Toxic interactions of different silver forms with freshwater green algae and cyanobacteria and their effects on mechanistic endpoints and the production of extracellular polymeric substances

Environmental Science: Nano

Volumn 3, Issue 2, 2016, Pages 396-408

  Taylor, Cameron ^a   Matzke, Marianne ^b   Kroll, Alexandra ^c   Read, Daniel S ^b   Svendsen, Claus ^b   Crossley, Alison ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^c SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84966350636     PISSN: 20518153     EISSN: 20518161     Source Type: Journal    
DOI: 10.1039/c5en00183h     Document Type: Article

References (66)

1. Woodrow-Wilson-Database. Project on Emerging Nanotechnologies (2014): Consumer Products Inventory [Internet]. 2014 [cited 2031 Jul 14]. Available from: http://www.nanotechproject.org/cpi/about/updates/
2. S. A. Blaser M. Scheringer M. MacLeod K. Hungerbuhler Estimation of cumulative aquatic exposure and risk due to silver: Contribution of nano-functionalised plastics and textiles Sci. Total Environ. 2008 390 396 409
3. L. Geranio M. Heuberger The Behavior of Silver Nanotextiles during Washing Environ. Sci. Technol. 2009 43 21 8113 8118
4. S. J. Klaine P. J. J. Alvarez G. E. Batley T. F. Fernandes R. D. Handy D. Y. Lyon et al., Nanomaterials in the environment: Behavior, fate, bioavailability, and effects Environ. Toxicol. Chem. 2008 27 9 1825 1851
5. T. M. Benn P. Westerhoff Nanoparticle Silver Released into Water from Commercially Available Sock Fabrics Environ. Sci. Technol. 2008 42 11 4133 4139
6. N. C. Mueller B. Nowack Exposure Modeling of Engineered Nanoparticles in the Environment Environ. Sci. Technol. 2008 42 12 4447 4453
7. F. Gottschalk T. Sonderer R. W. Scholz B. Nowack Modeled Environmental Concentrations of Engineered Nanomaterials (TiO2, ZnO, Ag, CNT, Fullerenes) for Different Regions Environ. Sci. Technol. 2009 43 24 9216 9222
8. F. Gottschalk T. Sonderer R. W. Scholz B. Nowack Possibilities and limitations of modeling environmental exposure to engineered nanomaterials by probabilistic material flow analysis Environ. Toxicol. Chem. 2010 29 5 1036 1048
9. D. M. Mitrano E. K. Lesher A. Bednar J. Monserud C. P. Higgins J. F. Ranville Detecting nanoparticulate silver using single-particle inductively coupled plasma-mass spectrometry Environ. Toxicol. Chem. 2012 31 1 115 121
10. F. Gottschalk T. Sun B. Nowack Environmental concentrations of engineered nanomaterials: review of modeling and analytical studies Environ. Pollut. 2013 181 287 300
11. J. Fabrega S. N. Luoma C. R. Tyler T. S. Galloway J. R. Lead Silver nanoparticles: behaviour and effects in the aquatic environment Environ. Int. 2011 37 2 517 531
12. E. Navarro A. Baun R. Behra N. B. Hartmann J. Filser Q. Antonietta et al., Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi Ecotoxicology 2008 17 5 372 386
13. J. R. Morones J. L. Elechiguerra A. Camacho K. Holt J. B. Kouri J. T. Ram et al., The bactericidal effect of silver nanoparticles Langmuir 2005 16 2346 2353
14. S. Pal Y. K. Tak J. M. Song Does the Antibacterial Activity of Silver Nanoparticles Depend on the Shape of the Nanoparticle? A Study of the Gram-Negative Bacterium Escherichia coli Appl. Environ. Microbiol. 2007 73 6 1712 1720
15. I. Sondi B. Salopek-Sondi Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria J. Colloid Interface Sci. 2004 275 1 177 182
16. A. D. Burchardt R. N. Carvalho A. Valente P. Nativo D. Gilliland C. P. Garcìa et al., Effects of Silver Nanoparticles in Diatom Thalassiosira pseudonana and Cyanobacterium Synechococcus sp Environ. Sci. Technol. 2012 46 20 11336 11344
17. M.-H. Park K.-H. Kim H.-H. Lee J.-S. Kim S.-J. Hwang Selective inhibitory potential of silver nanoparticles on the harmful cyanobacterium Microcystis aeruginosa Biotechnol. Lett. 2010 32 423 428
18. B. M. Angel G. E. Batley C. V. Jarolimek N. J. Rogers The impact of size on the fate and toxicity of nanoparticulate silver in aquatic systems Chemosphere 2013 93 2 359 365
19. A.-J. Miao K. A. Schwehr C. Xu S.-J. Zhang Z. Luo A. Quigg et al., The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances Environ. Pollut. 2009 157 11 3034 3041
20. E. Navarro F. Piccapietra B. Wagner F. Marconi R. Kaegi N. Odzak et al., Toxicity of Silver Nanoparticles to Chlamydomonas reinhardtii Environ. Sci. Technol. 2008 42 23 8959 8964
21. L. M. Stevenson H. Dickson T. Klanjscek A. A. Keller E. McCauley R. M. Nisbet Environmental feedbacks and engineered nanoparticles: mitigation of silver nanoparticle toxicity to Chlamydomonas reinhardtii by algal-produced organic compounds PLoS One 2013 8 9 e74456
22. C. Marambio-Jones E. V. Hoek A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment J. Nanopart. Res. 2010 12 5 1531 1551
23. D. He J. J. Dorantes-Aranda T. D. Waite Silver Nanoparticle-Algae Interactions: Oxidative Dissolution, Reactive Oxygen Species Generation and Synergistic Toxic Effects Environ. Sci. Technol. 2012 46 8731 8738
24. G. A. Sotiriou S. E. Pratsinis Antibacterial activity of nanosilver ions and particles Environ. Sci. Technol. 2010 44 14 5649 5654
25. A. Ivask I. Kurvet K. Kasemets I. Blinova V. Aruoja S. Suppi et al., Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro PLoS One 2014 9 7 e102108
26. H. L. Karlsson P. Cronholm J. Gustafsson L. Möller Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes Chem. Res. Toxicol. 2008 21 9 1726 1732
27. A. Oukarroum S. Bras F. Perreault R. Popovic Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta Ecotoxicol. Environ. Saf. 2012 78 null 80 85
28. A. Oukarroum L. Barhoumi L. Pirastru D. Dewez Silver nanoparticle toxicity effect on growth and cellular viability of the aquatic plant Lemna gibba Environ. Toxicol. Chem. 2013 32 4 902 907
29. I. Rodea-Palomares K. Boltes F. Fernández-Piñas F. Leganés E. García-Calvo J. Santiago et al., Physicochemical characterization and ecotoxicological assessment of CeO2 nanoparticles using two aquatic microorganisms Toxicol. Sci. 2011 119 1 135 145
30. I. Rodea-Palomares S. Gonzalo J. Santiago-Morales F. Leganés E. García-Calvo R. Rosal et al., An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms Aquat. Toxicol. 2012 122-123 133 143
31. A. Nel T. Xia L. Madler N. Li Toxic Potential of Materials Science 2006 311 5761 622 627
32. S. Zhang Y. Jiang C.-S. Chen D. Creeley K. A. Schwehr A. Quigg et al., Ameliorating effects of extracellular polymeric substances excreted by Thalassiosira pseudonana on algal toxicity of CdSe quantum dots Aquat. Toxicol. 2013 126 214 223
33. F. Ribeiro J. A. Gallego-Urrea K. Jurkschat A. Crossley M. Hassellöv C. Taylor et al., Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio Sci. Total Environ. 2013 466-467C 232 241
34. N. Joshi B. T. Ngwenya C. E. French Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances J. Hazard. Mater. 2012 241-242 363 370
35. A. Kroll R. Behra R. Kaegi L. Sigg Extracellular Polymeric Substances (EPS) of Freshwater Biofilms Stabilize and Modify CeO2 and Ag Nanoparticles PLoS One 2014 9 10 e110709
36. PROSPECT, Protocol for Nanoparticle Dispersion, 2010, (May). Available from: http://www.nanotechia.org/sites/default/files/files/PROSPECT-Dispersion-Protocol.pdf
37. W. Anderson D. Kozak V. A. Coleman Å. K. Jämting M. A. Trau Comparative study of submicron particle sizing platforms: Accuracy, precision and resolution analysis of polydisperse particle size distributions J. Colloid Interface Sci. 2013 405 322 330
38. OECD. Test No 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. OECD Guidel Test Chem. OECD Publishing, 2011, Section 2, 25
39. A. Cid C. Herrero J. Abalde Functional analysis of phytoplankton by flow cytometry a study of the effect of copper on a marine diatom Sci. Mar. 1996 60 Supl. 1 303 308
40. R. Prado C. Rioboo C. Herrero P. Suárez-Bregua A. Cid Flow cytometric analysis to evaluate physiological alterations in herbicide-exposed Chlamydomonas moewusii cells Ecotoxicology 2012 21 2 409 420
41. H. Zhao S. Kalivendi H. Zhang J. Joseph K. Nithipatikom J. Vásquez-Vivar et al., Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide Free Radical Biol. Med. 2003 34 11 1359 1368
42. P. Hyka S. Lickova P. Přibyl K. Melzoch K. Kovar Flow cytometry for the development of biotechnological processes with microalgae Biotechnol. Adv. 2013 31 1 2 16
43. C. Saison F. Perreault J.-C. Daigle C. Fortin J. Claverie M. Morin et al., Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii Aquat. Toxicol. 2010 96 2 109 114
44. K. Yoshida E. Igarashi M. Mukai K. Hirata K. Miyamoto Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid Plant, Cell Environ. 2003 26 3 451 457
45. N. von Moos V. I. Slaveykova Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae - state of the art and knowledge gaps Nanotoxicology 2014 8 6 605 630
46. T. J. Stewart J. Traber A. Kroll R. Behra L. Sigg Characterization of extracellular polymeric substances (EPS) from periphyton using liquid chromatography-organic carbon detection-organic nitrogen detection (LC-OCD-OND) Environ. Sci. Pollut. Res. 2013 20 5 3214 3223
47. R Development Core Team. R: A Language and Environment for Statistical Computing [Internet], Vienna, Austria: R Foundation for Statistical Computing, 2013, Available from: www.r-project.org
48. C. Ritz J. C. Streibig Bioassay Analysis using R J. Stat. Softw. 2005 12 5 1 21
49. C. Ritz and J. Streibig, Analysis of Dose Response Data, 2013
50. J. Jiang G. Oberdörster P. Biswas Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies J. Nanopart. Res. 2009 11 1 77 89
51. F. Piccapietra L. Sigg R. Behra Colloidal stability of carbonate-coated silver nanoparticles in synthetic and natural freshwater Environ. Sci. Technol. 2012 46 2 818 825
52. I. Bhatt B. N. Tripathi Chemosphere Interaction of engineered nanoparticles with various components of the environment and possible strategies for their risk assessment Chemosphere 2011 82 3 308 317
53. E. Hoiczyk A. Hansel Cyanobacterial Cell Walls: News from an Unusual Prokaryotic Envelope J. Bacteriol. 2000 182 5 1191 1199
54. Life Sciences, ed., M. A. Pabst, and, G. Zellnig, Graz: Verlag der TU Graz, 2009, vol. 2, MC2009, pp. 183-184
55. C. Zhang Z. Hu B. Deng Silver nanoparticles in aquatic environments: Physiochemical behavior and antimicrobial mechanisms Water Res. 2016 88 403 427
56. A. Kroll M. Pillukat D. Hahn J. Schnekenburger Interference of engineered nanoparticles with in vitro toxicity assays Arch. Toxicol. 2012 86 7 1123 1136
57. Z. Wang J. Li J. Zhao B. Xing Toxicity and Internalization of CuO Nanoparticles to Prokaryotic Alga Microcystis aeruginosa as Affected by Dissolved Organic Matter Environ. Sci. Technol. 2011 45 14 6032 6040
58. R. P. Rastogi S. P. Singh D. Häder R. P. Sinha Biochemical and Biophysical Research Communications Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2 0, 7 0 -dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937 Biochem. Biophys. Res. Commun. 2010 397 3 603 607
59. J. Wang J. Zhu S. Liu B. Liu Y. Gao Z. Wu Chemosphere Generation of reactive oxygen species in cyanobacteria and green algae induced by allelochemicals of submerged macrophytes Chemosphere 2011 85 6 977 982
60. K. K. Schrader F. E. Dayan N. P. D. Nanayakkara Generation of reactive oxygen species by a novel anthraquinone derivative in the cyanobacterium Planktothrix perornata (Skuja) Pestic. Biochem. Physiol. 2005 81 198 207
61. L.-Z. Chen G.-H. Wang S. Hong A. Liu C. Li Y.-D. Liu UV-B-induced oxidative damage and protective role of exopolysaccharides in desert cyanobacterium Microcoleus vaginatus J. Integr. Plant Biol. 2009 51 2 194 200
62. P. Hiriart-baer C. Fortin D. Lee P. G. C. Campbell Toxicity of silver to two freshwater algae, Chlamydomonas reinhardtii and Pseudokirchneriella subcapitata, grown under continuous culture conditions: Influence of thiosulphate Aquat. Bot. 2006 78 136 148
63. R. J. Griffitt J. Luo J. Gao J.-C. Bonzongo D. S. Barber Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms Environ. Toxicol. Chem. 2008 27 9 1972 1978
64. F. Kang P. J. Alvarez D. Zhu Microbial extracellular polymeric substances reduce Ag+ to silver nanoparticles and antagonize bactericidal activity Environ. Sci. Technol. 2014 48 1 316 322
65. C. Zhang Z. Liang Z. Hu Bacterial response to a continuous long-term exposure of silver nanoparticles at sub-ppm silver concentrations in a membrane bioreactor activated sludge system Water Res. 2014 50 350 358
66. D. McShan P. C. Ray H. Yu Molecular toxicity mechanism of nanosilver J. Food Drug Anal. 2014 22 1 116 127