Ameliorating effects of extracellular polymeric substances excreted by Thalassiosira pseudonana on algal toxicity of CdSe quantum dots

Aquatic Toxicology

Volumn 126, Issue , 2013, Pages 214-223

  Zhang, Saijin ^a   Jiang, Yuelu ^a   Chen, Chi Shuo ^b   Creeley, Danielle ^a   Schwehr, Kathleen A ^a   Quigg, Antonietta ^a,c   Chin, Wei Chun ^b   Santschi, Peter H ^a,c  

^a TEXAS A AND M UNIVERSITY AT GALVESTON   (United States)

^b Merced   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

CdSe ZnS quantum dots; Extracellular polymeric substances; Thalassiosira pseudonana; Toxicity

Indexed keywords

CADMIUM; CADMIUM SELENIDE; POLYMER; POLYSACCHARIDE; QUANTUM DOT; ZINC SULFIDE;

ALGA; CADMIUM; DETOXIFICATION; NUTRIENT; PARTITIONING; PHYTOPLANKTON; POLYMER; POLYSACCHARIDE; PROTEIN; SELENIUM; TOXICITY; ZINC;

ALGAL TOXICITY; AQUATIC ENVIRONMENT; ARTICLE; BIOMASS PARTITIONING; CONFOCAL LASER MICROSCOPY; CULTURE MEDIUM; ENRICHMENT CULTURE; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; THALASSIOSIRA PSEUDONANA; TOXICITY; TOXICITY TESTING;

DIATOMS; MICROSCOPY, CONFOCAL; QUANTUM DOTS; WATER POLLUTANTS, CHEMICAL;

ALGAE; NITZSCHIA ALBA; THALASSIOSIRA PSEUDONANA;

EID: 84870672056     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.11.012     Document Type: Article

References (80)

1. Ahner B.A., Morel F.M.M. Phytochelatin production in marine algae: 2. Induction by various metals. Limnology and Oceanography 1995, 40:658-665.
2. Ahner B.A., Price N.M., Morel F.M. Phytochelatin production by marine phytoplankton at low free metal ion concentrations: laboratory studies and field data from Massachusetts Bay. Proceedings of the National Academy of Sciences USA 1994, 91:8433-8436.
3. Becker W. Microalgae for Aquaculture: The Nutritional Value of Microalgae for Aquaculture Handbook of Microalgal Culture 2007, Blackwell Publishing Ltd., Oxford, pp. 380-391.
4. Ben-Amotz A., Avron M. The wavelength dependence of massive carotene synthesis in Dunaliella bardawil (Chlorophyceae). Journal of Phycology 1989, 25:175-178.
5. Berges J.A., Charlebois D.O., Mauzerall D.C., Falkowski P.G. Differential effects of nitrogen limitation on photosynthetic efficiency of Photosystems I and II in microalgae. Plant Physiology 1996, 110:689-696.
6. Biswal B., Smith A.J., Rogers L.J. Changes in carotenoids but not in D1 protein in response to nitrogen depletion and recovery in a cyanobacterium. FEMS Microbiology Letters 1994, 116:341-347.
7. Boxall A.B.A., Chaudhry Q., Sinclair C., Jones A., Aitken R., Jefferson B., Watts C. Current and Future Predicted Environmental Exposure to Engineered Nanoparticles 2007, Central Science Laboratory, Department of the Environment and Rural Affairs, London, UK, p. 89.
8. Brennan R.J., Schiestl R.H. Cadmium is an inducer of oxidative stress in yeast. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 1996, 356:171-178.
9. Bruchez M., Moronne M., Gin P., Weiss S., Alivisatos A.P. Semiconductor nanocrystals as fluorescent biological labels. Science 1998, 281:2013-2016.
10. 2, nitrate, phosphate, and silicate limitation on intracellular dimethylsulfoniopropionate in batch cultures of the coastal diatom Thalassiosira pseudonana. Limnology and Oceanography 2003, 48:2256-2265.
11. Chen C.S., Anaya J.M., Zhang S.J., Spurgin J., Chuang C.Y., Xu C., Miao A.J., Chen E.Y.T., Schwehr K.A., Jiang Y.L., Quigg A., Santschi P.H., Chin W.C. Effects of engineered nanoparticles on the assembly of exopolymeric substances from phytoplankton. Plos One 2011, 6:e21865.
12. Cho S.J., Maysinger D., Jain M., Röder B., Hackbarth S., Winnik F.M. Long-term exposure to CdTe quantum dots causes functional impairments in live cells. Langmuir 2007, 23:1974-1980.
13. Coe-Sullivan S. Quantum dot developments. Nature Photonics 2009, 3:315-316.
14. Dabbousi B.O., RodriguezViejo J., Mikulec F.V., Heine J.R., Mattoussi H., Ober R., Jensen K.F., Bawendi M.G. (CdSe)ZnS core-shell quantum dots: synthesis and characterization of a size series of highly luminescent nanocrystallites. Journal of Physical Chemistry B 1997, 101:9463-9475.
15. Derfus A.M., Chan W.C.W., Bhatia S.N. Probing the cytotoxicity of semiconductor quantum dots. Nano Letters 2004, 4:11-18.
16. Ding Y.X., Chin W.C., Rodriguez A., Hung C.C., Santschi P.H., Verdugo P. Amphiphilic exopolymers from Sagittula stellata induce DOM self-assembly and formation of marine microgels. Marine Chemistry 2008, 112:11-19.
17. Espinosa E.P., Perrigault M., Ward J.E., Shumway S.E., Allam B. Microalgal cell surface carbohydrates as recognition sites for particle sorting in suspension-feeding bivalves. Biological Bulletin 2010, 218:75-86.
18. Falkowski P.G., Raven J.A. Aquatic Photosynthesis 2007, Princeton University Press, Princeton.
19. Flemming H.C., Wingender J. The biofilm matrix. Nature Reviews Microbiology 2010, 8:623-633.
20. Galán A., García-Bermejo L., Troyano A., Vilaboa N.E., Fernández C., de Blas E., Aller P. The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays). European Journal of Cell Biology 2001, 80:312-320.
21. Geider R.J., La Roche J., Greene R.M., Olaizola M. Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. Journal of Phycology 1993, 29:755-766.
22. Gottschalk F., Sonderer T., Scholz R.W., Nowack B. Modeled environmental concentrations of engineered nanomaterials (TiO(2), ZnO, Ag, CNT fullerenes) for different regions. Environmental Science and Technology 2009, 43:9216-9222.
23. Granum E., Kirkvold S., Myklestad S.M. Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Marine Ecology Progress Series 2002, 242:83-94.
24. Griffiths M.J., Garcin C., van Hille R.P., Harrison S.T.L. Interference by pigment in the estimation of microalgal biomass concentration by optical density. Journal of Microbiological Methods 2011, 85:119-123.
25. Guillard R.L.L. Division rates. Handbook of Phycological Methods: Culture Methods and Growth Measurements 1973, 289-311. Cambridge University Press, Cambridge. J.R. Stein (Ed.).
26. Guillard R.R.L. Culture of phytoplankton for feeding of marine invertebrates. Culture of Marine Invertebrate Animals 1975, 26-60. Plenum Press, New York, USA. W. Smith, M. Chanley (Eds.).
27. Guillard R.R.L., Ryther J.H. Studies of marine planktonic diatoms I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology 1962, 8:229-239.
28. Hardman R. A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environmental Health Perspectives 2006, 114:165-172.
29. Heuillet E., Moreau A., Halpern S. Cadmium binding to a thiol-molecule in vacuoles of Dunaliella bioculata contaminated with CdCl2: electron probe microanalysis. Biology of the Cell 1986, 58:79-86.
30. Howe G., Merchant S. Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiology 1992, 98:127-136.
31. Ipe B.I., Lehnig M., Niemeyer C.M. On the generation of free radical species from quantum dots. Small 2005, 1:706-709.
32. Jia G., Wang H.F., Yan L., Wang X., Pei R.J., Yan T., Zhao Y.L., Guo X.B. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environmental Science and Technology 2005, 39:1378-1383.
33. Kim J., Park Y., Yoon T.H., Yoon C.S., Choi K. Phototoxicity of CdSe/ZnSe quantum dots with surface coatings of 3-mercaptopropionic acid or tri-n-octylphosphine oxide/gum arabic in Daphnia magna under environmentally relevant UV-B light. Aquatic Toxicology 2010, 97:116-124.
34. Kim S., Fisher B., Eisler H.-J., Bawendi M. Type-II quantum dots:CdTe/CdSe(Core/Shell) and CdSe/ZnTe(Core/Shell) heterostructures. Journal of the American Chemical Society 2003, 125:11466-11467.
35. Kirchner C., Liedl T., Kudera S., Pellegrino T., Muñoz Javier A., Gaub H.E., Stölzle S., Fertig N., Parak W.J. Cytotoxicity of colloidal CdSe and CdSe/ZnS nanoparticles. Nano Letters 2004, 5:331-338.
36. Laurentin A., Edwards C.A. A microtiter modification of the anthrone-sulfuric acid colorimetric assay for glucose-based carbohydrates. Analytical Biochemistry 2003, 315:143-145.
37. Lee M.Y., Shin H.W. Cadmium-induced changes in antioxidant enzymes from the marine alga Nannochloropsis oculata. Journal of Applied Phycology 2003, 15:13-19.
38. Mahendra S., Zhu H.G., Colvin V.L., Alvarez P.J. Quantum dot weathering results in microbial toxicity. Environmental Science and Technology 2008, 42:9424-9430.
39. Miao A.J., Schwehr K.A., Xu C., Zhang S.J., Luo Z.P., Quigg A., Santschi P.H. The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environmental Pollution 2009, 157:3034-3041.
40. Miao A.J., Wang W.X. Relationships between cell-specific growth rate and uptake rate of cadmium and zinc by a coastal diatom. Marine Ecology Progress Series 2004, 275:103-113.
41. Miao A.J., Wang W.X. Cadmium toxicity to two marine phytoplankton under different nutrient conditions. Aquatic Toxicology 2006, 78:114-126.
42. Miao A.J., Wang W.X., Juneau P. Comparison of Cd, Cu, and Zn toxic effects on four marine phytoplankton by pulse-amplitude-modulated fluorometry. Environmental Toxicology and Chemistry 2005, 24:2603-2611.
43. Michalet X., Pinaud F.F., Bentolila L.A., Tsay J.M., Doose S., Li J.J., Sundaresan G., Wu A.M., Gambhir S.S., Weiss S. Quantum dots for live cells, in vivo imaging, and diagnostics. Science 2005, 307:538-544.
44. Mishra A., Jha B. Antioxidant response of the microalga Dunaliella salina under salt stress. Botanica Marina 2011, 54:195-199.
45. Moreau J.W., Weber P.K., Martin M.C., Gilbert B., Hutcheon I.D., Banfield J.F. Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 2007, 316:1600-1603.
46. Mueller N.C., Nowack B. Exposure modeling of engineered nanoparticles in the environment. Environmental Science & Technology 2008, 42:4447-4453.
47. Murray C.B., Norris D.J., Bawendi M.G. Synthesis and characterization of nearly monodisperse CdE (E=S, Se Te) semiconductor nanocrystallites. Journal of the American Chemical Society 1993, 115:8706-8715.
48. Myklestad S. Production of carbohydrates by marine planktonic diatoms I. Comparison of nine different species in culture. Journal of Experimental Marine Biology and Ecology 1974, 15:261-274.
49. Myklestad S.M. Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Science of the Total Environment 1995, 165:155-164.
50. Myklestad S.M., Skanoy E., Hestmann S. A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Marine Chemistry 1997, 56:279-286.
51. Nassiri Y., Mansot J.L., Wéry J., Ginsburger-Vogel T., Amiard J.C. Ultrastructural and electron energy loss spectroscopy studies of sequestration mechanisms of Cd and Cu in the marine diatom Skeletonema costatum. Archives of Environmental Contamination and Toxicology 1997, 33:147-155.
52. Navarro E., Baun A., Behra R., Hartmann N.B., Filser J., Miao A.J., Quigg A., Santschi P.H., Sigg L. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 2008, 17:372-386.
53. Nel A., Xia T., Madler L., Li N. Toxic potential of materials at the nanolevel. Science 2006, 311:622-627.
54. Nies D.H. Microbial heavy-metal resistance. Applied Microbiology and Biotechnology 1999, 51:730-750.
55. Nishikawa K., Yamakoshi Y., Uemura I., Tominaga N. Ultrastructural changes in Chlamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism. FEMS Microbiology Ecology 2003, 44:253-259.
56. Passow U. Transparent exopolymer particles (TEP) in aquatic environments. Progress in Oceanography 2002, 55:287-333.
57. Penna A., Berluti S., Penna N., Magnani M. Influence of nutrient ratios on the in vitro extracellular polysaccharide production by marine diatoms from the Adriatic Sea. Journal of Plankton Research 1999, 21:1681-1690.
58. Priester J.H., Stoimenov P.K., Mielke R.E., Webb S.M., Ehrhardt C., Zhang J.P., Stucky G.D., Holden P.A. Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonic Pseudomonas aeruginosa. Environmental Science and Technology 2009, 43:2589-2594.
59. Quigg A. Trace Elements. Ecological Stoichiometry in the Encyclopedia of Ecology 2008, 3564-3573. Elsevier, Oxford. S.E. Jørgensen, B.D. Fath (Eds.).
60. Quigley M.S., Santschi P.H., Hung C.C., Guo L., Honeyman B.D. Importance of acid polysaccharides for 234Th complexation to marine organic matter. Limnology and Oceanography 2002, 47:367-377.
61. Rao M.V., Paliyath G., Ormrod D.P. Ultraviolet-B- and ozone-induced biochemical changes in antioxidant Enzymes of Arabidopsis thaliana. Plant Physiology 1996, 110:125-136.
62. Rejman J., Oberle V., Zuhorn I.S., Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin-and caveolae-mediated endocytosis. Biochemical Journal 2004, 377:159-169.
63. Rijstenbil J.W. Assessment of oxidative stress in the planktonic diatom Thalassiosira pseudonana in response to UVA and UVB radiation. Journal of Plankton Research 2002, 24:1277-1288.
64. Rijstenbil J.W., Sandee A., van Drie J., Wijnholds J.A. Interaction of toxic trace metals and mechanisms of detoxification in the planktonic diatoms Ditylum brightwellii and Thalassiosira pseudonana. FEMS Microbiology Reviews 1994, 14:387-396.
65. Santschi P.H., Hung C.C., Schultz G., Alvarado-Quiroz N., Guo L., Pinckney J., Walsh I. Control of acid polysaccharide production and 234Th and POC export fluxes by marine organisms. Geophysical Research Letters 2003, 30:11-16.
66. Siripornadulsil S., Traina S., Verma D.P.S., Sayre R.T. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 2002, 14:2837-2847.
67. Smeets K., Cuypers A., Lambrechts A., Semane B., Hoet P., Van Laere A., Vangronsveld J. Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiology and Biochemistry 2005, 43:437-444.
68. Smith A.M., Duan H., Mohs A.M., Nie S. Bioconjugated quantum dots for in vivo molecular and cellular imaging. Advanced Drug Delivery Reviews 2008, 60:1226-1240.
69. Spielmeyer A., Pohnert G. Daytime, growth phase and nitrate availability dependent variations of dimethylsulfoniopropionate in batch cultures of the diatom Skeletonema marinoi. Journal of Experimental Marine Biology and Ecology 2012, 413:121-130.
70. Tang M., Wang M., Xing T., Zeng J., Wang H., Ruan D.-Y. Mechanisms of unmodified CdSe quantum dot-induced elevation of cytoplasmic calcium levels in primary cultures of rat hippocampal neurons. Biomaterials 2008, 29:4383-4391.
71. Urbani R., Magaletti E., Sist P., Cicero A.M. Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium Thalassiosira pseudonana and Skeletonema costatum: effect of P-depletion and growth status. Science of the Total Environment 2005, 353:300-306.
72. Verdugo P. Dynamics of marine biopolymer networks. Polymer Bulletin 2007, 58:139-143.
73. Verdugo P. Marine Microgels. Annual Review of Marine Science 2012, 4:375-400.
74. Verdugo P., Alldredge A.L., Azam F., Kirchman D.L., Passow U., Santschi P.H. The oceanic gel phase: a bridge in the DOM-POM continuum. Marine Chemistry 2004, 92:67-85.
75. Verdugo P., Orellana M.V., Chin W.C., Petersen T.W., van den Eng G., Benner R., Hedges J.I. Marine biopolymer self-assembly: implications for carbon cycling in the ocean. Faraday Discussions 2008, 139:393-398.
76. Verdugo P., Santschi P.H. Polymer dynamics of DOC networks and gel formation in seawater. Deep-Sea Research Part II: Topical Studies in Oceanography 2010, 57:1486-1493.
77. Wang M.J., Wang W.X. Cadmium in three marine phytoplankton: accumulation, subcellular fate and thiol induction. Aquatic Toxicology 2009, 95:99-107.
78. Wang M.J., Wang W.X. Cadmium sensitivity, uptake, subcellular distribution and thiol induction in a marine diatom: exposure to cadmium. Aquatic Toxicology 2011, 101:377-386.
79. Wätjen W., Beyersmann D. Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress. BioMetals 2004, 17:65-78.
80. Zhang S., Jiang Y., Chen C.-S., Spurgin J., Schwehr K.A., Quigg A., Chin W.-C., Santschi P.H. Aggregation and dissolution of quantum dots in marine environments: the importance of extracellular polymeric substances (EPS). Environmental Science and Technology 2012, 46:8764-8772.