Environmental Science and Pollution Research

, Volume 22, Issue 18, pp 13710–13723 | Cite as

Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review

Microbial Ecology of the Continental and Coastal Environments

Abstract

This report presents an exhaustive literature review of the effects of engineered nanoparticles on soil microbial communities. The toxic effects on microbial communities are highly dependent on the type of nanoparticles considered. Inorganic nanoparticles (metal and metal oxide) seem to have a greater toxic potential than organic nanoparticles (fullerenes and carbon nanotubes) on soil microorganisms. Detrimental effects of metal and metal oxide nanoparticles on microbial activity, abundance, and diversity have been demonstrated, even for very low concentrations (<1 mg kg−1). On the opposite, the negative effects of carbon nanoparticles are observed only in presence of high concentrations (>250 mg kg−1), representing a worst case scenario. Considering that most of the available literature has analyzed the impact of an acute contamination of nanoparticles using high concentrations in a single soil, several research needs have been identified, and new directions have been proposed. The effects of realistic concentrations of nanoparticles based on the concentrations predicted in modelization studies and chronic contaminations should be simulated. The influence of soil properties on the nanoparticle toxicity is still unknown and that is why it is crucial to consider the ecotoxicity of nanoparticles in a range of different soils. The identification of soil parameters controlling the bioavailability and toxicity of nanoparticles is fundamental for a better environmental risk assessment.

Keywords

Nanomaterials Microbial ecotoxicology Terrestrial ecosystem Soil pollution Risk assessment Nanoscale zero valent iron 

References

  1. Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519CrossRefGoogle Scholar
  2. Ben-Moshe T, Dror I, Berkowitz B (2010) Transport of metal oxide nanoparticles in saturated porous media. Chemosphere 81:387–393CrossRefGoogle Scholar
  3. Ben-Moshe T, Frenk S, Dror I, Minz D, Berkowitz B (2013) Effects of metal oxide nanoparticles on soil properties. Chemosphere 90:640–646CrossRefGoogle Scholar
  4. Brookes PC (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279CrossRefGoogle Scholar
  5. Chung H, Son Y, Yoon TK, Kim S, Kim W (2011) The effect of multi-walled carbon nanotubes on soil microbial activity. Ecotoxicol Environ Saf 74:569–575CrossRefGoogle Scholar
  6. Colman BP, Arnaout CL, Anciaux S, Gunsch CK, Hochella MF Jr, Kim B, Lowry GV, McGill BM, Reinsch BC, Richardson CJ, Unrine JM, Wright JP, Yin L, Bernhardt ES (2013) Low concentrations of silver nanoparticles in sewage sludge cause adverse ecosystem responses under realistic field scenario. PLoS ONE 8:e57189CrossRefGoogle Scholar
  7. Collins D, Luxton T, Kumar N, Shah S, Walker VK, Shah V (2012) Assessing the impact of copper and zinc oxide nanoparticles on soil: A field study. PLoS ONE 7:e42663CrossRefGoogle Scholar
  8. Cornelis G, Pang L, Doolette C, Kirby JK, McLaughlin MJ (2013) Transport of silver nanoparticles in saturated columns of natural soils. Sci Total Environ 463:120–130CrossRefGoogle Scholar
  9. Cornelis G, Hund-Rinke K, Kuhlbusch T, Van den Brink N, Nickel C (2014) Fate and bioavailability of engineered nanoparticles in soils: a review. Crit Rev Environ Sci Technol 44:2720–2764CrossRefGoogle Scholar
  10. Cullen LG, Tilston EL, Mitchell GR, Collins CD, Shaw LJ (2011) Assessing the impact of nano-and micro-scale zerovalent iron particles on soil microbial activities: particle reactivity interferes with assay conditions and interpretation of genuine microbial effects. Chemosphere 82:1675–1682CrossRefGoogle Scholar
  11. Dinesh R, Anandaraj M, Srinivasan V, Hamza S (2012) Engineered nanoparticles in the soil and their potential implications to microbial activity. Geoderma 173:19–27CrossRefGoogle Scholar
  12. Du WC, Sun YY, Ji R, Zhu JG, Wu JC, Guo HY (2011) TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. J Environ Monit 13:822–828CrossRefGoogle Scholar
  13. Fabrega J, Fawcett SR, Renshaw JC, Lead JR (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290CrossRefGoogle Scholar
  14. Fajardo C, Ortíz LT, Rodríguez-Membibre ML, Nande M, Lobo MC, Martin M (2012) Assessing the impact of zero-valent iron (ZVI) nanotechnology on soil microbial structure and functionality: A molecular approach. Chemosphere 86:802–808CrossRefGoogle Scholar
  15. Fang J, Shan XQ, Wen B, Lin JM, Owens G (2009) Stability of titania nanoparticles in soil suspensions and transport in saturated homogeneous soil columns. Environ Pollut 157:1101–1109CrossRefGoogle Scholar
  16. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631CrossRefGoogle Scholar
  17. Ge YG, Schimel JP, Holden PA (2011) Evidence for negative effects of TiO2 and ZnO nanoparticles on soil bacterial communities. Environ Sci Technol 45:1659–1664CrossRefGoogle Scholar
  18. Ge YG, Schimel JP, Holden PA (2012) Identification of soil bacteria susceptible to TiO2 and ZnO nanoparticles. Appl Environ Microbiol 78:6749–6758CrossRefGoogle Scholar
  19. Ge YG, Priester JH, Van De Werfhorst LC, Schimel JP, Holden PA (2013) Potential Mechanisms and Environmental Controls of TiO2 Nanoparticle Effects on Soil Bacterial Communities. Environ Sci Technol 47:14411–14417CrossRefGoogle Scholar
  20. Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414CrossRefGoogle Scholar
  21. Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222CrossRefGoogle Scholar
  22. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129CrossRefGoogle Scholar
  23. Hänsch M, Emmerling C (2010) Effects of silver nanoparticles on the microbiota and enzyme activity in soil. J Plant Nutr Soil Sci 173:554–558CrossRefGoogle Scholar
  24. He S, Feng Y, Ren H, Zhang Y, Gu N, Lin X (2011) The impact of iron oxide magnetic nanoparticles on the soil bacterial community. J Soils Sediments 11:1408–1417CrossRefGoogle Scholar
  25. Holden PA, Schimel JP, Godwin HA (2014) Five reasons to use bacteria when assessing manufactured nanomaterial environmental hazards and fates. Curr Opin Biotechnol 27:73–78CrossRefGoogle Scholar
  26. Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano-and micro-scaled oxide particles. Environ Pollut 157:1619–1625CrossRefGoogle Scholar
  27. Jin L, Son Y, Yoon TK, Kang YJ, Kim W, Chung H (2013) High concentrations of single-walled carbon nanotubes lower soil enzyme activity and microbial biomass. Ecotoxicol Environ Saf 88:9–15CrossRefGoogle Scholar
  28. Jin L, Son Y, DeForest JL, Kang YJ, Kim W, Chung H (2014) Single-walled carbon nanotubes alter soil microbial community composition. Sci Total Environ 446:533–538CrossRefGoogle Scholar
  29. Johansen A, Pedersen AL, Jensen KA, Karlson U, Hansen BM, Scott‐Fordsmand JJ, Winding A (2008) Effects of C60 fullerene nanoparticles on soil bacteria and protozoans. Environ Toxicol Chem 27:1895–1903CrossRefGoogle Scholar
  30. Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400:396–414CrossRefGoogle Scholar
  31. Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306CrossRefGoogle Scholar
  32. Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15:1692CrossRefGoogle Scholar
  33. Khodakovskaya MV, Kim BS, Kim JN, Alimohammadi M, Dervishi E, Mustafa T, Cernigla CE (2013) Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small 9:115–123CrossRefGoogle Scholar
  34. Klaine SJ, Alvarez PJ, Batley GE, Fernandes TF, Handy RD, Lyon DY et al (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851CrossRefGoogle Scholar
  35. Kumar N, Shah V, Walker VK (2011) Perturbation of an arctic soil microbial community by metal nanoparticles. J Hazard Mater 190:816–822CrossRefGoogle Scholar
  36. Kumar N, Shah V, Walker VK (2012) Influence of a nanoparticle mixture on an arctic soil community. Environ Toxicol Chem 31:131–135CrossRefGoogle Scholar
  37. Lowry GV, Gregory KB, Apte SC, Lead JR (2012) Transformations of nanomaterials in the environment. Environ Sci Technol 46:6893–6899CrossRefGoogle Scholar
  38. Naja G, Apiratikul R, Pavasant P, Volesky B, Hawari J (2009) Dynamic and equilibrium studies of the RDX removal from soil using CMC-coated zerovalent iron nanoparticles. Environ Pollut 157:2405–2412CrossRefGoogle Scholar
  39. Neal AL (2008) What can be inferred from bacterium–nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles? Ecotoxicology 17:362–371CrossRefGoogle Scholar
  40. Nogueira V, Lopes I, Rocha-Santos T, Santos AL, Rasteiro GM, Antunes F, Gonçalves F, Soares AMVM, Cunha A, Almeida A, Gomes NNCM, Pereira R (2012) Impact of organic and inorganic nanomaterials in the soil microbial community structure. Sci Total Environ 424:344–350CrossRefGoogle Scholar
  41. Pan B, Xing B (2012) Applications and implications of manufactured nanoparticles in soils: a review. Eur J Soil Sci 63:437–456CrossRefGoogle Scholar
  42. Pawlett M, Ritz K, Dorey RA, Rocks S, Ramsden J, Harris JA (2013) The impact of zero-valent iron nanoparticles upon soil microbial communities is context dependent. Environ Sci Pollut Res 20:1041–1049CrossRefGoogle Scholar
  43. Peyrot C, Wilkinson KJ, Desrosiers M, Sauvé S (2014) Effects of silver nanoparticles on soil enzyme activities with and without added organic matter. Environ Toxicol Chem 33:115–125CrossRefGoogle Scholar
  44. Ranjard L, Richaume A, Jocteur‐Monrozier L, Nazaret S (1997) Response of soil bacteria to Hg (II) in relation to soil characteristics and cell location. FEMS Microbiol Ecol 24:321–331CrossRefGoogle Scholar
  45. Ranjard L, Richaume A (2001) Quantitative and qualitative microscale distribution of bacteria in soil. Res Microbiol 152:707–716CrossRefGoogle Scholar
  46. Robertson CE, Harris JK, Spear JR, Pace NR (2005) Phylogenetic diversity and ecology of environmental Archaea. Curr Opin Microbiol 8:638–642CrossRefGoogle Scholar
  47. Rodrigues DF, Jaisi DP, Elimelech M (2013) Toxicity of functionalized single-walled carbon nanotubes on soil microbial communities: implications for nutrient cycling in soil. Environ Sci Technol 47:625–633CrossRefGoogle Scholar
  48. Rousk J, Ackermann K, Curling SF, Jones DL (2012) Comparative toxicity of nanoparticulate CuO and ZnO to soil bacterial communities. PLoS ONE 7:e34197CrossRefGoogle Scholar
  49. Satapanajaru T, Anurakpongsatorn P, Pengthamkeerati P, Boparai H (2008) Remediation of atrazine-contaminated soil and water by nano zerovalent iron. Water Air Soil Pollut 192:349–359CrossRefGoogle Scholar
  50. Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488CrossRefGoogle Scholar
  51. Schloter M, Dilly O, Munch JC (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98:255–262CrossRefGoogle Scholar
  52. Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol. doi:10.3389/fmicb.2012.00348 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 197:143–148CrossRefGoogle Scholar
  54. Shah V, Collins D, Walker VK, Shah S (2014) The impact of engineered cobalt, iron, nickel and silver nanoparticles on soil bacterial diversity under field conditions. Environ Res Lett 9:024001CrossRefGoogle Scholar
  55. Shin YJ, Kwak JI, An YJ (2012) Evidence for the inhibitory effects of silver nanoparticles on the activities of soil exoenzymes. Chemosphere 88:524–529CrossRefGoogle Scholar
  56. Shrestha B, Acosta-Martinez V, Cox SB, Green MJ, Li S, Cañas-Carrell JE (2013) An evaluation of the impact of multiwalled carbon nanotubes on soil microbial community structure and functioning. J Hazard Mater 261:188–197CrossRefGoogle Scholar
  57. Simon-Deckers A, Loo S, Mayne-L’hermite M, Herlin-Boime N, Menguy N, Reynaud C et al (2009) Size-, composition-and shape-dependent toxicological impact of metal oxide nanoparticles and carbon nanotubes toward bacteria. Environ Sci Technol 43:8423–8429CrossRefGoogle Scholar
  58. Simonin M, Guyonnet JP, Martins JMF, Ginot M, Richaume A (2014) Influence of soil properties on the toxicity of TiO2 nanoparticles on carbon mineralization and bacterial abundance. J Hazard Mater. doi:10.1016/j.jhazmat.2014.10.004 Google Scholar
  59. Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76CrossRefGoogle Scholar
  60. Thio BJR, Zhou D, Keller AA (2011) Influence of natural organic matter on the aggregation and deposition of titanium dioxide nanoparticles. J Hazard Mater 189:556–563CrossRefGoogle Scholar
  61. Tilston EL, Collins CD, Mitchell GR, Princivalle J, Shaw LJ (2013) Nanoscale zerovalent iron alters soil bacterial community structure and inhibits chloroaromatic biodegradation potential in Aroclor 1242-contaminated soil. Environ Pollut 173:38–46CrossRefGoogle Scholar
  62. Tong Z, Bischoff M, Nies L, Applegate B, Turco RF (2007) Impact of fullerene (C60) on a soil microbial community. Environ Sci Technol 41:2985–2991CrossRefGoogle Scholar
  63. Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245CrossRefGoogle Scholar
  64. Tourinho PS, Van Gestel CA, Lofts S, Svendsen C, Soares AM, Loureiro S (2012) Metal‐based nanoparticles in soil: Fate, behavior, and effects on soil invertebrates. Environ Toxicol Chem 31:1679–1692CrossRefGoogle Scholar
  65. Vittori Antisari L, Carbone S, Gatti A, Vianello G, Nannipieri P (2013) Toxicity of metal oxide (CeO2, Fe3O4, SnO2) engineered nanoparticles on soil microbial biomass and their distribution in soil. Soil Biol Biochem 60:87–94CrossRefGoogle Scholar
  66. Wang Y, Gao B, Morales VL, Tian Y, Wu L, Gao J, Yang L (2012) Transport of titanium dioxide nanoparticles in saturated porous media under various solution chemistry conditions. J Nanopart Res 14:1–9Google Scholar
  67. Xia T, Kovochich M, Liong M, Mädler L, Gilbert B et al (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2:2121–2134CrossRefGoogle Scholar
  68. Zhang L-M, Offre PR, He J-Z, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U S A 107:17240–17245CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Université de LyonLyonFrance
  2. 2.Université Claude Bernard Lyon 1VilleurbanneFrance
  3. 3.Microbial Ecology, CNRS, UMR 5557Université Lyon 1VilleurbanneFrance
  4. 4.LTHE, UMR 5564, UJF-Grenoble/CNRS-INSU/G-INP/IRDGrenobleFrance

Personalised recommendations