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Can Metal Nanoparticles Be a Threat to Microbial Decomposers of Plant Litter in Streams?

  • Environmental Microbiology
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Abstract

The extensive use of nanometal-based products increases the chance of their release into aquatic environments, raising the question whether they can pose a risk to aquatic biota and the associated ecological processes. Aquatic microbes, namely fungi and bacteria, play a key role in forested streams by decomposing plant litter from terrestrial vegetation. Here, we investigated the effects of nanocopper oxide and nanosilver on leaf litter decomposition by aquatic microbes, and the results were compared with the impacts of their ionic precursors. Alder leaves were immersed in a stream of Northwest Portugal to allow microbial colonization before being exposed in microcosms to increased nominal concentrations of nanometals (CuO, 100, 200 and 500 ppm; Ag, 100 and 300 ppm) and ionic metals (Cu2+ in CuCl2, 10, 20 and 30 ppm; Ag+ in AgNO3, 5 and 20 ppm) for 21 days. Results showed that rates of leaf decomposition decreased with exposure to nano- and ionic metals. Nano- and ionic metals inhibited bacterial biomass (from 68.6% to 96.5% of control) more than fungal biomass (from 28.5% to 82.9% of control). The exposure to increased concentrations of nano- and ionic metals decreased fungal sporulation rates from 91.0% to 99.4%. These effects were accompanied by shifts in the structure of fungal and bacterial communities based on DNA fingerprints and fungal spore morphology. The impacts of metal nanoparticles on leaf decomposition by aquatic microbes were less pronounced compared to their ionic forms, despite metal ions were applied at one order of magnitude lower concentrations. Overall, results indicate that the increased release of nanometals to the environment may affect aquatic microbial communities with impacts on organic matter decomposition in streams.

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References

  1. Aitken RJ, Chaudhry MQ, Boxall ABA, Hull M (2006) Manufacture and use of nanomaterials: current status in the UK and global trends. Occup Med 56:300–306

    Article  CAS  Google Scholar 

  2. Aruoja V, Dubourguier HC, Kasemets K, Kahru A (2009) Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407:1461–1468

    Article  PubMed  CAS  Google Scholar 

  3. Azevedo MM, Almeida B, Ludovico P, Cássio F (2009) Metal stress induces programmed cell death in aquatic fungi. Aquat Toxicol 92:264–270

    Article  PubMed  CAS  Google Scholar 

  4. Blaser SA, Scheringer M, MacLeod M, Hungerbühler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 390:396–409

    Article  PubMed  CAS  Google Scholar 

  5. Battin TJ, Kammer FVD, Weilhartner A, Ottofuelling S, Hofmann T (2009) Nanostructured TiO2: transport behavior and effects on aquatic microbial communities under environmental conditions. Environ Sci Technol 43:8098–8104

    Article  PubMed  CAS  Google Scholar 

  6. Birceanu O, Chowdhury MJ, Gillis PL, McGeer JC, Wood CM, Wilkie MP (2008) Modes of metal toxicity and impaired branchial ionoregulation in rainbow trout exposed to mixtures of Pb and Cd in soft water. Aquat Toxicol 89:222–231

    Article  PubMed  CAS  Google Scholar 

  7. Bradford A, Handy RD, Redman JW, Atfield A, Mühling M (2009) Impact of silver nanoparticle contamination on the genetic diversity of natural bacterial assemblages in estuarine sediments. Environ Sci Technol 43:4530–4536

    Article  PubMed  CAS  Google Scholar 

  8. Braha B, Tintemann H, Krauss G, Ehrman J, Bärlocher F, Krauss GJ (2007) Stress response in two strains of the aquatic hyphomycete Heliscus lugdunensis after exposure to cadmium and copper ions. Biometals 20:93–105

    Article  PubMed  CAS  Google Scholar 

  9. Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42:4583–4588

    Article  PubMed  CAS  Google Scholar 

  10. Duarte S, Pascoal C, Alves A, Correia A, Cássio F (2008) Copper and zinc mixtures induce shifts in microbial communities and reduce leaf litter decomposition in streams. Freshw Biol 53:91–101

    CAS  Google Scholar 

  11. Duarte S, Pascoal C, Cássio F (2008) High diversity of fungi may mitigate the impact of pollution on plant litter decomposition in streams. Microb Ecol 56:688–695

    Article  PubMed  CAS  Google Scholar 

  12. Duarte S, Pascoal C, Cássio F (2009) Functional stability of stream-dwelling microbial decomposers exposed to copper and zinc stress. Freshw Biol 54:1683–1691

    Article  CAS  Google Scholar 

  13. Fernandes I, Duarte S, Pascoal C, Cássio F (2009) Mixtures of zinc and phosphate affect leaf litter decomposition by aquatic fungi in streams. Sci Total Environ 407:4283–4288

    Article  PubMed  CAS  Google Scholar 

  14. Gessner MO (2005) Ergosterol as a measure of fungal biomass. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition: a practical guide. Springer, Dordrecht, Netherlands, pp 189–196

    Chapter  Google Scholar 

  15. Gopalakrishnan S, Thilagam H, Raja PV (2008) Comparison of heavy metal toxicity in life stages (spermiotoxicity, egg toxicity, embryotoxicity and larval toxicity) of Hydroides elegans. Chemosphere 71:515–528

    Article  PubMed  CAS  Google Scholar 

  16. Graça MAS (2001) The role of invertebrates on leaf litter decomposition in streams – a Review. Int Rev Hydrobiol 86:383–393

    Article  Google Scholar 

  17. Griffitt RJ, Luo J, Gao J, Bonzango JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanoparticles in aquatic organisms. Environ Toxicol Chem 27:1972–1978

    Article  PubMed  CAS  Google Scholar 

  18. Griffitt RJ, Hyndman K, Denslow ND, Barber DS (2009) Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 107:404–415

    Article  PubMed  CAS  Google Scholar 

  19. Heinlaan M, Ivask A, Blinova I, Dubourguier HC, Kahru A (2008) Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71:1308–1316

    Article  PubMed  CAS  Google Scholar 

  20. Holsapple MP, Farland WH, Landry TD, Monteiro-Riviere NA, Carter JM, Walker NJ, Thomas KV (2005) Research strategies for safety evaluation of nanomaterials, part II: toxicological and safety evaluation of nanomaterials, current challenges and data needs. Toxicol Sci 88:12–17

    Article  PubMed  CAS  Google Scholar 

  21. Hsiao MC, Wang HP, Yang YW (2001) EXAFS and XANES studies of copper in a solidified fly ash. Environ Sci Technol 35:2532–2535

    Article  PubMed  CAS  Google Scholar 

  22. Huang HL, Wang HP, Wei GT, Sun IW, Huang JF, Yang YW (2006) Extraction of nanosize copper pollutants with an ionic liquid. Environ Sci Technol 40:4761–4764

    Article  PubMed  CAS  Google Scholar 

  23. Jaeckel P, Krauss GJ, Krauss G (2005) Cadmium and zinc response of the fungi Heliscus lugdunensis and Verticillium cf. alboatrum isolated from highly polluted water. Sci Total Environ 346:274–279

    Article  PubMed  CAS  Google Scholar 

  24. Kaegi R, Ulrich A, Sinnet B, Vonbank R, Wichser A, Zuleeg S, Simmler H, Brunner S, Vonmont H, Burkhardt M, Boller M (2008) Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. Environ Pollut 156:233–239

    Article  PubMed  CAS  Google Scholar 

  25. Karlsson HL, Gustafsson J, Cronholm P, Möller L (2009) Size-dependent toxicity of metal oxide particles–A comparison between nano- and micrometer size. Toxicol Lett 188:112–118

    Article  PubMed  CAS  Google Scholar 

  26. Kasemets K, Ivask A, Dubourguier HC, Kahru A (2009) Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol Vitro 23:1116–1122

    Article  CAS  Google Scholar 

  27. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3:95–101

    PubMed  CAS  Google Scholar 

  28. Kim KJ, Sung WS, Moon SK, Choi JS, Kim JG, Lee DG (2008) Antifungal effect of silver nanoparticles on dermatophytes. J Microbiol Biotechnol 18:1482–1484

    PubMed  CAS  Google Scholar 

  29. Luechinger NA, Athanassiou EK, Stark WJ (2008) Graphene-stabilized copper nanoparticles as an air-stable substitute for silver and gold in low-cost ink-jet printable electronics. Nanotechnology 19:445201 (6 pp)

    Google Scholar 

  30. Medeiros A, Duarte S, Pascoal C, Cássio F, Graça MAS (2010) Effects of Zn, Fe and Mn on leaf litter breakdown by aquatic fungi: a microcosm study. Internat Rev Hydrobiol 95:12–26

    Article  CAS  Google Scholar 

  31. Miao AJ, Schwehr KA, Xu C, Zhang SJ, Luo Z, Quigg A, Santschi PH (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Pollut 157:3034–3041

    Article  PubMed  CAS  Google Scholar 

  32. Moreirinha C, Duarte S, Pascoal C, Cássio F (2010) Effects of cadmium and phenanthrene mixtures on aquatic fungi and microbially mediated leaf litter decomposition. Arch Environ Contam Toxicol. doi:10.1007/s00244-010-9610-6

    PubMed  Google Scholar 

  33. Mortimer M, Kasemets K, Kahru A (2010) Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology 269:182–189

    Article  PubMed  CAS  Google Scholar 

  34. Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453

    Article  PubMed  CAS  Google Scholar 

  35. Nair LS, Laurencin CT (2007) Silver nanoparticles: synthesis and therapeutic applications. J Biomed Nanotech 3:301–316

    Article  CAS  Google Scholar 

  36. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386

    Article  PubMed  CAS  Google Scholar 

  37. Niyogi DK, Lewis WM Jr, McKnight DM (2002) Effects of stress from mine drainage on diversity, biomass, and function of primary producers in mountain streams. Ecosystems 5:554–567

    CAS  Google Scholar 

  38. Norland S (1993) The relationship between biomass and volume of bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of Methods in Aquatic Microbial Ecology. Lewis publishers, Boca Raton, Florida, pp 303–307

    Google Scholar 

  39. Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen-Dechent W (2007) Size-dependent cytotoxicity of gold nanoparticles. Small 3:1941–1949

    Article  PubMed  CAS  Google Scholar 

  40. Panyala NR, Peña-Méndez EM, Havel J (2008) Silver or silver nanoparticles: a hazardous threat to the environment and human health? J Appl Biomed 6:117–119

    CAS  Google Scholar 

  41. Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microbiol 70:5266–5273

    Article  PubMed  CAS  Google Scholar 

  42. Pascoal C, Cássio F, Gomes P (2001) Leaf breakdown rates: a measure of water quality? Int Rev Hydrobiol 86:407–416

    Article  CAS  Google Scholar 

  43. Pascoal C, Cássio F, Marcotegui A, Sanz B, Gomes P (2005) Role of fungi, bacteria, and invertebrates in leaf litter breakdown in a polluted river. J N Am Benthol Soc 24:784–797

    Article  Google Scholar 

  44. Pascoal C, Marvanová L, Cássio F (2005) Aquatic hyphomycete diversity in streams of Northwest Portugal. Fungal Divers 19:109–128

    Google Scholar 

  45. Pascoal C, Pinho M, Cássio F, Gomes P (2003) Assessing structural and functional ecosystem condition using leaf breakdown: studies on a polluted river. Freshw Biol 48:2033–2044

    Article  Google Scholar 

  46. Perugini P, Simeoni S, Scalia S, Genta I, Modena T, Conti B, Pavanetto F (2002) Effect of nanoparticle encapsulation on the photostability of the sunscreen agent, 2-ethylhexyl-p-methoxycinnamate. Int J Pharm 246:37–45

    Article  PubMed  CAS  Google Scholar 

  47. Ren G, Hu D, Cheng EWC, Vargas-Reus MA, Reip P, Allaker RP (2009) Characterisation of copper oxide nanoparticles for antimicrobial applications. Int J Antimicrob Ag 33:587–590

    Article  CAS  Google Scholar 

  48. Rispoli F, Angelov A, Badia D, Kumar A, Seal S, Shah V (2010) Understanding the toxicity of aggregated zero valent copper nanoparticles against Escherichia coli. J Hazard Mater 180:212–216

    Article  PubMed  CAS  Google Scholar 

  49. Saison C, Perreault F, Daigle JC, Fortin C, Claverie J, Morin M, Popovic R (2010) 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 96:109–114

    Article  PubMed  CAS  Google Scholar 

  50. Salata OV (2004) Applications of nanoparticles in biology and medicine. J Nanobiotechnol 2 (6 pp)

  51. Saquing CD, Manasco JL, Khan SA (2009) Electrospun nanoparticle–nanofiber composites via a one-step Synthesis. Small 5:944–951

    Article  PubMed  CAS  Google Scholar 

  52. Schneider T, Gerrits B, Gassmann R, Schmid E, Gessner MO, Richter A, Battin T, Eberl L, Riedel K (2010) Proteome analysis of fungal and bacterial involvement in leaf litter decomposition. Proteomics 10:1819–1830

    Article  PubMed  CAS  Google Scholar 

  53. Shah V, Belozerova I (2009) Influence of metal nanoparticles on the soil microbial community and germination of lettuce seeds. Water Air Soil Pollut 197:143–148

    Article  CAS  Google Scholar 

  54. Shah V, Dobiášová P, Baldrian P, Nerud F, Kumar A, Seal S (2010) Influence of iron and copper nanoparticle powder on the production of lignocellulose degrading enzymes in the fungus Trametes versicolor. J Hazard Mater 178:1141–1145

    Article  PubMed  CAS  Google Scholar 

  55. Sridhar KR, Bärlocher F, Krauss GJ, Krauss G (2005) Response of aquatic hyphomycete communities to changes in heavy metal exposure. Int Rev Hydrobiol 90:21–32

    Article  CAS  Google Scholar 

  56. Van Hoecke K, Quik JT, Mankiewicz-Boczek J, De Schamphelaere KA, Elsaesser A, Van der Meeren P, Barnes C, McKerr G, Howard CV, Van de Meent D, Rydzyński K, Dawson KA, Salvati A, Lesniak A, Lynch I, Silversmit G, De Samber B, Vincze L, Janssen CR (2009) Fate and effects of CeO2 nanoparticles in aquatic ecotoxicity tests. Environ Sci Technol 43:4537–4546

    Article  PubMed  Google Scholar 

  57. Wang W, Zhan Y, Wang X, Liu Y, Zheng C, Wang G (2002) Synthesis and characterization of CuO nanowhiskers by a novel one-step, solid-state reaction in the presence of a nonionic surfactant. Mater Res Bull 37:1093–1100

    Article  CAS  Google Scholar 

  58. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Inc, New York, pp 315–322

    Google Scholar 

  59. Yoon KY, Byeon JH, Park JH, Hwang J (2007) Susceptibility constants of Escherichia coli and Bacillus subtilis to silver and copper nanoparticles. Sci Total Environ 373:572–575

    Article  PubMed  CAS  Google Scholar 

  60. Zar JH (2009) Biostatistical analysis, 5th edn. Prentice-Hall, Upper Saddle River, New Jersey

    Google Scholar 

  61. Zhang F, Wu X, Chen Y, Lin H (2009) Application of silver nanoparticles to cotton fabric as an antibacterial textile finish. Fibers Polym 10:496–501

    Article  CAS  Google Scholar 

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Acknowledgements

A. Pradhan was supported by the Portuguese Foundation for Science and Technology (SFRH/BD/45614/2008).

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Correspondence to Fernanda Cássio.

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Pradhan, A., Seena, S., Pascoal, C. et al. Can Metal Nanoparticles Be a Threat to Microbial Decomposers of Plant Litter in Streams?. Microb Ecol 62, 58–68 (2011). https://doi.org/10.1007/s00248-011-9861-4

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