Skip to main content
SpringerLink
Log in

Insight into the impact of Fe3O4 nanoparticles on anammox process of subsurface-flow constructed wetlands under long-term exposure

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

Abstract

The increasing use of Fe3O4 nanoparticles (NPs) had posed an emerging challenge to wastewater treatment processes, and their potential impact on anaerobic ammonium oxidation (anammox) process of unplanted subsurface-flow constructed wetlands (USFCWs) was investigated firstly under the long-term exposure of different Fe3O4 NP concentrations. It was found that Fe3O4 NP exposure could improve total nitrogen (TN) removal. The abundance of Candidatus Anammoxoglobus increased significantly at 10 mg/L Fe3O4 NPs, while decreased under 1 mg/L Fe3O4 NP exposure. Desulfosporosinus and Exiguobacterium increased to some extent at 1 mg/L Fe3O4 NPs, suggesting that Fe-anammox played an important role in TN removal. The ROS production increased with the increase of Fe3O4 NP concentration, and the integrity of cell membrane was good under Fe3O4 NP exposure. The functional genes that related to inorganic ion transport and metabolism and lipid transport and metabolism were upregulated, and cell motility decreased after long-term exposure of 1 mg/L Fe3O4 NPs.

ᅟ

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
Fig. 5

Similar content being viewed by others

References

  • APHA (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

    Google Scholar 

  • Applerot G, Lellouche J, Lipovsky A, Nitzan Y, Lubart R, Gedanken A, Banin E (2012) Understanding the antibacterial mechanism of CuO nanoparticles: revealing the route of induced oxidative stress. Small 8:3326–3337

    Article  CAS  Google Scholar 

  • Chen H, Yu JJ, Jia XY, Jin RC (2014) Enhancement of anammox performance by Cu (II), Ni (II) and Fe (III) supplementation. Chemosphere 117:610–616

    Article  CAS  Google Scholar 

  • Chu Z, Wang K, Li X, Zhu M, Yang L, Zhang J (2015) Microbial characterization of aggregates within a one-stage nitritation–anammox system using high-throughput amplicon sequencing. Chem Eng J 262:41–48

    Article  CAS  Google Scholar 

  • Chung H, Kim MJ, Ko K, Kim JH, Kwon H, Hong I, Park N, Lee SW, Kim W (2015) Effects of graphene oxides on soil enzyme activity and microbial biomass. Sci Total Environ 514:307–313

    Article  CAS  Google Scholar 

  • de Almeida NM, Wessels HJCT, de Graaf RM, Ferousi C, Jetten M, Keltjens J, Kartal B (2016) Membrane-bound electron transport systems of an anammox bacterium: a complexome analysis. Biochim Biophys Acta Biomembr 1857(10):1694–1704

    Article  Google Scholar 

  • Ding LJ, An XL, Li S, Zhang G, Zhu Y (2014) Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ Sci Technol 48(18):10641–10647

    Article  CAS  Google Scholar 

  • Ding B, Li Z, Qin Y (2017) Nitrogen loss from anaerobic ammonium oxidation coupled to iron (III) reduction in a riparian zone. Environ Pollut 231:379–386

    Article  CAS  Google Scholar 

  • Dwivedi S, Siddiqui MA, Farshori NN, Ahamed M, Musarrat J, Al-Khedhairy A (2014) Synthesis, characterization and toxicological evaluation of iron oxide nanoparticles in human lung alveolar epithelial cells. Colloids Surf B Biointerfaces 122:209–215

    Article  CAS  Google Scholar 

  • Gao C, Wang A, Wu WM, Yin Y, Zhao YG (2014) Enrichment of anodic biofilm inoculated with anaerobic or aerobic sludge in single chambered air-cathode microbial fuel cells. Bioresour Technol 167:124–132

    Article  CAS  Google Scholar 

  • Hai R, Wang Y, Wang X, Du Z, Li Y (2014) Impacts of multiwalled carbon nanotubes on nutrient removal from wastewater and bacterial community structure in activated sludge. PLoS One 9(9):e107345

    Article  Google Scholar 

  • Hira D, Toh H, Migita CT, Okubo H, Nishiyama T, Hattori M, Furukawa K, Fujii T (2012) Anammox organism KSU-1 expresses a NirK-type copper-containing nitrite reductase instead of a NirS-type with cytochrome cd 1. FEBS Lett 586(11):1658–1663

    Article  CAS  Google Scholar 

  • Hou J, Miao L, Wang C, Wang P, Ao Y, Qian J (2014) Inhibitory effects of ZnO nanoparticles on aerobic wastewater biofilms from oxygen concentration profiles determined by microelectrodes. J Hazard Mater 276:164–170

    Article  CAS  Google Scholar 

  • Hou J, Miao L, Wang C, Wang P, Ao Y, Lv B (2015) Effect of CuO nanoparticles on the production and composition of extracellular polymeric substances and physicochemical stability of activated sludge flocs. Bioresour Technol 176:65–70

    Article  CAS  Google Scholar 

  • Huang X, Gao D, Peng S, Tao Y (2014) Effects of ferrous and manganese ions on anammox process in sequencing batch biofilm reactors. J Environ Sci 26(5):1034–1039

    Article  CAS  Google Scholar 

  • Kaegi R, Voegelin A, Sinnet B, Zuleeg S, Hagendorfer H, Burkhardt M, Siegrist H (2011) Behavior of metallic silver nanoparticles in a pilot wastewater treatment plant. Environ Sci Technol 45(9):3902–3908

    Article  CAS  Google Scholar 

  • Li H, Chi Z, Li J (2014) Covalent bonding synthesis of magnetic graphene oxide nanocomposites for Cr (III) removal. Desalin Water Treat 52(10–12):1937–1946

    Article  CAS  Google Scholar 

  • Li B, Pan X, Zhang D, Lee D, Al-Misned F, Golam Mortuza M (2015) Anaerobic nitrate reduction with oxidation of Fe (II) by Citrobacter freundii strain PXL1–a potential candidate for simultaneous removal of As and nitrate from groundwater. Ecol Eng 77:196–201

    Article  CAS  Google Scholar 

  • Liu S, Yang F, Meng F, Chen L, Gong Z (2008) Enhanced anammox consortium activity for nitrogen removal: impacts of static magnetic field. J Biotechnol 138(3–4):96–102

    Article  CAS  Google Scholar 

  • Liu TY, Hu SH, Liu DM, Chen SY, Chen IW (2009) Biomedical nanoparticle carriers with combined thermal and magnetic responses. Nano Today 4(1):52–65

    Article  CAS  Google Scholar 

  • Liu S, Zeng TH, Hofmann M, Burcombe E, Wei J, Jiang R, Kong J, Chen Y (2011) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5(9):6971–6980

    Article  CAS  Google Scholar 

  • Liu L, Lee D, Wang A, Ren N, Su A, Lai JY (2016) Isolation of Fe (III)-reducing bacterium, Citrobacter sp. LAR-1, for startup of microbial fuel cell. Int J Hydrog Energy 41(7):4498–4503

    Article  CAS  Google Scholar 

  • Ma Y, Metch JW, Vejerano EP, Miller IJ, Leon EC, Marr LC, Vikesland PJ, Pruden A (2015) Microbial community response of nitrifying sequencing batch reactors to silver, zero-valent iron, titanium dioxide and cerium dioxide nanomaterials. Water Res 68:87–97

    Article  CAS  Google Scholar 

  • Ma B, Wang S, Li Z, Gao M, Li S, Guo L, She Z, Zhao Y, Zheng D, Jin C, Wang X, Gao F (2017) Magnetic Fe3O4 nanoparticles induced effects on performance and microbial community of activated sludge from a sequencing batch reactor under long-term exposure. Bioresour Technol 225:377–385

    Article  CAS  Google Scholar 

  • Ni SQ, Ni J, Yang N, Wang J (2013) Effect of magnetic nanoparticles on the performance of activated sludge treatment system. Bioresour Technol 143:555–561

    Article  CAS  Google Scholar 

  • Oshiki M, Ishii S, Yoshida K, Fujii N, Ishiguro M, Satoh H, Okabe S (2013) Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Appl Environ Microbiol 79(13):4087–4093

    Article  CAS  Google Scholar 

  • Quan X, Cen Y, Lu F, Gu L, Ma J (2015) Response of aerobic granular sludge to the long-term presence to nanosilver in sequencing batch reactors: reactor performance, sludge property, microbial activity and community. Sci Total Environ 506:226–233

    Article  Google Scholar 

  • Reinhart DR, Berge ND, Santra S, Bolyard SC (2010) Emerging contaminants: nanomaterial fate in landfills. Waste Manag 30:2020–2021

    Article  Google Scholar 

  • Ren Y, Li D, Li X, Yang L, Ding A, Zhang J (2014) High-rate nitrogen removal and microbial community of an up-flow anammox reactor with ceramics as biomass carrier. Chemosphere 113:125–131

    Article  CAS  Google Scholar 

  • Sawayama S (2006) Possibility of anoxic ferric ammonium oxidation. J Biosci Bioeng 101(1):70–72

    Article  CAS  Google Scholar 

  • Sevcu A, El-Temsah YS, Joner EJ, Cernik M (2011) Oxidative stress induced in microorganisms by zerovalent iron nanoparticles. Microbes Environ 26:271–281

  • Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Fujii T (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol 73(4):1065–1072

    Article  CAS  Google Scholar 

  • Song YX, Chai LY, Tang CJ, Xiao R, Li BR, Wu D, Min XB (2018) Influence of ZnO nanoparticles on anammox granules: the inhibition kinetics and mechanism analysis by batch assays. Biochem Eng J 133:122–129

    Article  CAS  Google Scholar 

  • Sorokina AY, Chernousova EY, Dubinina GA (2012) Ferrovibrio denitrificans gen. nov., sp. nov., a novel neutrophilic facultative anaerobic Fe (II)-oxidizing bacterium. FEMS Microbiol Lett 335(1):19–25

    Article  CAS  Google Scholar 

  • Srinivas A, Rao PJ, Selvam G, Goparaju A, Murthy B, Reddy N (2012) Oxidative stress and inflammatory responses of rat following acute inhalation exposure to iron oxide nanoparticles. Hum Exp Toxicol 31(11):1113–1131

    Article  CAS  Google Scholar 

  • Straub KL, Benz M, Schink B, Widdel F (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62(4):1458–1460

    CAS  Google Scholar 

  • Tang CJ, Duan CS, Yu C, Song YX, Chai LY, Xiao R, Wei Z, Min XB (2017) Removal of nitrogen from wastewaters by anaerobic ammonium oxidation (ANAMMOX) using granules in upflow reactors. Environ Chem Lett 15(2):311–328

    Article  CAS  Google Scholar 

  • Van de Graaf AA, de Bruijn P, Robertson LA, Jetten MS, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiology 142(8):2187–2196

    Article  Google Scholar 

  • Wang Z, Zhang L, Zhao J, Xing B (2016) Environmental processes and toxicity of metallic nanoparticles in aquatic systems as affected by natural organic matter. Environ. Sci Nano 3(2):240–255

    Article  Google Scholar 

  • Xu JJ, Zhang ZZ, Ji ZQ, Zhu YH, Qi SY, Tang CJ, Jin RC (2018) Short-term effects of nanoscale zero-valent iron (nZVI) and hydraulic shock during high-rate anammox wastewater treatment. J Environ Manag 215:248–257

    Article  CAS  Google Scholar 

  • Yao C, Lei HY, Yu Q, Li S, Li H, Chen K, Zhang X (2013) Application of magnetic enhanced bio-effect on nitrification: a comparative study of magnetic and non-magnetic carriers. Water Sci Technol 67(6):1280–1287

    Article  CAS  Google Scholar 

  • Zhang L, Yang J, Ma Y, Li Z, Fuji T, Zhang W, Takashi N, Furukawa K (2010) Treatment capability of an up-flow anammox column reactor using polyethylene sponge strips as biomass carrier. J Biosci Bioeng 110(1):72–78

    Article  CAS  Google Scholar 

  • Zhang ZZ, Xu JJ, Shi ZJ, Bai YH, Cheng YF, Hu HY, Jin RC (2017a) Unraveling the impact of nanoscale zero-valent iron on the nitrogen removal performance and microbial community of anammox sludge. Bioresour Technol 243:883–892

    Article  CAS  Google Scholar 

  • Zhang ZZ, Xu JJ, Shi ZJ, Cheng YF, Ji ZQ, Deng R, Jin RC (2017b) Combined impacts of nanoparticles on anammox granules and the roles of EDTA and S2− in attenuation. J Hazard Mater 334:49–58

    Article  CAS  Google Scholar 

  • Zhang ZZ, Cheng YF, Bai YH, Xu JJ, Shi ZJ, Zhang QQ, Jin RC (2018a) Enhanced effects of maghemite nanoparticles on the flocculent sludge wasted from a high-rate anammox reactor: performance, microbial community and sludge characteristics. Bioresour Technol 250:265–272

    Article  CAS  Google Scholar 

  • Zhang X, Zhou Y, Xu T, Zheng K, Zhang R, Peng Z, Zhang H (2018b) Toxic effects of CuO, ZnO and TiO2 nanoparticles in environmental concentration on the nitrogen removal, microbial activity and community of anammox process. Chem Eng J 332:42–48

    Article  CAS  Google Scholar 

  • Zhou GW, Yang XR, Li H, Marshall C, Zheng B, Yan Y, Su J, Zhu Y (2016) Electron shuttles enhance anaerobic ammonium oxidation coupled to iron (III) reduction. Environ Sci Technol 50(17):9298–9307

    Article  CAS  Google Scholar 

Download references

Funding

This work was financially supported by the National Key R&D Program of China (no. 2017YFC0505901), the National Natural Science Foundation of China (no. 41401548; no. 41772244), the Open Project of State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (no. HC201622), and the China Scholarship Council (no. 201804910339 and 201806175055).

Author information

Authors and Affiliations

  1. Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, People’s Republic of China

    Huai Li & Baixing Yan

  2. State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin, 150090, People’s Republic of China

    Huai Li

  3. Key Lab of Groundwater Resources and Environment, Ministry of Education, Jilin University, Changchun, 130021, People’s Republic of China

    Zifang Chi

Authors
  1. Huai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zifang Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baixing Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zifang Chi.

Additional information

Responsible editor: Bingcai Pan

Highlights

• Long-term exposure of Fe3O4 NPs could increase the USFCWs performance.

• Fe-anammox played an important role in TN removal under 1 mg/L Fe3O4 NP exposure

• Desulfosporosinus and Exiguobacterium increased to some extent at 1 mg/L Fe3O4 NPs

• HDH activity of USFCWs decreased to 23% at 1 mg/L Fe3O4 NPs

• Self-adaptive ability of microbial community was explained by PICRUSt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Chi, Z. & Yan, B. Insight into the impact of Fe3O4 nanoparticles on anammox process of subsurface-flow constructed wetlands under long-term exposure. Environ Sci Pollut Res 25, 29584–29592 (2018). https://doi.org/10.1007/s11356-018-2975-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2975-1

Keywords

Search

Navigation