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Direct and indirect effects of zinc oxide and titanium dioxide nanoparticles on the decomposition of leaf litter in streams

  • Sumaya Al Riyami
  • Dalal Al Mahrouqi
  • Raeid M. M. Abed
  • Abdulkadir Elshafie
  • Priyanka Sathe
  • Michael J. BarryEmail author
Article

Abstract

As the production of metallic nanoparticles has grown, it is important to assess their impacts on structural and functional components of ecosystems. We investigated the effects of zinc and titanium nanoparticles on leaf decomposition in freshwater habitats. We hypothesized that nanoparticles would inhibit the growth and activity of microbial communities leading to decreased decomposition rates. We also hypothesized that under natural light, the nanoparticles would produce reactive oxygen species that could potentially accelerate decomposition. In the lab, whole Ficus vasta leaves were placed in containers holding one liter of stream water and exposed to either 0, 1, 10 or 100 mg/L of ZnO or TiO2 nanoparticles for six weeks (referred to as Exp. 1). We measured leaf mass loss, microbial metabolism, and bacterial density at 2, 4, and 6 weeks. In a second experiment (referred to as Exp. 2), we measured the effects of light and 10 and 100 mg/L ZnO or TiO2 nanoparticles on leaf mass loss, bacterial density and the bacterial and fungal community diversity over a 2 week period. In Experiment 1, mass loss was significantly reduced at 10 and 100 mg/L after 6 weeks and bacterial density decreased at 100 mg/L. In Experiment 2, there was no effect of ZnO nanoparticles on leaf mass loss, but TiO2 nanoparticles significantly reduced mass loss in the dark but not in the light. One possible explanation is that release of reactive oxygen species by the TiO2 nanoparticles in the light may have increased the rate of leaf decomposition. Bacterial and fungal diversity was highest in the dark, but nanoparticles did not reduce overall diversity.

Keywords

Nanoparticle Zinc Titanium Leaf litter Ecosystem function Decomposition 

Notes

Acknowledgements

We acknowledge the assistance and advice of Prof Joydeep Dutta, Drs Mohammed Al Abri, Myo Tay Zar Myint and Laila Al-Naamani from the Chair in Nanotechnology at Sultan Qaboos University. This project was funded through a Sultan Qaboos University internal grant to MJB.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This research did not involve the use of human or animal subjects.

References

  1. Abed RMM, Al-Kharusi S, Prigent S, Headley T (2014) Diversity, distribution and hydrocarbon biodegradation capabilities of microbial communities in oil-contaminated cyanobacterial mats from a constructed wetland. PLoS ONE 9:e114570.  https://doi.org/10.1371/journal.pone.0114570 CrossRefGoogle Scholar
  2. Adams LK, Lyon DY, Alvarez PJJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40:3527–3532.  https://doi.org/10.1016/j.watres.2006.08.004 CrossRefGoogle Scholar
  3. Al-Riyami M, Victor R, Seena S et al. (2009) Leaf decomposition in a mountain stream in the sultanate of oman. Int Rev Hydrobiol 94:16–28.  https://doi.org/10.1002/iroh.200811085 CrossRefGoogle Scholar
  4. Badawy AMEl, Luxton TP, Silva RG et al. (2010) Impact of environmental conditions (pH, ionic strength, and electrolyte type) on the surface charge and aggregation of silver nanoparticles suspensions. Environ Sci Technol 44:1260–1266CrossRefGoogle Scholar
  5. Bai W, Zhang Z, Tian W et al. (2010) Toxicity of zinc oxide nanoparticles to zebrafish embryo: A physicochemical study of toxicity mechanism. J Nanopart Res 12:1645–1654.  https://doi.org/10.1007/s11051-009-9740-9 CrossRefGoogle Scholar
  6. Bian S-W, Mudunkotuwa IA, Rupasinghe T, Grassian VH (2011) Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27:6059–6068CrossRefGoogle Scholar
  7. Binh CTT, Tong T, Gaillard J-F et al. (2014a) Acute effects of TiO2 nanomaterials on the viability and taxonomic composition of aquatic bacterial communities assessed via high-throughput screening and next generation sequencing. PLoS ONE 9:e106280.  https://doi.org/10.1371/journal.pone.0106280 CrossRefGoogle Scholar
  8. Binh CTT, Tong T, Gaillard JF et al. (2014b) Common freshwater bacteria vary in their responses to short-term exposure to nano-TiO2. Environ Toxicol Chem 33:317–327.  https://doi.org/10.1002/etc.2442 CrossRefGoogle Scholar
  9. Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 5:1701–1712.  https://doi.org/10.1038/ismej.2011.52 CrossRefGoogle Scholar
  10. Brunner TJ, Wick P, Manser P et al. (2006) In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 40:4374–4381CrossRefGoogle Scholar
  11. Bunn SE, Balcombe SR, Davies PM et al. (2006) Aquatic productivity and food webs of desert river ecosystems. In: Kingsford RC (ed.) Ecology of Desert Rivers, 1st edition. Cambridge University Press, Cambridge; New York, pp 76–99Google Scholar
  12. Cohen JS, Ng S, Blossey B (2012) Quantity counts: amount of litter determines tadpole performance in experimental microcosms. J Herpetol 46:85–90.  https://doi.org/10.1670/10-289 CrossRefGoogle Scholar
  13. Collins D, Luxton T, Kumar N et al. (2012) Assessing the impact of copper and zinc oxide nanoparticles on soil: a field study. PLoS ONE 7:e42663.  https://doi.org/10.1371/journal.pone.0042663 CrossRefGoogle Scholar
  14. Coltro L, Borghetti J (2007) Plastic packages for personal care products—evaluation of light barrier properties. Polim Cienc e Tecnol 17:56–61.  https://doi.org/10.1590/S0104-14282007000100013 CrossRefGoogle Scholar
  15. Dangles O, Chauvet E (2003) Effects of stream acidification on fungal biomass in decaying beech leaves and leaf palatability. Water Res 37:533–538CrossRefGoogle Scholar
  16. Du J, Zhang Y, Cui M et al. (2017) Evidence for negative effects of ZnO nanoparticles on leaf litter decomposition in freshwater ecosystems. Environ Sci Nano 3:1–2.  https://doi.org/10.1039/C7EN00784A Google Scholar
  17. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998CrossRefGoogle Scholar
  18. Elskus AA, Smalling KL, Hladik ML, Kuivila KM (2016) Effects of 2 fungicide formulations on microbial and macroinvertebrate leaf decomposition under laboratory conditions. Environ Toxicol Chem.  https://doi.org/10.1002/etc.3465
  19. Franken RJM (2008) Habitat variation and life history strategies of Benthic invertebrates. Thesis Wageningen University, WageningenGoogle Scholar
  20. Gajbhiye M, Kesharwani J, Ingle A et al. (2009) Fungus-mediated synthesis of silver nanoparticles and their activity against pathogenic fungi in combination with fluconazole. Nanomedicine 5:382–386.  https://doi.org/10.1016/j.nano.2009.06.005 CrossRefGoogle Scholar
  21. Gessner MO, Chauvet E (2002) A case for using litter breakdown to assess functional stream integrity. Ecol Appl 12:498–510CrossRefGoogle Scholar
  22. Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134CrossRefGoogle Scholar
  23. Haas BJ, Gevers D, Earl AM et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504.  https://doi.org/10.1101/gr.112730.110 CrossRefGoogle Scholar
  24. Heinlaan M, Ivask A, Blinova I et al. (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.  https://doi.org/10.1016/j.chemosphere.2007.11.047 CrossRefGoogle Scholar
  25. Hendren CO, Mesnard X, Dröge J, Wiesner MR (2011) Estimating production data for five engineered nanomaterials as a basis for exposure assessment. Environ Sci Technol 45:2562–2569.  https://doi.org/10.1021/es103300g CrossRefGoogle Scholar
  26. Holden PA, Nisbet RM, Lenihan HS et al. (2013) Ecological nanotoxicology: integrating nanomaterial hazard considerations across the subcellular, population, community, and ecosystems levels. Acc Chem Res 46(3):813–22.  https://doi.org/10.1021/ar300069t CrossRefGoogle Scholar
  27. Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625.  https://doi.org/10.1016/J.ENVPOL.2008.12.025 CrossRefGoogle Scholar
  28. Jonsson M, Malmqvist B, Hoffsten P-O (2001) Leaf litter breakdown rates in boreal streams: does shredder species richness matter? Freshw Biol 46:161–171.  https://doi.org/10.1046/j.1365-2427.2001.00655.x CrossRefGoogle Scholar
  29. Kiser MA, Westerhoff P, Benn T et al. (2009) Titanium nanomaterial removal and release from wastewater treatment plants. Environ Sci Technol 43:6757–6763.  https://doi.org/10.1021/es901102n CrossRefGoogle Scholar
  30. Klindworth A, Pruesse E, Schweer T et al. (2012) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:gks808CrossRefGoogle Scholar
  31. Kohen R, Nyska A (2002) Invited review: oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650.  https://doi.org/10.1080/01926230290166724 CrossRefGoogle Scholar
  32. Kumar A, Pandey AK, Singh SS et al. (2011) Engineered ZnO and TiO2 nanoparticles induce oxidative stress and DNA damage leading to reduced viability of Escherichia coli. Free Radic Biol Med 51:1872–1881.  https://doi.org/10.1016/j.freeradbiomed.2011.08.025 CrossRefGoogle Scholar
  33. Lin L, Webster JR (2014) Detritus decomposition and nutrient dynamics in a forested headwater stream. Ecol Modell 293:58–68.  https://doi.org/10.1016/j.ecolmodel.2013.12.013 CrossRefGoogle Scholar
  34. Liu X, Huang Q-H, Jiang H-L, Song N (2016) Effects of visible light radiation on macrophyte litter degradation and nutrient release in water samples from a eutrophic shallow lake. Chem Ecol 32:961–975.  https://doi.org/10.1080/02757540.2016.1203910 CrossRefGoogle Scholar
  35. Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles – A review. Environ Pollut 172:76–85.  https://doi.org/10.1016/J.ENVPOL.2012.08.011 CrossRefGoogle Scholar
  36. Mace GM, Norris K, Fitter AH (2012) Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol Evol 27:19–26.  https://doi.org/10.1016/J.TREE.2011.08.006 CrossRefGoogle Scholar
  37. Maltby L, Forrow DM, Boxall ABA et al. (1995) The effects of motorway runoff on freshwater ecosystems: 1. Feild study. Environ Toxicol Chem 14:1079–1092.  https://doi.org/10.1002/etc.5620140620 CrossRefGoogle Scholar
  38. Maron M, Mitchell MGE, Runting RK et al. (2017) Towards a threat assessment framework for ecosystem services. Trends Ecol Evol 32(4):240–248.  https://doi.org/10.1016/j.tree.2016.12.011 CrossRefGoogle Scholar
  39. Matranga V, Corsi I (2012) Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar Environ Res 76:32–40CrossRefGoogle Scholar
  40. McBeth JM, Fleming EJ, Emerson D (2013) The transition from freshwater to marine iron-oxidizing bacterial lineages along a salinity gradient on the Sheepscot River, Maine, USA. Environ Microbiol Rep 5:453–463.  https://doi.org/10.1111/1758-2229.12033 CrossRefGoogle Scholar
  41. Mesbah NM, Abou-El-Ela SH, Wiegel J (2007) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol 54:598–617.  https://doi.org/10.1007/s00248-006-9193-y CrossRefGoogle Scholar
  42. Moezzi A, McDonagh AM, Cortie MB (2012) Zinc oxide particles: synthesis, properties and applications. Chem Eng J 185–186:1–22.  https://doi.org/10.1016/J.CEJ.2012.01.076 CrossRefGoogle Scholar
  43. Mulholland PJ (2004) The importance of in-stream uptake for regulating stream concentrations and outputs of N and P from a forested watershed: evidence from long-term chemistry records for Walker Branch Watershed. Biogeochemistry 70:403–426.  https://doi.org/10.1007/s10533-004-0364-y CrossRefGoogle Scholar
  44. Nair S, Sasidharan A, Divya Rani VV et al. (2009) Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells. J Mater Sci Mater Med 20:235–241.  https://doi.org/10.1007/s10856-008-3548-5 CrossRefGoogle Scholar
  45. Niyogi DK, Lewis Jr WM, McKnight DM (2002) Effects of stress from mine drainage on diversity, biomass, and function of primary producers in mountain streams. Ecosystems 5:554–567Google Scholar
  46. Nuyanzina-Boldareva EN, Akimov VN, Takaichi S, Gorlenko VM (2016) New strains of an aerobic anoxygenic phototrophic bacterium Porphyrobacter donghaensis isolated from a Siberian thermal spring and a weakly mineralized lake. Microbiology 85:77–86.  https://doi.org/10.1134/S0026261716010070 CrossRefGoogle Scholar
  47. Ozaki A, Adams E, Binh CTT et al. (2015) One-time addition of nano-TiO2 triggers short-term responses in benthic bacterial communities in artificial streams. Microb Ecol 1–10.  https://doi.org/10.1007/s00248-015-0646-z
  48. Pascoal C, Cássio F, Marcotegui A et al. (2005) Role of fungi, bacteria, and invertebrates in leaf litter breakdown in a polluted river. J North Am Benthol Soc 24:784–797.  https://doi.org/10.1899/05-010.1 CrossRefGoogle Scholar
  49. Paulsson M, Nyström B, Blanck H (2000) Long-term toxicity of zinc to bacteria and algae in periphyton communities from the river Göta Älv, based on a microcosm study. Aquat Toxicol 47:243–257.  https://doi.org/10.1016/S0166-445X(99)00013-2 CrossRefGoogle Scholar
  50. Petrochenko PE, Zhang Q, Bayati R et al. (2014) Cytotoxic evaluation of nanostructured zinc oxide (ZnO) thin films and leachates. Toxicol Vitr 28:1144–1152.  https://doi.org/10.1016/j.tiv.2014.05.004 CrossRefGoogle Scholar
  51. Pradhan A, Seena S, Pascoal C, Cássio F (2011) Can metal nanoparticles be a threat to microbial decomposers of plant litter in streams? Microb Ecol 62:58–68CrossRefGoogle Scholar
  52. Prince RC, Gramain A, Mcgenity TJ (2010) Prokaryotic hydrocarbon degraders. Handbook of Hydrocarbon and Lipid Microbiology. 1672–1692.  https://doi.org/10.1007/978-3-540-77587-4_118
  53. Sandin L, Solimini AG (2009) Freshwater ecosystem structure-function relationships: from theory to application. Freshw Biol 54:2017–2024.  https://doi.org/10.1111/j.1365-2427.2009.02313.x CrossRefGoogle Scholar
  54. Sauer FG, Bundschuh M, Zubrod JP et al. (2016) Effects of salinity on leaf breakdown: dryland salinity versus salinity from a coalmine. Aquat Toxicol 177:425–432.  https://doi.org/10.1016/j.aquatox.2016.06.014 CrossRefGoogle Scholar
  55. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  56. Sharma VK (2009) Aggregation and toxicity of titanium dioxide nanoparticles in aquatic environment—a review. J Environ Sci Heal Part A 44:1485–1495.  https://doi.org/10.1080/10934520903263231 CrossRefGoogle Scholar
  57. Shi H, Magaye R, Castranova V, Zhao J (2013) Titanium dioxide nanoparticles: a review of current toxicological data. Part Fibre Toxicol 10:15.  https://doi.org/10.1186/1743-8977-10-15 CrossRefGoogle Scholar
  58. Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493.  https://doi.org/10.1146/annurev-ecolsys-120213-091917 CrossRefGoogle Scholar
  59. Vannote RL, Minshall GW, Cummins KW et al. (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137.  https://doi.org/10.1139/f80-017 CrossRefGoogle Scholar
  60. von Schiller D, Acuña V, Aristi I et al. (2017) River ecosystem processes: a synthesis of approaches, criteria of use and sensitivity to environmental stressors. Sci Total Environ 596–597:465–480.  https://doi.org/10.1016/j.scitotenv.2017.04.081 CrossRefGoogle Scholar
  61. Wang ZL (2004) Zinc oxide nanostructures: growth, properties and applications. J Phys Condens Matter 16:R829–R858.  https://doi.org/10.1088/0953-8984/16/25/R01 CrossRefGoogle Scholar
  62. Ward AK, Johnson MD (1996) Heterotrophic microorganisms. In: Hauer FR, Lamberti GA (eds) Methods in Stream Ecology. Academic Press, San Diego, p 233–268Google Scholar
  63. Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10.  https://doi.org/10.1890/10-0340.1 CrossRefGoogle Scholar
  64. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosoma RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds). PCR Protocols: A Guide to Methods and Applications. Academic Press, Inc., New York, pp 315–322Google Scholar

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Authors and Affiliations

  1. 1.Biology DepartmentSultan Qaboos UniversityMuscatOman
  2. 2.Department of Marine Biology and FisheriesSultan Qaboos UniversityMuscatOman

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