Skip to main content
Log in

Negative effects of rare earth oxide nanoparticles of La2O3, Nd2O3, and Gd2O3 on the ammonia-oxidizing microorganisms

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Nanoparticles released into soil environment potentially impact microorganisms, which furtherly disturb terrestrial biogeochemical cycles. However, how rare earth oxide nanoparticles affect the functional microorganisms inhabited in natural soil is still unknown. This study was aimed to investigate the effect of different types of rare earth oxide nanoparticles on the ammonia-oxidizing microorganisms.

Materials and methods

Soil respectively added with 0, 10, 50, and 100 mg kg−1 of La2O3, Nd2O3, or Gd2O3 nanoparticle were incubated at 25 °C in the dark for 60 days. The potential ammonia oxidation (PAO), abundance and communities of ammonia-oxidizing archaea (AOA), and ammonia-oxidizing bacteria (AOB) were measured at the 1st, 7th, and 60th day.

Results and discussion

Our results showed that the PAO in soils with nanoparticles significantly decreased due to nanoparticle toxicity at the 1st day, but it gradually increased to the control level owing to the adaptation of AOA and AOB in soils with nano-Nd2O3 and nano-Gd2O3. Interestingly, the abundance of AOB as reflected by the qPCR analysis was upregulated for the hormesis effect of AOB responding to nano-Nd2O3 or nano-Gd2O3 with 50 mg kg−1 level. Moreover, terminal restriction fragment length polymorphism (T-RFLP) results suggested that the communities for AOA and AOB shifted with nanoparticles type and incubation time.

Conclusions

Rare earth oxide nanoparticles could inhibit activities of ammonia-oxidizing microorganisms, and thus they might be used as potential nitrification inhibitors to improve nitrogen use efficiency in the agricultural ecosystems.

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

Similar content being viewed by others

References

  • Ahmad HR, Zia-ur-Rehman M, Sohail MI, ul Haq MA, Khalid H, Ayub MA, Ishaq G (2018) Effects of rare earth oxide nanoparticles on plants. In: Nanomaterials in plants, algae, and microorganisms. Academic Press, Pittsburgh, pp 239–275

    Google Scholar 

  • Ali J, Ali N, Wang L, Waseem H, Pan G (2019) Revisiting the mechanistic pathways for bacterial mediated synthesis of noble metal nanoparticles. J Microbiol Methods 159:18–25

    CAS  Google Scholar 

  • Aydın A, Sipahi H, Mohammad C (2012) Nanoparticles toxicity and their routes of exposures. In: Recent advances in novel drug carrier systems, pp 483–500

  • Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol 2:16242

    Google Scholar 

  • de Scally SZ, Makhalanyane TP, Frossard A, Hogg ID, Cowan DA (2016) Antarctic microbial communities are functionally redundant, adapted and resistant to short term temperature perturbations. Soil Biol Biochem 103:160–170

    Google Scholar 

  • Dhand C, Dwivedi N, Loh XJ, Ying ANJ, Verma NK, Beuerman RW, Lakshminarayanan R, Ramakrishna S (2015) Methods and strategies for the synthesis of diverse nanoparticles and their applications: a comprehensive overview. RSC Adv 5:105003–105037

    CAS  Google Scholar 

  • Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature 509(7502):612–616

    CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688

    CAS  Google Scholar 

  • Galand PE, Pereira O, Hochart C, Auguet JC, Debroas D (2018) A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J 12:2470–2478

    CAS  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

    CAS  Google Scholar 

  • Ge Y, Priester JH, Van De Werfhorst LC, Walker SL, Nisbet RM, An Y, Schimel JP, Gardea-Torresdey JL, Holden PA (2014) Soybean plants modify metal oxide nanoparticle effects on soil bacterial communities. Environ Sci Technol 48(22):13489–13496

    CAS  Google Scholar 

  • Ge Y, Horst AM, Kim J, Priester JH, Welch ZS, Holden PA (2016a) Toxicity of manufactured nanomaterials to microorganisms. In: Senesi N, Xing B (eds) Toxicity of engineered nanoparticles and risk assessment. Wiley, Hoboken, pp 320–346

    Google Scholar 

  • Ge Y, Priester JH, Mortimer M, Chang CH, Ji Z, Schimel JP, Holden PA (2016b) Long-term effects of multiwalled carbon nanotubes and graphene on microbial communities in dry soil. Environ Sci Technol 50:3965–3974

    CAS  Google Scholar 

  • Ge Y, Shen C, Wang Y, Sun Y, Schimel JP, Gardea-Torresdey JL, Holden PA (2018) Carbonaceous nanomaterials have higher effects on soybean rhizosphere prokaryotic communities during the reproductive growth phase than during vegetative growth. Environ Sci Technol 52:6636–6646

    CAS  Google Scholar 

  • Grün A-L, Manz W, Kohl YL, Meier F, Straskraba S, Jost C, Drexel R, Emmerling C (2019) Impact of silver nanoparticles (AgNP) on soil microbial community depending on functionalization, concentration, exposure time, and soil texture. Environ Sci Eur 31:15

    Google Scholar 

  • Gustave W, Yuan Z, Sekar R, Toppin V, Liu J, Ren Y, Zhang J, Chen Z (2019) Relic DNA does not obscure the microbial community of paddy soil microbial fuel cells. Res Microbiol 170:97–104

    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

    CAS  Google Scholar 

  • Hink L, Gubry-Rangin C, Nicol GW, Prosser JI (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12:1084–1093

    CAS  Google Scholar 

  • Hu H-W, He J-Z (2017) Comammox-a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soils Sediments 17:2709–2717

    CAS  Google Scholar 

  • Kurola J, Salkinoja-Salonen M, Aarnio T, Hultman J, Romantschuk M (2005) Activity, diversity and population size of ammonia-oxidising bacteria in oil-contaminated landfarming soil. FEMS Microbiol Lett 250:33–38

    CAS  Google Scholar 

  • Lennon JT, Muscarella ME, Placella SA, Lehmkuhla BK (2018) How, when, and where relic DNA affects microbial diversity. ASM 9(3):e00637–e00618

    Google Scholar 

  • Li Y, Chapman SJ, Nicol GW, Yao H (2018) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301

    CAS  Google Scholar 

  • Li Y, Chen Z, He J, Wang Q, Shen C, Ge Y (2019a) Ectomycorrhizal fungi inoculation alleviates simulated acid rain effects on soil ammonia oxidisers and denitrifiers in Masson pine forest. Environ Microbiol 21(1):299–313

    CAS  Google Scholar 

  • Li Y, Xi R, Wang W, Yao H (2019b) The relative contribution of nitrifiers to autotrophic nitrification across a pH-gradient in a vegetable cropped soil. J Soils Sediments 19:1416–1426

    CAS  Google Scholar 

  • Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z (2010) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78:273–279

    CAS  Google Scholar 

  • Moeinzadeh S, Jabbari E (2018) Nanoparticles and their applications. In: Bhushan B (ed) Springer handbook of nanotechnology, 4th edn. Springer, Berlin, pp 335–361

    Google Scholar 

  • Moore JD, Stegemeier JP, Bibby K, Marinakos SM, Lowry GV, Gregory KB (2016) Impacts of pristine and transformed Ag and Cu engineered nanomaterials on surficial sediment microbial communities appear short-lived. Environ Sci Technol 50:2641–2651

    CAS  Google Scholar 

  • Nichol D, Rutter J, Bryant C, Hujer AM, Lek S, Adams MD, Jeavons P, Anderson ARA, Bonomo RA, Scott JG (2019) Antibiotic collateral sensitivity is contingent on the repeatability of evolution. Nat Commun 10:334

    Google Scholar 

  • Oliver TH, Isaac NJB, August TA, Woodcock BA, Roy DB, Bullock JM (2015) Declining resilience of ecosystem functions under biodiversity loss. Nat Commun 6:10122

    Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammoniaoxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20(11):523–531

    CAS  Google Scholar 

  • Qi L, Ge Y, Xia T, He J, Shen C, Wang J, Liu Y (2019) Rare earth oxide nanoparticles promote soil microbial antibiotic resistance by selectively enriching antibiotic resistance genes. Environ Sci-Nano 6:456–466

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Reichardt N, Vollmer M, Holtrop G, Farquharson FM, Wefers D, Bunzel M, Duncan SH, Drew JE, Williams LM, Milligan G, Preston T, Morrison D, Flint HJ, Louis P (2018) Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production. ISME J 12:610–622

    CAS  Google Scholar 

  • Ren L, Cai C, Zhang J, Yang Y, Wu G, Luo L, Huang H, Zhou Y, Qin P, Yu M (2018) Key environmental factors to variation of ammonia-oxidizing archaea community and potential ammonia oxidation rate during agricultural waste composting. Bioresour Technol 270:278–285

    CAS  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  Google Scholar 

  • Šantrůčková H, Kotas P, Bárta J, Urich T, Čapek P, Palmtag J, Alves RJE, Biasi C, Diáková K, Gentsch N, Gittel A, Guggenberger G, Hugelius G, Lashchinsky N, Martikainen PJ, Mikutta R, Schleper C, Schnecker J, Schwab C, Shibistova O, Wild B, Richter A (2018) Significance of dark CO2 fixation in arctic soils. Soil Biol Biochem 119:11–21

    Google Scholar 

  • Sepehri A, Sarrafzadeh M-H (2019) Activity enhancement of ammonia-oxidizing bacteria and nitrite-oxidizing bacteria in activated sludge process: metabolite reduction and CO2 mitigation intensification process. Appl Water Sci 9:131

    Google Scholar 

  • Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JBH, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417

    Google Scholar 

  • Srivastava V, Gusain D, Sharma YC (2015) Critical review on the toxicity of some widely used engineered nanoparticles. Ind Eng Chem Res 54:6209–6233

    CAS  Google Scholar 

  • Sun R, Myrold DD, Wang D, Guo X, Chu H (2019) AOA and AOB communities respond differently to changes of soil pH under long-term fertilization. Soil Ecol Lett 1(3–4):126–135

    Google Scholar 

  • Tang J, Wu Y, Esquivel-Elizondo S, Sørensen SJ, Rittmann BE (2018) How microbial aggregates protect against nanoparticle toxicity. Trends Biotechnol 36(11):1171–1182

    CAS  Google Scholar 

  • Wang J, Wang J, Rhodes G, He J, Ge Y (2019) Adaptive responses of comammox Nitrospira and canonical ammonia oxidizers to long-term fertilizations: implications for the relative contributions of different ammonia oxidizers to soil nitrogen cycling. Sci Total Environ 668:224–233

    CAS  Google Scholar 

  • Xiang SR, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biol Biochem 40:2281–2289

    CAS  Google Scholar 

  • Xu C, Peng C, Sun L, Zhang S, Huang H, Chen Y, Shi J (2015) Distinctive effects of TiO2 and CuO nanoparticles on soil microbes and their community structures in flooded paddy soil. Soil Biol Biochem 86:24–33

    CAS  Google Scholar 

  • Yue L, Chen F, Yu K, Xiao Z, Yu X, Wang Z, Xing B (2019) Early development of apoplastic barriers and molecular mechanisms in juvenile maize roots in response to La2O3 nanoparticles. Sci Total Environ 653:675–683

    CAS  Google Scholar 

  • Zhang L, Hu H, Shen J, He J (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    CAS  Google Scholar 

  • Zhang H, Sun H, Zhou S, Bai N, Zheng X, Li S, Zhang J, Lv W (2019a) Effect of straw and straw biochar on the community structure and diversity of ammonia-oxidizing bacteria and archaea in rice-wheat rotation ecosystems. Sci Rep 9:9367

    Google Scholar 

  • Zhang Q, Li Y, He Y, Brookes PC, Xu J (2019b) Elevated temperature increased nitrification activity by stimulating AOB growth and activity in an acidic paddy soil. Plant Soil 445:71–83

    CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (41671254), the National Postdoctoral Program for Innovative Talents (BX201700273), and the State Key Laboratory of Urban and Regional Ecology (SKLURE2017-1-7).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuan Ge.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

This manuscript is new and not being considered elsewhere. All authors have approved the submission of this manuscript.

Additional information

Responsible editor: Huaiying Yao

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yue, Y., Qi, L., Li, Y. et al. Negative effects of rare earth oxide nanoparticles of La2O3, Nd2O3, and Gd2O3 on the ammonia-oxidizing microorganisms. J Soils Sediments 20, 3114–3123 (2020). https://doi.org/10.1007/s11368-020-02627-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-020-02627-x

Keywords

Navigation