Sulphate, more than a nutrient, protects the microalga Chlamydomonas moewusii from cadmium toxicity

Aquatic Toxicology

Volumn 148, Issue , 2014, Pages 92-103

  Mera, Roi ^a   Torres, Enrique ^a   Abalde, Julio ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

Cadmium; Chlamydomonas moewusii; Low molecular mass thiol compounds; Sulphate; Tolerance; Toxicity

Indexed keywords

CADMIUM; PHYTOCHELATIN; SULFATE;

CADMIUM; CONCENTRATION (COMPOSITION); GROWTH RATE; GROWTH RESPONSE; MICROALGA; NUMERICAL MODEL; SULFATE; TOLERANCE; TOXICITY;

ALGAL GROWTH; ARTICLE; BIOSYNTHESIS; CADMIUM POISONING; CELL CULTURE; CELL GROWTH; CELL PROTECTION; CHLAMYDOMONAS; CHLAMYDOMONAS MOEWUSII; CONCENTRATION RESPONSE; CONTROLLED STUDY; FRESHWATER SPECIES; MATHEMATICAL MODEL; MICROALGA; MOLECULAR WEIGHT; NONHUMAN; PHYSICAL TOLERANCE; PRIORITY JOURNAL; TOXICITY TESTING;

CADMIUM; CHLAMYDOMONAS MOEWUSII; LOW-MOLECULAR MASS THIOL COMPOUNDS; SULPHATE; TOLERANCE; TOXICITY;

CADMIUM; CHLAMYDOMONAS; INHIBITORY CONCENTRATION 50; MODELS, THEORETICAL; SULFATES; WATER POLLUTANTS, CHEMICAL;

EID: 84892866202     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.12.034     Document Type: Article

References (56)

1. Aguilera A., Amils R. Tolerance to cadmium in Chlamydomonas sp. (Chlorophyta) strains isolated from an extreme acidic environment, the Tinto River (SW, Spain). Aquat. Toxicol. 2005, 75:316-329.
2. Ahner B.A., Morel F.M.M. Phytochelatin production in marine algae. 2. Induction by various metals. Limnol. Oceanogr. 1995, 40:658-665.
3. Alves de Oliveira J., Cambraia J., Valle de Sousa M., Oliva M.A. Sulphate uptake and metabolism in water hyacinth and salvinia during cadmium stress. Aquat. Bot. 2009, 91:257-261.
4. Anjum N.A., Umar S., Ahmad A., Iqbal M., Khan N.A. Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regul. 2008, 54:271-279.
5. Baścik-Remisiewicz A., Aksmann A., Zak A., Kowalska M., Tukaj Z. Toxicity of cadmium, anthracene, and their mixture to Desmodesmus subspicatus estimated by algal growth-inhibition ISO standard test. Arch. Environ. Contam. Toxicol. 2011, 60:610-617.
6. Bednarz T., Warkowska-Dratnal H. Toxicity of zinc, cadmium, lead, copper, and their mixture for Chlorella pyrenoidosa. Acta Hydrobiol. 1985, 25-26:389-400.
7. Bernstein E.O. Physiology of an obligate photoautotroph (Chlamydomonas moewusii). II. The effect of light-dark cycles on cell division. Exp. Cell Res. 1966, 41:307-315.
8. Bräutigam A., Schaumloffel D., Preud'homme H., Thondorf I., Wesenberg D. Physiological characterization of cadmium-exposed Chlamydomonas reinhardtii. Plant Cell Environ. 2011, 34:2071-2082.
9. Brown T.E., Richardson F.L., Vaughn M.L. Development of red pigmentation in Chlorococcum wimmeri (Chlorophyta: Chlorococcales). Phycologia 1967, 6:167-184.
10. Brzóska M.M., Moniuszko-Jakoniuk J. Interactions between cadmium and zinc in the organism. Food Chem. Toxicol. 2001, 39:967-980.
11. Cobbett C.S., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 2002, 53:159-182.
12. Chen J., Zhou J., Goldsbrough P.B. Characterization of phytochelatin synthase from tomato. Physiol. Plant. 1997, 101:162-172.
13. Dameron C.T., Winge D.R. Characterization of peptide-coated cadmium-sulfide crystallites. Inorg. Chem. 1990, 29:1343-1348.
14. Davies T.D. Sulphate toxicity to the aquatic moss, Fontinalis antipyretica. Chemosphere 2007, 66:444-451.
15. Elphick J.R., Davies M., Gilron G., Canaria E.C., Lo B., Bailey H.C. An aquatic toxicological evaluation of sulfate: the case for considering hardness as a modifying factor in setting water quality guidelines. Environ. Toxicol. Chem. 2011, 30:247-253.
16. Folgar S., Torres E., Pérez-Rama M., Cid A., Herrero C., Abalde J. Dunaliella salina as a marine microalga highly tolerant to but a poor remover of cadmium. J. Hazard. Mater. 2009, 165:486-493.
17. García-García J.D., Olin-Sandoval V., Saavedra E., Girard L., Hernández G., Moreno-Sánchez R. Sulfate uptake in photosynthetic Euglena gracilis. Mechanisms of regulation and contribution to cysteine homeostasis. BBA-Gen. Subj. 2012, 1820:1567-1575.
18. Grill E., Winnacker E.L., Zenk M.H. Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. PNAS 1987, 84:439-443.
19. Hell R., Dahl C., Knaff D.B., Leustek T. Sulfur Metabolism in Phototrophic Organisms 2008, Springer Netherlands, The Netherlands.
20. 2: electron probe microanalysis. Biol. Cell 1986, 58:79-86.
21. Holmer M., Storkholm P. Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biol. 2001, 46:431-451.
22. Jacobson K.B., Turner J.E. The interaction of cadmium and certain other metal ions with proteins and nucleic acids. Toxicology 1980, 16:1-37.
23. Järup L. Hazards of heavy metal contamination. Br. Med. Bull. 2003, 68:167-182.
24. Källqvist T. Effect of water hardness on the toxicity of cadmium to the green alga Pseudokirchneriella subcapitata in an artificial growth medium and nutrient-spiked natural lake waters. J. Toxicol. Environ. Health Part A 2009, 72:277-283.
25. Kaplan D., Heimer Y.M., Abeliovich A., Goldsbrough P.B. Cadmium toxicity and resistance in Chlorella sp. Plant Sci. 1995, 109:129-137.
26. Lavoie M., Le Faucheur S., Fortin C., Campbell P.G. Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aquat. Toxicol. 2009, 92:65-75.
27. Lee R.W., Dumas C., Lemieux C., Turmel M. Cloning and characterization of the Chlamydomonas moewusii mitochondrial genome. Mol. Gen. Genet. 1991, 231:53-58.
28. Magdaleno A., Gomez C.E., Velez C.G., Accorinti J. Preliminary toxicity tests using the green alga, Ankistrodesmus falcatus. Environ. Toxic. Water 1997, 12:11-14.
29. Mason A.Z., Jenkins K.D. Metal detoxification in aquatic organisms. Metal Speciation and Bioavailability in Aquatic Systems 1995, 479-608. John Wiley & Sons Ltd, California. A. Tessier, D.R. Turner (Eds.).
30. Mehra R.K., Mulchandani P., Hunter T.C. Role of CdS quantum crystallites in cadmium resistance in Candida Glabrata. Biochem. Biophys. Res. Commun 1994, 200:1193-1200.
31. Mendoza-Cózatl D., Loza-Tavera H., Hernández-Navarro A., Moreno-Sánchez R. Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol. Rev. 2005, 29:653-671.
32. Mislin H., Ravera O. Cadmium in the environment 1986, Birkhäuser Verlag Basel, Basel, Switzerland.
33. Nocito F.F., Lancilli C., Crema B., Fourcoy P., Davidian J.C., Sacchi G.A. Heavy metal stress and sulfate uptake in maize roots. Plant Physiol. 2006, 141:1138-1148.
34. Nocito F.F., Pirovano L., Cocucci M., Sacchi G.A. Cadmium-induced sulfate uptake in maize roots. Plant Physiol. 2002, 129:1872-1879.
35. Noël L., Huynh-Delerme C., Guérin T., Huet H., Frémy J.-M., Kolf-Clauw M. Cadmium accumulation and interactions with zinc, copper, and manganese, analysed by ICP-MS in a long-term Caco-2 TC7 cell model. Biometals 2006, 19:473-481.
36. Okamoto O.K., Asano C.S., Aidar E., Colepicolo P. Effects of cadmium on growth and superoxide dismutase activity of the marine microalga Tetraselmis gracilis (Prasinophyceae). J. Phycol. 1996, 32:74-79.
37. Ortiz D.F., Ruscitti T., McCue K.F., Ow D.W. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 1995, 270:4721-4728.
38. Pawlik-Skowrońska B. Phytochelatin production in freshwater algae Stigeoclonium in response to heavy metals contained in mining water; effects of some environmental factors. Aquat. Toxicol. 2001, 52:241-249.
39. Pérez-Rama M., Abalde J., Herrero C., Torres E. Cadmium removal by living cells of the marine microalga Tetraselmis suecica. Bioresour. Technol. 2002, 84:265-270.
40. Pérez-Rama M., Torres E., Abalde J. Capillary zone electrophoresis for analysis of phytochelatins and other thiol peptides in complex biological samples derivatized with monobromobimane. Electrophoresis 2005, 26:610-620.
41. Pérez-Rama M., Torres E., Abalde J. Composition and production of thiol constituents induced by cadmium in the marine microalga Tetraselmis suecica. Environ. Toxicol. Chem. 2006, 25:128-136.
42. Prado R., Rioboo C., Herrero C., Cid A. Characterization of cell response in Chlamydomonas moewusii cultures exposed to the herbicide paraquat: induction of chlorosis. Aquat. Toxicol. 2011, 102:10-17.
43. Prévot P., Soyer-Gobillard M.O. Combined action of cadmium and selenium on two marine dinoflagellates in culture, Prorocentrum micans Ehrgb. and Crypthecodinium cohnii Biecheler. J. Protozool. 1986, 33:42-47.
44. Rachlin J.W., Grosso A. The growth response of the green alga Chlorella vulgaris to combined divalent cation exposure. Arch. Environ. Contam. Toxicol 1993, 24:16-20.
45. Rauser W.E. Phytochelatins. Annu. Rev. Biochem. 1990, 59:61-86.
46. Steffens J.C. The heavy metal-binding peptides of plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1990, 41:553-575.
47. Stohs S.J., Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18:321-336.
48. Suárez C., Torres E., Pérez-Rama M., Herrero C., Abalde J. Cadmium toxicity on the freshwater microalga Chlamydomonas moewusii Gerloff: biosythesis of thiol compounds. Environ. Toxicol. Chem 2010, 29:1-7.
49. Sunda G.W., Huntsman S.A. Antagonisms between cadmium and zinc toxicity and manganese limitation in a coastal diatom. Limnol. Oceanogr. 1996, 41:373-387.
50. Torres E., Cid A., Fidalgo P., Herrero C., Abalde J. Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum Bohlin. Aquat. Toxicol. 1997, 39:231-246.
51. Turbak S.C., Olson S.B., Mcfeters G.A. Comparison of algal assay systems for detecting waterborne herbicides and metals. Water Res. 1986, 20:91-96.
52. Vatamaniuk O.K., Mari S., Lang A., Chalasani S., Demkiv L.O., Rea P.A. Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with gamma-glutamylcysteine during catalysis: stoichiometric and site-directed mutagenic analysis of arabidopsis thaliana PCS1-catalyzed phytochelatin synthesis. J. Biol. Chem. 2004, 279:22449-22460.
53. WHO, 1992. Cadmium, Environmental Health Criteria 134. International Programme on Chemical Safety, Geneva.
54. Wirtz M., Droux M. Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth. Res. 2005, 86:345-362.
55. Yap C.K., Ismail A., Omar H., Tan S.G. Toxicities and tolerances of Cd, Cu, Pb and Zn in a primary producer (Isochrysis galbana) and in a primary consumer (Perna viridis). Environ. Int. 2004, 29:1097-1104.
56. Zenk M.H. Heavy metal detoxification in higher plants-a review. Gene 1996, 179:21-30.