Effects of metal oxide nanoparticles on soil enzyme activities and bacterial communities in two different soil types

PurposeWith the increased availability of nanoparticle-based products, their releases to soil are undoubtedly inevitable. Among the nanoparticle-based products, potential risks of metal oxide nanoparticles (MO-ENPs) have attracted increasing concerns. However, their effects on soil and soil microorganisms remain largely unknown.Materials and methodsIn this study, four metal oxide nanoparticles, i.e., zinc oxide nanoparticles (nZnO), titanium dioxide nanoparticles (nTiO2), cerium dioxide nanoparticles (nCeO2), and magnetite nanoparticles (nFe3O4), were enrolled to evaluate their impact on soil enzyme activities (invertase, urease, catalase, and phosphatase) and bacterial communities in two typical soils from northeast China (black soil and saline-alkali soil). The community structure and size were analyzed using pyrosequencing and real-time polymerase chain reaction (RT-PCR). The soils were exposed to metal oxide nanoparticles at 0.5, 1.0, and 2.0 mg g−1 for 15 and 30 days.Results and discussionIn general, nZnO had a stronger effect on soil enzymatic activities than nTiO2, nCeO2, and nFe3O4, and saline-alkali soil was more susceptible to metal oxide nanoparticles than black soil. In RT-PCR analysis, a significant decrease (41.66, 36.34, and 47.99%, respectively) on total bacteria population was only observed in saline-alkali soil treated by 0.5, 1.0, and 2.0 mg g−1 nZnO. Meanwhile, pyrosequencing analysis revealed that the samples of saline-alkali soil treated with nZnO showed high variance in their bacterial community composition, e.g., Bacilli, Alphaproteobacteria, and Gammaproteobacteria class.ConclusionsThe results suggested that metal oxide nanoparticle incubation could influence soil enzyme activities and change soil bacterial community. Moreover, the soil type was a key component dictating the effect of metal oxide nanoparticles on the bacterial community composition and size. These findings are of great help towards building a comprehensive understanding of the potential environmental risks of metal oxide nanoparticles.

[1]  Rebecca Klaper,et al.  Behavioral and physiological changes in Daphnia magna when exposed to nanoparticle suspensions (titanium dioxide, nano- , 2008 .

[2]  R. Pini,et al.  CHEMICAL AND PHYSICAL PROPERTIES OF SOIL INFLUENCING TiO 2 NANOPARTICLES AVAILABILITY IN TERRESTRIAL ECOSYSTEMS , 2012 .

[3]  Janeck J Scott-Fordsmand,et al.  Effects of C60 fullerene nanoparticles on soil bacteria and protozoans , 2008, Environmental toxicology and chemistry.

[4]  Gabriele Berg,et al.  The ignored diversity: complex bacterial communities in intensive care units revealed by 16S pyrosequencing , 2013, Scientific Reports.

[5]  F. Schinner,et al.  Xylanase-, CM-cellulase- and invertase activity in soil: An improved method , 1990 .

[6]  Rebecca Klaper,et al.  Behavioral and physiological changes in Daphnia magna when exposed to nanoparticle suspensions (titanium dioxide, nano-C60, and C60HxC70Hx). , 2007, Environmental science & technology.

[7]  M. Sastry,et al.  Bacterial aerobic synthesis of nanocrystalline magnetite. , 2005, Journal of the American Chemical Society.

[8]  Yunqing Kang,et al.  Toxicological effect of ZnO nanoparticles based on bacteria. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[9]  Toshifumi Sakaguchi,et al.  Magnetite formation by a sulphate-reducing bacterium , 1993, Nature.

[10]  Pedro J J Alvarez,et al.  Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. , 2006, Water research.

[11]  Kerstin Hund-Rinke,et al.  Ecotoxic Effect of Photocatalytic Active Nanoparticles (TiO2) on Algae and Daphnids (8 pp) , 2006, Environmental science and pollution research international.

[12]  Robert A Hoke,et al.  Development of a base set of toxicity tests using ultrafine TiO2 particles as a component of nanoparticle risk management. , 2007, Toxicology letters.

[13]  Rıdvan Kızılkaya,et al.  Effects of N-enriched sewage sludge on soil enzyme activities , 2005 .

[14]  W. Dick,et al.  Soil acid and alkaline phosphatase activity as pH adjustment indicators , 2000 .

[15]  Yong-guan Zhu,et al.  Resistance and resilience of Cu-polluted soil after Cu perturbation, tested by a wide range of soil microbial parameters. , 2009, FEMS microbiology ecology.

[16]  Patrick D. Schloss,et al.  Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies , 2011, PloS one.

[17]  N. Tam,et al.  Illumina Sequencing of 16S rRNA Tag Revealed Spatial Variations of Bacterial Communities in a Mangrove Wetland , 2013, Microbial Ecology.

[18]  J. Peralta-Videa,et al.  Physiological and biochemical responses of sunflower (Helianthus annuus L.) exposed to nano-CeO2 and excess boron: Modulation of boron phytotoxicity. , 2017, Plant physiology and biochemistry : PPB.

[19]  R. Knight,et al.  Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau , 2012, Environmental microbiology.

[20]  B. Berkowitz,et al.  Effect of Metal Oxide Nanoparticles on Microbial Community Structure and Function in Two Different Soil Types , 2013, PloS one.

[21]  B. Berkowitz,et al.  Effects of metal oxide nanoparticles on soil properties. , 2013, Chemosphere.

[22]  Milton Sommerfeld,et al.  Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. , 2008, Chemosphere.

[23]  Wei Jiang,et al.  Bacterial toxicity comparison between nano- and micro-scaled oxide particles. , 2009, Environmental pollution.

[24]  Yoram Cohen,et al.  The University of California Center for the Environmental Implications of Nanotechnology. , 2009, Environmental science & technology.

[25]  V. Shah,et al.  Perturbation of an arctic soil microbial community by metal nanoparticles. , 2011, Journal of hazardous materials.

[26]  Michael A. Wilson,et al.  Nanomaterials in soils , 2008 .

[27]  J. Chen,et al.  Assessment of the Phytotoxicity of Metal Oxide Nanoparticles on Two Crop Plants, Maize (Zea mays L.) and Rice (Oryza sativa L.) , 2015, International journal of environmental research and public health.

[28]  D. Chittleborough,et al.  Solubility and batch retention of CeO2 nanoparticles in soils. , 2011, Environmental science & technology.

[29]  Jamie R. Lead,et al.  Aquatic Colloids and Nanoparticles: Current Knowledge and Future Trends , 2006 .

[30]  B. Griffiths,et al.  The Relationship between Microbial Community Structure and Functional Stability, Tested Experimentally in an Upland Pasture Soil , 2002, Microbial Ecology.

[31]  José Adilson de Castro,et al.  Modeling the Transport Phenomena of TiO2 Nanoparticles into Leachate of Municipal Waste Landfills , 2012 .

[32]  Anne Kahru,et al.  Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. , 2008, Chemosphere.

[33]  P. Trebše,et al.  Comparative toxicity of chlorpyrifos and its oxon derivatives to soil microbial activity by combined methods. , 2010, Chemosphere.

[34]  Kevin Robbie,et al.  Nanomaterials and nanoparticles: Sources and toxicity , 2007, Biointerphases.

[35]  Yan Li,et al.  Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage , 2008, Journal of environmental science and health. Part A, Toxic/hazardous substances & environmental engineering.

[36]  Jamie R Lead,et al.  Nanomaterials in the environment: Behavior, fate, bioavailability, and effects , 2008, Environmental toxicology and chemistry.

[37]  Jun Yao,et al.  The Effect of Metal Oxide Nanoparticles on Functional Bacteria and Metabolic Profiles in Agricultural Soil , 2015, Bulletin of Environmental Contamination and Toxicology.

[38]  N. Qafoku Chapter Two - Terrestrial Nanoparticles and Their Controls on Soil-/Geo-Processes and Reactions , 2010 .

[39]  Wenchao Du,et al.  TiO2 and ZnO nanoparticles negatively affect wheat growth and soil enzyme activities in agricultural soil. , 2011, Journal of environmental monitoring : JEM.

[40]  G. E. Gadd,et al.  Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. , 2007, Environmental science & technology.

[41]  Yuan Ge,et al.  Identification of Soil Bacteria Susceptible to TiO2 and ZnO Nanoparticles , 2012, Applied and Environmental Microbiology.

[42]  F. Eivazi,et al.  Factors affecting glucosidase and galactosidase activities in soils , 1990 .

[43]  I. Mackinnon,et al.  Bismuth oxide nanoparticles in the stratosphere , 1997 .

[44]  Yuan Ge,et al.  Evidence for negative effects of TiO2 and ZnO nanoparticles on soil bacterial communities. , 2011, Environmental science & technology.

[45]  byBrooke LaBranche,et al.  Comparative eco-toxicity of nanoscale TiO 2 , SiO 2 , and ZnO water suspensions , 2017 .

[46]  Peng Wang,et al.  Urease, invertase, dehydrogenase and polyphenoloxidase activities in paddy soil influenced by allelopathic rice variety , 2009 .

[47]  Mark Crane,et al.  The ecotoxicology and chemistry of manufactured nanoparticles , 2008, Ecotoxicology.

[48]  R. Andreazza,et al.  Evaluation of copper resistant bacteria from vineyard soils and mining waste for copper biosorption , 2011, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[49]  Loring Nies,et al.  Impact of fullerene (C60) on a soil microbial community. , 2007, Environmental science & technology.

[50]  Ning Gu,et al.  The impact of iron oxide magnetic nanoparticles on the soil bacterial community , 2011 .

[51]  W. Stark,et al.  Graphene-stabilized copper nanoparticles as an air-stable substitute for silver and gold in low-cost ink-jet printable electronics , 2008, Nanotechnology.

[52]  Liu Guangming Characteristics and Agro-Biological Management of Saline-Alkalized Land in Northeast China , 2006 .

[53]  Virginia K. Walker,et al.  Assessing the Impact of Copper and Zinc Oxide Nanoparticles on Soil: A Field Study , 2012, PloS one.

[54]  R. Knight,et al.  Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data , 2009, The ISME Journal.

[55]  M. Benedetti,et al.  Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. , 2006, Nano letters.

[56]  G. Lowry,et al.  Role of Particle Size and Soil Type in Toxicity of Silver Nanoparticles to Earthworms , 2011 .

[57]  I. Burke,et al.  Carbon fluxes, nitrogen cycling, and soil microbial communities in adjacent urban, native and agricultural ecosystems , 2005 .

[58]  S. Simeoni,et al.  Effect of nanoparticle encapsulation on the photostability of the sunscreen agent, 2-ethylhexyl-p-methoxycinnamate. , 2002, International journal of pharmaceutics.

[59]  C. Desai,et al.  Evaluation of in vitro Cr(VI) reduction potential in cytosolic extracts of three indigenous Bacillus sp. isolated from Cr(VI) polluted industrial landfill. , 2008, Bioresource technology.

[60]  G. Lowry,et al.  Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. , 2009, Nature nanotechnology.

[61]  P. Nannipieri,et al.  Use of enzymes to detoxify pesticide-contaminated soils and waters , 1991 .

[62]  Jianguo Zhu,et al.  Free-air CO2 enrichment (FACE) enhances the biodiversity of purple phototrophic bacteria in flooded paddy soil , 2009, Plant and Soil.

[63]  M Boller,et al.  Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. , 2008, Environmental pollution.

[64]  Hongwen Sun,et al.  Immobilization of cadmium in soils by UV-mutated Bacillus subtilis 38 bioaugmentation and NovoGro amendment. , 2009, Journal of hazardous materials.

[65]  E. Roduner Size matters: why nanomaterials are different. , 2006, Chemical Society reviews.

[66]  F. Achuba,et al.  Effect of spent engine oil on soil catalase and dehydrogenase activities , 2008 .

[67]  Baoshan Xing,et al.  Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. , 2009, Environmental pollution.