F. Thielen, F. Baska, J. Messerschmidt, and A. von Bohlen The intestinal parasite Pomphorhynchus laevis as a sensitive accumulation indicator for the platinum group metals Pt, Pd, and Rh Environmental Research 98 2005 83 88 (Pubitemid 40254947)
60. B. Sures, and H. Radszuweit Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala) Journal of Helminthology 81 2007 191 197 (Pubitemid 46956872)
61. R.S. Terry, J.E. Smith, and A.M. Dunn Impact of a novel, feminising microsporidium on its crustacean host Journal of Eukaryotic Microbiology 45 1998 497 501 (Pubitemid 28490161)
62. R.S. Terry, J.E. Smith, R.G. Sharpe, T. Rigaud, D.T.J. Littlewood, J.E. Ironside, D. Rollinson, D. Bouchon, C. MacNeil, J.T.A. Dick, and A.M. Dunn Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora Proceedings of the Royal Society of London. Series B: Biological Sciences 271 2004 1783 1789
63. P. Thomas, and H.W. Wofford Effects of cadmium and Aroclor 1254 on lipid peroxidation, glutathione peroxidase activity, and selected antioxidants in Atlantic croaker tissues Aquatic Toxicology 27 1993 159 177
64. M.A. Timofeyev, Z.M. Shatilina, A.V. Kolesnichenko, D.S. Bedulina, V.V. Kolesnichenko, S. Pflugmacher, and C.E. Steinberg Natural organic matter (NOM) induces oxidative stress in freshwater amphipods Gammarus lacustris Sars and Gammarus tigrinus (Sexton) Science of the Total Environment 366 2006 673 681 (Pubitemid 44063546)
65. 2 Ecotoxicology and Environmental Safety 70 2008 99 105 (Pubitemid 351410524)
66. P. Vasseur, and C. Leguille Defense systems of benthic invertebrates in response to environmental stressors Environmental Toxicology 19 2004 433 436 (Pubitemid 39199209)
67. C.P. Vivars, B.J. Martin, and H.J. Ceccaldi Acides gras de trois microsporidies (Protozoa) et de leur hôte Carcinus mediterraneus (Crustacea), sain et parasité par Thelohania maenadis Parasitology Research 61 1980 99 107 (Pubitemid 10136006)
68. C.P. Vivars, and J.L. Cuq Physiological and metabolic variations in Carcinus mediterraneus (Crustacea: Decapoda) parasitized by Thelohania maenadis (Microspora: Microsporida): an ecophysiopathological approach Journal of Invertebrate Pathology 37 1981 38 46
69. M. Wittner, and L.M. Weiss The Microsporidia and Microsporidiosis 1999 American Society for Microbiology Washington DC, USA 553 pp