Skip to main content
SpringerLink
Log in

Insights on the effects of ZnO nanoparticle exposure on soil heterotrophic respiration as revealed by soil microbial communities and activities

  • Soils, Sec 4 • Ecotoxicology • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The information on the effects of ZnONPs on soil biological processes and the resulting changes of ecosystem function is limited in wheat straw return agricultural soil. This study investigated the effects of ZnONPs on soil heterotrophic respiration and biochemical properties in wheat straw return farmland soil.

Materials and methods

An 84-day microcosm incubation experiment was implemented after the exposure of different doses of ZnONPs (0, 100, and 500 mg kg−1 dry soil) in a greenhouse under the temperature of 25 ± 3 °C. Soil heterotrophic respiration and soil enzyme activities were detected. Microbial community composition and diversity were analyzed by Illumina MiSeq platform.

Results and discussion

Heterotrophic respiration was significantly inhibited by ZnONPs at 500 mg kg−1. The activities of β-glucosidase, cellulose, and cellobiohydrolase decreased under high-level exposure of ZnONPs. The labile Zn2+ assimilated by soil microorganism was increased by 331% and 707%, respectively. Bacterial communities in the soil are more sensitive to ZnONPs than fungal ones. The changes of heterotrophic respiration were closely correlated with soil pH values and microbial compositions, especially fungal communities. Although ascomycetes were inhibited by ZnONPs, their abundance was the highest within soil fungal community.

Conclusions

The inhibition of heterotrophic respiration was associated with the variation of soil fungal communities, although the bacterial communities are sensitive to ZnONPs. The microbiome modulation is necessary for the management of the decomposition of returned wheat straw in the field contaminated by ZnONPs. The effects of ZnONPs on soil ecological process should be considered when the application of fertilizers and pesticides which contain ZnONPs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, Vetrovsky T, Zifcakova L, Snajdr J, Ridl J, Vlcek C, Voriskova J (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6:248–258

    Article  CAS  Google Scholar 

  • Ben-Moshe T, Frenk S, Dror I, Minz D, Berkowitz B (2013) Effects of metal oxide nanoparticles on soil properties. Chemosphere 90:640–646

  • Briones MJ, Elias DMO, Grant HK, McNamara NP (2019) Plant identity control on soil food web structure and C transfers under perennial bioenergy plantations. Soil Biol Biochem 138:107603

    Article  CAS  Google Scholar 

  • Chen ZM, Wang HY, Liu XW, Zhao XL, Lu DJ, Zhou JM, Li CZ (2017) Changes in soil microbial community and organic carbon fractions under short-term straw return in a rice–wheat cropping system. Soil Tillage Res 165:121–127

    Article  Google Scholar 

  • Chhipa H (2016) Nanofertilizers and nanopesticides for agriculture. Environ Chem Lett 15:1–8

    Google Scholar 

  • Collins D, Luxton T, Kumar N, Shah S, Virginia KW, Shah V (2012) Assessing the impact of copper and zinc oxide nanoparticles on soil: a field study. PLoS One 7:e42663

    Article  CAS  Google Scholar 

  • Du JJ, Zhang YY, Liu LN, Qv MX, Lv YN, Yin YF, Zhou YF, Cui MH, Zhu YF, Zhang HZ (2017a) Can visible light impact litter decomposition under pollution of ZnO nanoparticles? Chemosphere 187:368–375

    Article  CAS  Google Scholar 

  • Du JJ, Zhang YY, Cui MH, Yang JC, Lin ZD, Zhang HZ (2017b) Evidence for negative effects of ZnO nanoparticles on leaf litter decomposition in freshwater ecosystems. Environ Sci: Nano 4:2377–2387

  • Du JJ, Zhang YY, Guo W, Li NY, Gao CS, Cui MH, Lin ZD, Wei MB, Zhang HZ (2018) Chronic impacts of TiO2 nanoparticles on Populus nigra L. leaf decomposition in freshwater ecosystem. J Hazard Mater 350:121–127

    Article  CAS  Google Scholar 

  • Du JJ, Zhang YY, Guo R, Meng F, Gao Y, Ma C, Zhang HZ (2019) Harmful effect of nanoparticles on the functions of freshwater ecosystems: insight into nanoZnO-polluted stream. Chemosphere 214:830–838

    Article  CAS  Google Scholar 

  • Fadrosh DW, Bing M, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2:2–6

    Article  Google Scholar 

  • García-Gómez C, Babin M, Obrador A, Álvarez JM, Fernández MD (2015) Integrating ecotoxicity and chemical approaches to compare the effects of ZnO nanoparticles, ZnO bulk, and ZnCl2 on plants and microorganisms in a natural soil. Environ Sci Pollut Res 22(21):16803–16813

    Article  Google Scholar 

  • García-Gómez C, Fernández MD, García S, Obrador AF, Letón M, Babín M (2018) Soil pH effects on the toxicity of zinc oxide nanoparticles to soil microbial community. Environ Sci Pollut Res 25:28140–28152

    Article  Google Scholar 

  • García-Gómez C, García-Gutiérrez S, Obrador A, Fernandez MD (2020) Study of Zn availability, uptake, and effects on earthworms of zinc oxide nanoparticle versus bulk applied to two agricultural soils: acidic and calcareous. Chemosphere 239:124814

    Article  Google Scholar 

  • Ge Y, Schimel JP, Holden PA (2011) Evidence for negative effects of TiO2 and ZnO nanoparticles on soil bacterial communities. Environ Sci Technol 45:1659–1664

    Article  CAS  Google Scholar 

  • Ge Y, Schimel JP, Holden PA (2012) Identification of soil bacteria susceptible to TiO2 and ZnO nanoparticles. Appl Environ Microbiol 78:6749–6758

    Article  CAS  Google Scholar 

  • Guan SY (1983) Soil enzymes and their research methods. Agriculture Press, Beijing

    Google Scholar 

  • Guerriero G, Hausman JF, Strauss J, Ertan H, Siddiqui KS (2015) Destructuring plant biomass: focus on fungal and extremophilic cell wall hydrolases. Plant Sci 234:180–193

    Article  CAS  Google Scholar 

  • Hao Y, Ma CX, Zhang ZT, Song YH, Cao WD, Guo J, Zhou GP, Rui YK, Liu LM, Xing BS (2018) Carbon nanomaterials alter plant physiology and soil bacterial community composition in a rice-soil-bacterial ecosystem. Environ Pollut 232:123–136

    Article  CAS  Google Scholar 

  • Hao MM, Hu HY, Liu Z, Dong QQ, Sun K, Feng YP, Li G, Ning TY (2019) Shifts in microbial community and carbon sequestration in farmland soil under long-term conservation tillage and straw returning. Appl Soil Ecol 136:43–54

    Article  Google Scholar 

  • Hopkins DW, Shiel RS, O`donnell AG (1988) The influence of sward species composition on the rate of organic matter decomposition in grassland soil. J Soil Sci 39:385–392

    Article  Google Scholar 

  • Hou Z, Chen Z, Shen ZY, Li TT, Yang JJ, Lu XX (2014) Effects of zinc oxide nanoparticles on enzyme activities of soil microorganisms. J Agro-Environ Sci 33:1153–1158

    CAS  Google Scholar 

  • Ida K, Hanna F, Christian S, Paula P (2014) Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS One 9:e111786

    Article  Google Scholar 

  • Jośko I, Oleszczuk P, Futa B (2014) The effect of inorganic nanoparticles (ZnO, Cr2O3, CuO and Ni) and their bulk counterparts on enzyme activities in different soils. Geoderma 232-234:528–537

    Article  Google Scholar 

  • Jośko I, Oleszczuk P, Dobrzyńska J, Futa B, Joniec J, Dobrowolski R (2019) Long-term effect of ZnO and CuO nanoparticles on soil microbial community in different types of soil. Geoderma 352:204–212

    Article  Google Scholar 

  • Khan KS, Heinze S, Joergensen RG (2009) Simultaneous measurement of S, macronutrients, and heavy metals in the soil microbial biomass with CHCl3 fumigation and NH4NO3 extraction. Soil Biol Biochem 41:309–314

    Article  CAS  Google Scholar 

  • Kizildag N, Cenkseven S, Koca FD, Sagliker HA, Darici C (2019) How titanium dioxide and zinc oxide nanoparticles do affect soil microorganism activity? Eur J Soil Biol 91:18–24

    Article  CAS  Google Scholar 

  • Kwak JI, Yoon SJ, An YJ (2016) Long-term effects of ZnO nanoparticles on exoenzyme activities in planted soils. Environ Eng Res 22:224–229

    Article  Google Scholar 

  • Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota – a review. Soil Biol Biochem 43:1812–1836

    Article  CAS  Google Scholar 

  • Li Y (1983) The general analysis method of soil agricultural chemistry. Science Press, Beijing

    Google Scholar 

  • Li ZG, Luo YM, Teng Y (2008) Soil and environmental microbiology research. Science Press, Beijing

    Google Scholar 

  • Ma HB, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles--a review. Environ Pollut 172:76–85

    Article  CAS  Google Scholar 

  • Mohammad JZ, Nasrin K, Ebrahim MG, Amir G (2011) Effect of cropping systems and arbuscular mycorrhizal fungi on soil microbial activity and root nodule nitrogenise. J Saudi Soc Agric Sci 10:109–120

    Google Scholar 

  • Moll J, Klingenfuss F, Widmer F, Gogos A, Bucheli TD, Hartmann M, Heijden MGA (2017) Effects of titanium dioxide nanoparticles on soil microbial communities and wheat biomass. Soil Biol Biochem 111:85–93

    Article  CAS  Google Scholar 

  • Nelson DV, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL (ed) Methods of soil analysis, part 3: chemical methods. American Society of Agronomy, Madison, pp 961–1010

  • Qi XZ, Zhao JQ, Tian CG, Ma YH (2013) Study on alkaline cellulase in fungal sources. In: Ninth Chinese Enzyme Engineering Conference Proceedings, p 41

  • Qiu HS, Ge TD, Liu JY, Chen XB, Hu YJ, Wu JS, Su YR, Kuzyakov Y (2018) Effects of biotic and abiotic factors on soil organic matter mineralization: Experiments and structural modeling analysis. Eur J Soil Biol 84:27–34

    Article  CAS  Google Scholar 

  • Rashid MI, Shahzad T, Shahid M, Ismail IM, Shah GM, Almeelbi T (2017a) Zinc oxide nanoparticles affect carbon and nitrogen mineralization of Phoenix dactylifera leaf litter in a sandy soil. J Hazard Mater 324:298–305

    Article  CAS  Google Scholar 

  • Rashid MI, Shahzad T, Shahid M, Imran M, Dhavamani J, Ismail IM, Basahi JM, Almeelbi T (2017b) Toxicity of iron oxide nanoparticles to grass litter decomposition in a sandy soil. Sci Rep-UK 7:41965

    Article  CAS  Google Scholar 

  • Read DS, Matzke M, Gweon HS, Newbold LK, Heggelund L, Ortiz MD, Lahive E, Spurgeon D, Svendsen C (2016) Soil pH effects on the interactions between dissolved zinc, non-nano-and nano-ZnO with soil bacterial communities. Environ Sci Pollut Res 23:4120–4128

    Article  CAS  Google Scholar 

  • Shen ZY, Chen Z, Hou Z, Li TT, Lu XX (2015) Ecotoxicological effect of zinc oxide nanoparticles on soil microorganisms. Front Environ Sci Eng 9:912–918

    Article  CAS  Google Scholar 

  • Sheng H, Song DS, Wang CH, Zhou P, Zhang YZ (2015) Comparison and transform of soil dissolved organic carbon measured by four methods. Soils 47:1049–1053

    CAS  Google Scholar 

  • Shi QQ, Deng DL, Yan C, Pu SY (2018) Review on effects of engineered nano-metal oxide particles on soil enzyme activities. Asian J Ecotoxicol 13:47–56

    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 

  • Song N, Xu HC, Yan ZS, Yang T, Wang CH, Jiang HL (2019) Improved lignin degradation through distinct microbial community in subsurface sediments of one eutrophic lake. Renew Energy 138:861–869

    Article  CAS  Google Scholar 

  • Sun YQ, Shen CC, Ge Y (2016) Review on microbiological effects of typical nanomaterials in soil ecosystem. Asian J Ecotoxicol 11(5):2–13

    Google Scholar 

  • Sun Q, Li J, Le T, Zhang L (2019) Research progress on antifungal activity of zinc oxide nanoparticles. J Chongqing Normal University (Nat Sci) 36:122–129

    Google Scholar 

  • Tlili A, Cornut J, Behra R, Gil-Allué C, Gessner MO (2016) Harmful effects of silver nanoparticles on a complex detrital model system. Nanotoxicology 10(6):728–735

    Article  CAS  Google Scholar 

  • Vance E, Brookes P, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Waalewijn-Kool PL, Rupp S, Lofts S, Svendsen C, Gestel CAMV (2014) Effect of soil organic matter content and pH on the toxicity of ZnO nanoparticles to Folsomia candida. Ecotox Environ Safe 108:9–15

    Article  CAS  Google Scholar 

  • Wang H, Hu GQ, Xu WH, Boutton TW, Zhuge YP, Bai E (2018) Effects of nitrogen addition on soil organic carbon mineralization after maize stalk addition. Eur J Soil Biol 89:33–38

    Article  CAS  Google Scholar 

  • Wu DM, Guo JF, Zhang Z, Li SJ, Yang YS (2018) Effects of dissolved organic matter addition on soil microbial respiration and quotient values in a secondary Castanopsis carlesii forest. Acta Ecol Sin 38:3806–3815

    Google Scholar 

  • Xu HW, Shao HB, Lu Y (2019) Arbuscular mycorrhiza fungi and related soil microbial activity drive carbon mineralization in the maize rhizosphere. Ecotoc Environ Safe 182:109476

    Article  CAS  Google Scholar 

  • You TT, Liu DD, Chen J, Yang ZZ, Dou RZ, Gao X, Wang L (2017) Effects of metal oxide nanoparticles on soil enzyme activities and bacterial communities in two different soil types. J Soils Sediments 18(1):211–221

    Article  Google Scholar 

  • Yu Q, Xia J, Xu C, Yan Y (2019) Study on physicochemical properties of nanometer zinc oxide. J Agric Dev Equip 4:53–54

    Google Scholar 

  • Zhao SC, Zhang SQ (2018) Linkages between straw decomposition rate and the change in microbial fractions and extracellular enzyme activities in soils under different long-term fertilization treatments. PLoS One 13:e0202660

    Article  Google Scholar 

  • Zhao SC, Qiu SJ, Xu XP, Ciampitti IA, Zhang SQ, He P (2019) Change in straw decomposition rate and soil microbial community composition after straw addition in different long-term fertilization soils. Appl Soil Ecol 138:123–133

    Article  Google Scholar 

  • Zhu J, Peng H, Ji XH, Li CJ, Li SN (2019) Effects of reduced inorganic fertilization and rice straw recovery on soil enzyme activities and bacterial community in double-rice paddy soils. Eur J Soil Biol 94:103116

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (41877424; 31870606), the Natural Science Foundation of Shandong Province (ZR2018MD002; ZR2017MD022), and the joint funds of the National Natural Science Foundation of China (U1806217). Thanks to Dr. Edward C. Mignot, of Shandong University, for linguistic advice.

Author information

Author notes

  1. Hao Jiang and Baoshan Yang contributed equally to this work.

Authors and Affiliations

  1. School of Water Conservancy and Environment, University of Jinan, Jinan, 250022, China

    Hao Jiang, Baoshan Yang, Hui Wang, Xinlei Cao, Chunhui Zhao & Kexin Yin

  2. Key Laboratory of Water Resources and Environmental Engineering in Universities of Shandong Province, University of Jinan, Jinan, 250022, China

    Baoshan Yang & Hui Wang

  3. Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia

    Qinglin Chen

  4. Qilu University of Technology (Shandong Academy of Sciences), Ecology Institute, Shandong Provincial Key Laboratory of Applied Microbiology, Jinan, 250103, China

    Yongchao Gao

Authors
  1. Hao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Baoshan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinglin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinlei Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yongchao Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chunhui Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kexin Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hui Wang.

Additional information

Responsible editor: Qiaoyun Huang

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 1176 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, H., Yang, B., Wang, H. et al. Insights on the effects of ZnO nanoparticle exposure on soil heterotrophic respiration as revealed by soil microbial communities and activities . J Soils Sediments 21, 2315–2326 (2021). https://doi.org/10.1007/s11368-021-02947-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-021-02947-6

Keywords

Search

Navigation