Skip to main content
Log in

Water-dispersible nano-pollutions reshape microbial metabolism in type-specific manners: A metabolic and bacteriological investigation in Escherichia coli

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Incomplete separation and recycling of nanoparticles are causing undesirable nanopollution and thus raising great concerns with regard to nanosafety. Since microorganisms are important regulator of physiological processes in many organisms, the interaction between nanopollution and microbial metabolomics and the resultant impact on the host’s health are important but unclear. To investigate how typical nanopollution perturbs microbial growth and metabolism, Escherichia coli (E. coli) in vitro was treated with six water-dispersible nanomaterials (nanoplastic, nanosilver, nano-TiO2, nano-ZnO, semiconductor quantum dots (QDs), carbon dots (CDs)) at human-/environment-relevant concentration levels. The nanomaterials exhibited type-specific toxic effects on E. coli growth. Global metabolite profiling was used to characterize metabolic disruption patterns in the model microorganism exposed to different nanopollutants. The percentage of significant metabolites (p < 0.05, VIP > 1) accounted for 6%–38% of the total 293 identified metabolites in each of the nanomaterial-contaminated bacterial groups. Metabolic results also exhibited significant differences between different nanopollutants and dose levels, revealing type-specific and untypical concentration-dependent metabolic responses. Key metabolites responsive to nanopollution exposures were mainly involved in amino acid and purine metabolisms, where 5, 4, and 7 significant metabolic features were included in arginine and proline metabolism, phenylalanine metabolism, and purine metabolism, respectively. In conclusion, this study horizontally compared and demonstrated how typical nanopollution perturbs microbial growth and metabolomics in a type-specific manner, which broadens our understanding of the ecotoxicity of nanopollutants on microorganisms.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad N S, Abdullah N, Yasin F M (2020). Toxicity assessment of reduced graphene oxide and titanium dioxide nanomaterials on gram-positive and gram-negative bacteria under normal laboratory lighting condition. Toxicology Reports, 7: 693–699

    Article  CAS  Google Scholar 

  • Castro R C, Ribeiro D S M, Santos J L M (2021). Visual detection using quantum dots sensing platforms. Coordination Chemistry Reviews, 429: 213637

    Article  CAS  Google Scholar 

  • Choudhary R K, Choudhary S, Pathak D, Udehiya R, Verma R, Kaswan S, Sharma A, Gupta D, Honparkhe M, Capuco A V (2018a). Evaluation of xanthosine treatment on gene expression of mammary glands in early lactating goats. Journal of Dairy Research, 85(3): 288–294

    Article  CAS  Google Scholar 

  • Choudhary S, Li W, Bickhart D, Verma R, Sethi R S, Mukhopadhyay C S, Choudhary R K (2018b). Examination of the xanthosine response on gene expression of mammary epithelial cells using RNA-seq technology. Journal of Animal Science and Technology, 60(1): 18

    Article  Google Scholar 

  • Clift M J D, Jenkins G J S, Doak S H (2020). An alternative perspective towards reducing the risk of engineered nanomaterials to human health. Small, 16(36): 2002002

    Article  CAS  Google Scholar 

  • Cox K D, Covernton G A, Davies H L, Dower J F, Juanes F, Dudas S E (2019). Human consumption of microplastics. Environmental Science & Technology, 53(12): 7068–7074

    Article  CAS  Google Scholar 

  • Daignan-Fornier B, Pinson B (2019). Yeast to study human purine metabolism diseases. Cells, 8(1): 67

    Article  CAS  Google Scholar 

  • Goryacheva I Y, Sapelkin A V, Sukhorukov G B (2017). Carbon nanodots: Mechanisms of photoluminescence and principles of application. Trends in Analytical Chemistry, 90: 27–37

    Article  CAS  Google Scholar 

  • Horst M F, Lassalle V, Ferreira M L (2015). Nanosized magnetite in low cost materials for remediation of water polluted with toxic metals, azo- and antraquinonic dyes. Frontiers of Environmental Science & Engineering, 9(5): 746–769

    Article  CAS  Google Scholar 

  • Hu X, Li Y, Xu Y, Gan Z, Zou X, Shi J, Huang X, Li Z, Li Y (2021). Green one-step synthesis of carbon quantum dots from orange peel for fluorescent detection of Escherichia coli in milk. Food Chemistry, 339: 127775

    Article  CAS  Google Scholar 

  • Jalili R, Khataee A (2020). Application of molecularly imprinted polymers and dual-emission carbon dots hybrid for ratiometric determination of chloramphenicol in milk. Food and Chemical Toxicology, 146: 111806

    Article  CAS  Google Scholar 

  • Ji Q, Zhang C, Li D (2020). Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains. Frontiers of Environmental Science & Engineering, 14(6): 108

    Article  CAS  Google Scholar 

  • Jia B, Liao X, Sun C, Fang L, Zhou L, Kong W (2021). Development of a quantum dot nanobead-based fluorescent strip immunosensor for on-site detection of aflatoxin B1 in lotus seeds. Food Chemistry, 356: 129614

    Article  CAS  Google Scholar 

  • Joo J I, Choi M, Jang S H, Choi S, Park S M, Shin D, Cho K H (2020). Realizing cancer precision medicine by integrating systems biology and nanomaterial engineering. Advanced Materials, 32(35): 1906783

    Article  CAS  Google Scholar 

  • Kaphle A, Navya P N, Umapathi A, Daima H K (2018). Nanomaterials for agriculture, food and environment: applications, toxicity and regulation. Environmental Chemistry Letters, 16(1): 43–58

    Article  CAS  Google Scholar 

  • Keerthisinghe T P, Wang M, Zhang Y, Dong W, Fang M (2019). Low-dose tetracycline exposure alters gut bacterial metabolism and hostimmune response: “Personalized” effect? Environment International, 131: 104989

    Article  CAS  Google Scholar 

  • Levine A G (2014). Biosystems nanotechnology: Big opportunities in the science of the small. Science, 346(6211): 870

    Article  Google Scholar 

  • Lin W, Jiang R, Hu S, Xiao X, Wu J, Wei S, Xiong Y, Ouyang G (2019a). Investigating the toxicities of different functionalized polystyrene nanoplastics on Daphnia magna. Ecotoxicology and Environmental Safety, 180: 509–516

    Article  CAS  Google Scholar 

  • Lin W, Jiang R, Xiong Y, Wu J, Xu J, Zheng J, Zhu F, Ouyang G (2019b). Quantification of the combined toxic effect of polychlorinated biphenyls and nano-sized polystyrene on Daphnia magna. Journal of Hazardous Materials, 364: 531–536

    Article  CAS  Google Scholar 

  • Liu S, Fang S, Huang Y, Xiang Z, Ouyang G (2020). A heterogeneous pore decoration strategy on a hydrophobic microporous polymer for high-coverage capture of metabolites. Chemical Communications, 56 (52): 7167–7170

    Article  CAS  Google Scholar 

  • Liu S, Fang S, Xiang Z, Chen X, Song Y, Chen C, Ouyang G (2021). Combined effect of microplastics and DDT on microbial growth: A bacteriological and metabolomics investigation in Escherichia coli. Journal of Hazardous Materials, 407: 124849

    Article  CAS  Google Scholar 

  • Liu Y, Bhattarai P, Dai Z, Chen X (2019). Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chemical Society Reviews, 48(7): 2053–2108

    Article  CAS  Google Scholar 

  • Ma J, Sheng G D, Chen Q L, O’Connor P (2020). Do combined nanoscale polystyrene and tetracycline impact on the incidence of resistance genes and microbial community disturbance in Enchytraeus crypticus? Journal of Hazardous Materials, 387: 122012

    Article  CAS  Google Scholar 

  • Montet J C, Salmon L, Caroli-Bosc F X, Demarquay J F, Montet A M, Delmont J P (2000). L-arginine infusion protects against hyperammonemia and hepatic encephalopathy in cirrhotic patients with variceal haemorrhage. Gastroenterology, 118(4): A978

    Article  Google Scholar 

  • Mura S, Seddaiu G, Bacchini F, Roggero P P, Greppi G F (2013). Advances of nanotechnology in agro-environmental studies. Italian Journal of Agronomy, 8(3): 18

    Article  Google Scholar 

  • Musazzi U M, Franzè S, Minghetti P, Casiraghi A (2018). Emulsion versus nanoemulsion: How much is the formulative shift critical for a cosmetic product? Drug Delivery and Translational Research, 8(2): 414–421

    Article  CAS  Google Scholar 

  • Parsai T, Kumar A (2020). Tradeoff between risks through ingestion of nanoparticle contaminated water or fish: Human health perspective. Science of the Total Environment, 740: 140140

    Article  CAS  Google Scholar 

  • Ranjan S, Dasgupta N, Singh S, Gandhi M (2019). Toxicity and regulations of food nanomaterials. Environmental Chemistry Letters, 17(2): 929–944

    Article  CAS  Google Scholar 

  • Rillig M C, Lehmann A (2020). Microplastic in terrestrial ecosystems. Science, 368(6498): 1430–1431

    Article  CAS  Google Scholar 

  • Sekhon B S (2010). Food nanotechnology: An overview. Nanotechnology, Science and Applications, 3: 1–15

    CAS  Google Scholar 

  • Trevisan R, Voy C, Chen S, Di Giulio R T (2019). Nanoplastics decrease the toxicity of a complex PAH mixture but impair mitochondrial energy production in developing zebrafish. Environmental Science & Technology, 53(14): 8405–8415

    Article  CAS  Google Scholar 

  • van der Zande M, Jemec Kokalj A, Spurgeon D J, Loureiro S, Silva P V, Khodaparast Z, Drobne D, Clark N J, van den Brink N W, Baccaro M, van Gestel C A M, Bouwmeester H, Handy R D (2020). The gut barrier and the fate of engineered nanomaterials: A view from comparative physiology. Environmental Science. Nano, 7(7): 1874–1898

    Article  CAS  Google Scholar 

  • Weir A, Westerhoff P, Fabricius L, Hristovski K, von Goetz N (2012). Titanium dioxide nanoparticles in food and personal care products. Environmental Science & Technology, 46(4): 2242–2250

    Article  CAS  Google Scholar 

  • Yuan W, Wei Y, Zhang Y, Riaz L, Yang Q, Wang Q, Wang R (2021). Resistance of multidrug resistant Escherichia coli to environmental nanoscale TiO2 and ZnO. Science of the Total Environment, 761: 144303

    Article  CAS  Google Scholar 

  • Zhang Y, Keerthisinghe T P, Han Y, Liu M, Wanjaya E R, Fang M (2018). “Cocktail” of xenobiotics at human relevant levels reshapes the gut bacterial metabolome in a species-specific manner. Environmental Science & Technology, 52(19): 11402–11410

    Article  CAS  Google Scholar 

  • Zhang Z, Zhang R, Xiao H, Bhattacharya K, Bitounis D, Demokritou P, McClements D J (2019). Development of a standardized food model for studying the impact of food matrix effects on the gastrointestinal fate and toxicity of ingested nanomaterials. NanoImpact, 13: 13–25

    Article  Google Scholar 

  • Zhou J, Rao L, Yu G, Cook T R, Chen X, Huang F (2021). Supramolecular cancer nanotheranostics. Chemical Society Reviews, 50(4): 2839–2891

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge financial support from the projects of the National Natural Science Foundation of China (Nos. 22006143 and 21806189), the Science and Technology Program of Guangzhou (China) (No. 202102020601), the Natural Science Foundation of Guangdong Province (China) (No. 2021A1515012336), the Guangdong Provincial Key R&D Programme (China) (No. 2020B1111350002), and the special project of Guangdong Enterprise Science and Technology Commissioner (China) (No. GDKTP2021011600).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zhangmin Xiang or Shenghong Yang.

Additional information

Highlights

• Water-dispersible nano-pollutions exhibit type-specific toxic effects on E. coli.

• Global metabolite profiling was used to characterize metabolic disruption patterns.

• Key dysregulated metabolites responsive to nano-pollution exposures were found.

• Amino acid metabolism and purine metabolism are perturbed at nano-pollutions.

Supporting Materials

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Wu, R., Yang, X. et al. Water-dispersible nano-pollutions reshape microbial metabolism in type-specific manners: A metabolic and bacteriological investigation in Escherichia coli. Front. Environ. Sci. Eng. 16, 116 (2022). https://doi.org/10.1007/s11783-022-1548-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-022-1548-1

Keywords

Navigation