Skip to main content
Log in

Effects of PVP-coated silver nanoparticles on enzyme activity, bacterial and archaeal community structure and function in a yellow-brown loam soil

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The undesirable effects of silver nanoparticles (AgNPs) on soil environment have caused much concern. The previous studies, however, focused on sandy soil, with little known on others. In present study, the effects of polyvinylpyrrolidone-coated AgNPs (0, 1, 10, and 100 mg kg− 1 soil) on enzyme activities (urease and dehydrogenase), ammonia-oxidizing bacteria (AOB) and archaea (AOA), bacterial and archaeal communities, and microbial function profile in a yellow-brown loam soil were investigated. The significant dose-response inhibitions of AgNPs on enzyme activities were observed, with dehydrogenase more susceptible to AgNPs. Both of bacterial and archaeal amoA genes were reduced by AgNPs above 10 mg kg− 1, with AOB more susceptible to AgNPs than AOA. AgNPs at 100 mg kg− 1 caused reductions on the dominant Nitrosospira and Nitrosomonas, and even disappearance on Nitrosovibrio, while increase on Nitrososphaera significantly. AgNPs also changed bacterial and archaeal community structure. Exposure to AgNPs at 100 mg kg− 1 caused significant increases by 186.79% and 44.89% for Bacteroidetes and Proteobacteria, while decreases by 47.82%, 44.09%, 43.67%, and 80.44% for Actinobacteria, Chloroflexi, Planctomycetes, and Verrucomicrobia, respectively. Moreover, three dominant archaeal phyla (Thaumarchaeota, Euryarchaeota, and Parvarchaeota) were also reduced in the presence of AgNPs, especially Thaumarchaeota with the significant reduction of 13.71%. PICRUSt prediction revealed that AgNPs indeed had the potential to change soil microbial community’s functional contributions. It must be cautious on the interference of AgNPs to soil ecological functions in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arnaout CL, Gunsch CK (2012) Impacts of silver nanoparticle coating on the nitrification potential of Nitrosomonas europaea. Environ Sci Technol 46(10):5387–5395

    Article  CAS  Google Scholar 

  • Auvinen H, Sepúlveda VV, Rousseau DPL, Du Laing G (2016) Substrate -and plant-mediated removal of citrate-coated silver nanoparticles in constructed wetlands. Environ Sci Pollut Res 23:21920–21926

    Article  CAS  Google Scholar 

  • Baranwal A, Srivastava A, Kumar P, Bajpai VK, Maurya PK, Chandra P (2018) Prospects of nanostructure materials and their composites as antimicrobial agents. Front Microbiol 9

  • Beddow J, Stolpe B, Cole PA, Lead JR, Sapp M, Lyons BP, Colbeck I, Whitby C (2017) Nanosilver inhibits nitrification and reduces ammonia-oxidising bacterial but not archaeal amoA gene abundance in estuarine sediments. Environ Microbiol 19:500–510

    Article  CAS  Google Scholar 

  • Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139

    Article  CAS  Google Scholar 

  • Button M, Auvinen H, Van Koetsem F, Hosseinkhani B, Rousseau D, Weber KP, Du Laing G (2016) Susceptibility of constructed wetland microbial communities to silver nanoparticles: a microcosm study. Ecol Eng 97:476–485

    Article  Google Scholar 

  • Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34:171–198

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 44:2720–2764

    Article  CAS  Google Scholar 

  • Dick RP (1994) Soil enzyme activities as indicators of soil quality. Soil Sci Soc Am J 58:107–124

    Google Scholar 

  • Dunfield PF, Yurgey AQ, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y, Wang J, Mountain BW, Crowe MA, Weatherby TM, Bodelier PLE, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–882

    Article  CAS  Google Scholar 

  • Eivazi F, Afrasiabi Z, Jose E (2018) Effects of silver nanoparticles on the activities of soil enzymes involved in carbon and nutrient cycling. Pedosphere 28:209–214

    Article  Google Scholar 

  • Farid M, Ali S, Zubair M, Saeed R, Rizwan M, Sallah-Ud-Din R, Azam A, Ashraf R, Ashraf W (2018) Glutamic acid assisted phyto-management of silver-contaminated soils through sunflower; physiological and biochemical response. Environ Sci Pollut Res 25:25390–25400

    Article  CAS  Google Scholar 

  • Garcia-Gomez C, Fernandez MD, Garcia S, Obrador AF, Leton M, Babin M (2018) Soil pH effects on the toxicity of zinc oxide nanoparticles to soil microbial community. Environ Sci Pollut Res 25:28140–28152

    Article  CAS  Google Scholar 

  • Gong P (1997) Dehydrogenase activity in soil: a comparison between the TTC and INT assay under their optimum conditions. Soil Biol Biochem 29:211–214

    Article  CAS  Google Scholar 

  • 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 43:9216–9222

    Article  CAS  Google Scholar 

  • Grün A, Emmerling C (2018) Long-term effects of environmentally relevant concentrations of silver nanoparticles on major soil bacterial phyla of a loamy soil. Environ Sci Eur 30:31

    Article  CAS  Google Scholar 

  • Grün A, Straskraba S, Schulz S, Schloter M, Emmerling C (2018) Long-term effects of environmentally relevant concentrations of silver nanoparticles on microbial biomass, enzyme activity, and functional genes involved in the nitrogen cycle of loamy soil. J Environ Sci 69:12–22

    Article  Google Scholar 

  • Gu L, Li Q, Quan X, Cen Y, Jiang X (2014) Comparison of nanosilver removal by flocculent and granular sludge and short- and long-term inhibition impacts. Water Res 58:62–70

    Article  CAS  Google Scholar 

  • Guo Z, Chen G, Liu L, Zeng G, Huang Z, Chen A, Hu L (2016) Activity variation of Phanerochaete chrysosporium under nanosilver exposure by controlling of different sulfide sources. Sci Rep 6:20813

    Article  CAS  Google Scholar 

  • Hänsch M, Emmerling C (2010) Effects of silver nanoparticles on the microbiota and enzyme activity in soil. J Plant Nutr Soil Sci 173:554–558

    Article  CAS  Google Scholar 

  • He S, Feng Y, Ni J, Sun Y, Xue L, Feng Y, Yu Y, Lin X, Yang L (2016) Different responses of soil microbial metabolic activity to silver and iron oxide nanoparticles. Chemosphere 147:195–202

    Article  CAS  Google Scholar 

  • Holden PA, Schimel JP, Godwin HA (2014) Five reasons to use bacteria when assessing manufactured nanomaterial environmental hazards and fates. Curr Opin Biotech 27:73–78

    Article  CAS  Google Scholar 

  • Huang J, Cao C, Li RQ, Guan WZ (2018) Effects of silver nanoparticles on soil ammonia-oxidizing microorganisms under temperatures of 25 and 5 °C. Pedosphere 28:607–616

    Article  Google Scholar 

  • Kaegi R, Sinnet B, Zuleeg S, Hagendorfer H, Mueller E, Vonbank R, Boller M, Burkhardt M (2010) Release of silver nanoparticles from outdoor facades. Environ Pollut 158(9):2900–2905

    Article  CAS  Google Scholar 

  • Kalyuhznaya MG, Martens-Habbena W, Wang T, Hackett M, Stolyar SM, Stahl DA, Lidstrom ME, Chistoserdova L (2009) Methylophilaceae link methanol oxidation to denitrification in freshwater lake sediment as suggested by stable isotope probing and pure culture analysis. Environ Microbiol Rep 1:385–392

    Article  CAS  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  CAS  Google Scholar 

  • Li M, Liang Z, Callier MD, d'Orbcastel ER, Ma X, Sun L, Li X, Wang S, Song X, Liu Y (2018) Nitrogen and organic matter removal and enzyme activities in constructed wetlands operated under different hydraulic operating regimes. Aquaculture 496:247–254

    Article  CAS  Google Scholar 

  • Li H, Chi Z, Yan B (2019) Long-term impacts of graphene oxide and Ag nanoparticles on anammox process: performance, microbial community and toxic mechanism. J Environ Sci 79:239–247

    Article  Google Scholar 

  • Liu X, Yang X, Hu X, He Q, Zhai J, Chen Y, Xiong Q, Vymazal J (2019) Comprehensive metagenomic analysis reveals the effects of silver nanoparticles on nitrogen transformation in constructed wetlands. Chem Eng J 358:1552–1560

    Article  CAS  Google Scholar 

  • Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun HZ, Tam P, Chiu JF, Che CM (2006) Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J Proteome Res 5:916–924

    Article  CAS  Google Scholar 

  • Marti M, Juottonen H, Robroek B, Yrjala K, Danielsson A, Lindgren PE, Svensson BH (2015) Nitrogen and methanogen community composition within and among three Sphagnum dominated peatlands in Scandinavia. Soil Biol Biochem 81:204–211

    Article  CAS  Google Scholar 

  • McBride MJ, Liu W, Lu X, Zhu Y, Zhang W (2014) The family Cytophagaceae, 4th edn. Springer Reference, London, pp 577–593

    Google Scholar 

  • McGee CF, Storey S, Clipson N, Doyle E (2017) Soil microbial community responses to contamination with silver, aluminium oxide and silicon dioxide nanoparticles. Ecotoxicology 26:449–458

    Article  CAS  Google Scholar 

  • McGee CF, Storey S, Clipson N, Doyle E (2018) Concentration-dependent responses of soil bacterial, fungal and nitrifying communities to silver nano and micron particles. Environ Sci Pollut Res 25:18693–18704

    Article  CAS  Google Scholar 

  • Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353

    Article  CAS  Google Scholar 

  • Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S, Hemp A, Kalko EKV, Linsenmair KE, Pfeiffer S, Renner S, Schöning I, Weisser WW, Wells K, Fischer M, Overmann J, Friedrich MW (2012) Environmental factors affect Acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406

    Article  CAS  Google Scholar 

  • Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627

    Article  CAS  Google Scholar 

  • Nemergut DR, Martin AP, Schmidt SK (2004) Integron diversity in heavy-metal-contaminated mine tailings and inferences about integron evolution. Appl Environ Microbiol 70(2):1160–1168

    Article  CAS  Google Scholar 

  • Nilgiriwala KS, Alahari A, Rao AS, Apte SK (2008) Cloning and overexpression of alkaline phosphatase PhoK from Sphingomonas sp. strain BSAR-1 for bioprecipitation of uranium from alkaline solutions. Appl Environ Microbiol 74(17):5516–5523

    Article  CAS  Google Scholar 

  • Pester M, Rattei T, Flechl S, Grongroft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539

    Article  CAS  Google Scholar 

  • 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 33:115–125

    Article  CAS  Google Scholar 

  • Rahmatpour S, Shirvani M, Mosaddeghi MR, Nourbakhsh F, Bazarganipour M (2017) Dose-response effects of silver nanoparticles and silver nitrate on microbial and enzyme activities in calcareous soils. Geoderma 285:313–322

    Article  CAS  Google Scholar 

  • Reidy B, Haase A, Luch A, Dawson KA, Lynch I (2013) Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 6:2295–2350

    Article  CAS  Google Scholar 

  • Samarajeewa AD, Velicogna JR, Princz JI, Subasinghe RM, Scroggins RP, Beaudette LA (2017) Effect of silver nano-particles on soil microbial growth, activity and community diversity in a sandy loam soil. Environ Pollut 220:504–513

    Article  CAS  Google Scholar 

  • Sheng Z, Liu Y (2017) Potential impacts of silver nanoparticles on bacteria in the aquatic environment. J Environ Manag 191:290–296

    Article  CAS  Google Scholar 

  • Shin Y, Kwak JI, An Y (2012) Evidence for the inhibitory effects of silver nanoparticles on the activities of soil exoenzymes. Chemosphere 88:524–529

    Article  CAS  Google Scholar 

  • Simonin M, Richaume A (2015) Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environ Sci Pollut Res 22:13710–13723

    Article  CAS  Google Scholar 

  • Sinsabaugh RS (1994) Enzymic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74

    Article  CAS  Google Scholar 

  • Sun TY, Gottschalk F, Hungerbühler K, Nowack B (2014) Comprehensive probabilistic modelling of environmental emissions of engineered nanomaterials. Environ Pollut 185:69–76

    Article  CAS  Google Scholar 

  • Sutcliffe IC (2011) Cell envelope architecture in the Chloroflexi: a shifting frontline in a phylogenetic turf war. Environ Microbiol 13(2):279–282

    Article  Google Scholar 

  • Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI (2016) Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol 92(7):w91

    Article  CAS  Google Scholar 

  • Tiede K, Hassellov M, Breitbarth E, Chaudhry Q, Boxall A (2009) Considerations for environmental fate and ecotoxicity testing to support environmental risk assessments for engineered nanoparticles. J Chromatogr A 1216:503–509

    Article  CAS  Google Scholar 

  • Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M (2010) An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 408:999–1006

    Article  CAS  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Konneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425

    Article  CAS  Google Scholar 

  • Unine JM, Colman BP, Bone AJ, Gondikas AP, Matson CW (2012) Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of Ag nanoparticles. Part 1. Aggregation and dissolution. Environ Sci Technol 46:6915–6924

    Article  CAS  Google Scholar 

  • Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A, Hemp J, Hügler M, Karr EA, Könneke M, Shin M, Lawton TJ, Lowe T, MartensHabbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci U S A 107:8818–8823

    Article  CAS  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, Deboy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, GwinnGiglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren QH, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu CH, Zafar N, Zhou LW, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  CAS  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Nat Acad Sci U S A 74:5088–5090

    Article  CAS  Google Scholar 

  • Wu Y, Ke X, Hernández M, Wang B, Dumont MG, Jia Z, Conrad R (2013) Autotrophic growth of bacterial and archaeal ammonia oxidizers in freshwater sediment microcosms incubated at different temperatures. Appl Environ Microbiol 79:3076–3084

    Article  CAS  Google Scholar 

  • Zeng JW, Xu P, Chen GQ, Zeng GM, Chen AW, Hu L, Huang ZZ, He K, Guo Z, Liu WW, Wu J, Shi JB (2019) Effects of silver nanoparticles with different dosing regimens and exposure media on artificial ecosystem. J Environ Sci 75:181–192

    Article  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. Isme J 6:1032

    Article  CAS  Google Scholar 

  • Zhang C, Liang Z, Hu Z (2014) 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 50:350–358

    Article  CAS  Google Scholar 

  • Zhao J, Li YQ, Pan S, Tu QQ, Dang WY, Wang Z, Zhu HT (2018) Effects of magnesium chloride on the anaerobic digestion and the implication on forward osmosis membrane bioreactor for sludge anaerobic digestion. Bioresour Technol 268:700–707

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by the National Natural Science Foundation of China (No. 51479034 and No.51650410657), Fundamental Research Funds for the Central Universities (No.2242019 K40064), and Postgraduate Research & Practice Innovation Program of Jiangsu Province (No. KYCX19_0096).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Huang.

Additional information

Responsible editor: Thomas D. Bucheli

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 655 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, C., Huang, J., Cao, C. et al. Effects of PVP-coated silver nanoparticles on enzyme activity, bacterial and archaeal community structure and function in a yellow-brown loam soil. Environ Sci Pollut Res 27, 8058–8070 (2020). https://doi.org/10.1007/s11356-019-07347-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-07347-5

Keywords

Navigation