Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Environmental dimensions of the protein corona

Abstract

The adsorption of biomolecules to the surface of engineered nanomaterials, known as corona formation, defines their biological identity by altering their surface properties and transforming the physical, chemical and biological characteristics of the particles. In the first decade since the term protein corona was coined, studies have focused primarily on biomedical applications and human toxicity. The relevance of the environmental dimensions of the protein corona is still emerging. Often referred to as the eco-corona, a biomolecular coating forms upon nanomaterials as they enter the environment and may include proteins, as well as a diverse array of other biomolecules such as metabolites from cellular activity and/or natural organic matter. Proteins remain central in studies of eco-coronas because of the ease of monitoring and structurally characterizing proteins, as well as their crucial role in receptor engagement and signalling. The proteins within the eco-corona are optimal targets to establish the biophysicochemical principles of corona formation and transformation, as well as downstream impacts on nanomaterial uptake, distribution and impacts on the environment. Moreover, proteins appear to impart a biological identity, leading to cellular or organismal recognition of nanomaterials, a unique characteristic compared with natural organic matter. We contrast insights into protein corona formation from clinical samples with those in environmentally relevant systems. Principles specific to the environment are also explored to gain insights into the dynamics of interaction with or replacement by other biomolecules, including changes during trophic transfer and ecotoxicity. With many challenges remaining, we also highlight key opportunities for method development and impactful systems on which to focus the next phase of eco-corona studies. By interrogating these environmental dimensions of the protein corona, we offer a perspective on how mechanistic insights into protein coronas in the environment can lead to more sustainable, environmentally safe nanomaterials, as well as enhancing the efficacy of nanomaterials used in remediation and in the agri-food sector.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The evolution of scientific understanding of the bimolecular corona of nanoparticles.
Fig. 2: Properties that control protein corona formation.
Fig. 3: Eco-coronas can form outside or inside organisms.
Fig. 4: Protein coronas are formed upon ENM internalization by an organism.
Fig. 5: Tackling real-world environmental corona complexity.
Fig. 6: Analysis of the diversity of ENMs used in protein corona studies from 2007–2019.

References

  1. 1.

    Ke, P. C., Lin, S., Parak, W. J., Davis, T. P. & Caruso, F. A decade of the protein corona. ACS Nano 11, 11773–11776 (2017).

    CAS  Google Scholar 

  2. 2.

    Carrillo-Carrion, C., Carril, M. & Parak, W. J. Techniques for the experimental investigation of the protein corona. Curr. Opin. Biotechnol. 46, 106–113 (2017).

    CAS  Google Scholar 

  3. 3.

    Walkey, C. D. & Chan, W. C. W. W. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem. Soc. Rev. 41, 2780–2799 (2012).

    CAS  Google Scholar 

  4. 4.

    Treuel, L. & Nienhaus, G. U. Toward a molecular understanding of nanoparticle–protein interactions. Biophys. Rev. 4, 137–147 (2012).

    CAS  Google Scholar 

  5. 5.

    Payne, C. K. A protein corona primer for physical chemists. J. Chem. Phys. 151, 130901 (2019).

    Google Scholar 

  6. 6.

    Hadjidemetriou, M. & Kostarelos, K. Evolution of the nanoparticle corona. Nat. Nanotechnol. 12, 288–290 (2017). A review of corona formation from the medical perspective with a focus on the role of complement proteins, including effects on intended molecular recognition and role of corona in a range of biomedical applications.

    CAS  Google Scholar 

  7. 7.

    Nasser, F. & Lynch, I. Updating traditional regulatory tests for use with novel materials: nanomaterial toxicity testing with Daphnia magna. Saf. Sci. 118, 497–504 (2019).

    Google Scholar 

  8. 8.

    Tenzer, S. et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat. Nanotechnol. 8, 772–781 (2013).

    CAS  Google Scholar 

  9. 9.

    Markiewicz, M. et al. Changing environments and biomolecule coronas: consequences and challenges for the design of environmentally acceptable engineered nanoparticles. Green Chem. 20, 4133–4168 (2018). A comprehensive review of nanomaterial transformations under environmental conditions that summarizes trends in nanomaterial behaviour in the presence of natural organic matter based upon core composition.

    CAS  Google Scholar 

  10. 10.

    Grassi, G. et al. Proteomic profile of the hard corona of charged polystyrene nanoparticles exposed to sea urchin Paracentrotus lividus coelomic fluid highlights potential drivers of toxicity. Environ. Sci. Nano 6, 2937–2947 (2019).

    CAS  Google Scholar 

  11. 11.

    Svendsen, C. et al. Key principles and operational practices for improved nanotechnology environmental exposure assessment. Nat. Nanotechnol. 15, 731–742 (2020).

    CAS  Google Scholar 

  12. 12.

    Padín-González, E. et al. A custom-made functionalization method to control the biological identity of nanomaterials. Nanomedicine 29, 102268 (2020).

    Google Scholar 

  13. 13.

    Spielman-Sun, E. et al. Protein coating composition targets nanoparticles to leaf stomata and trichomes. Nanoscale 12, 3630–3636 (2020).

    CAS  Google Scholar 

  14. 14.

    Santana, I., Wu, H., Hu, P. & Giraldo, J. P. Targeted delivery of nanomaterials with chemical cargoes in plants enabled by a biorecognition motif. Nat. Commun. 11, 2045 (2020).

    CAS  Google Scholar 

  15. 15.

    Lowry, G. V., Gregory, K. B., Apte, S. C. & Lead, J. R. Transformations of nanomaterials in the environment. Environ. Sci. Technol. 46, 6893–6899 (2012).

    CAS  Google Scholar 

  16. 16.

    Fadare, O. O. et al. Eco-corona vs protein corona: effects of humic substances on corona formation and nanoplastic particle toxicity in Daphnia magna. Environ. Sci. Technol. 54, 8001–8009 (2020).

    CAS  Google Scholar 

  17. 17.

    Chetwynd, A. J. & Lynch, I. The rise of the nanomaterial metabolite corona, and emergence of the complete corona. Environ. Sci. Nano 7, 1041–1060 (2020).

    CAS  Google Scholar 

  18. 18.

    Chetwynd, A. J., Zhang, W., Thorn, J. A., Lynch, I. & Ramautar, R. The nanomaterial metabolite corona determined using a quantitative metabolomics approach: a pilot study. Small 16, 2000295 (2020).

    CAS  Google Scholar 

  19. 19.

    Kahru, A. & Ivask, A. Mapping the dawn of nanoecotoxicological research. Acc. Chem. Res. 46, 823–833 (2013).

    CAS  Google Scholar 

  20. 20.

    Lynch, I., Dawson, K. A., Lead, J. R. & Valsami-Jones, E. in Frontiers of Nanoscience (eds. Lead, J. R. & Valsami-Jones, E.) 127–156 (Elsevier, 2014).

  21. 21.

    Tollefson, E. J. et al. Preferential binding of cytochrome c to anionic ligand-coated gold nanoparticles: a complementary computational and experimental approach. ACS Nano 13, 6856–6866 (2019).

    CAS  Google Scholar 

  22. 22.

    Daly, C. A. et al. Surface coating structure and its interaction with cytochrome c in eg6-coated nanoparticles varies with surface curvature. Langmuir 36, 5030–5039 (2020).

    CAS  Google Scholar 

  23. 23.

    Kim, J. & Doudrick, K. Emerging investigator series: protein adsorption and transformation on catalytic and food-grade TiO2 nanoparticles in the presence of dissolved organic carbon. Environ. Sci. Nano 6, 1688–1703 (2019).

    CAS  Google Scholar 

  24. 24.

    Shakiba, S., Hakimian, A., Barco, L. R. & Louie, S. M. Dynamic intermolecular interactions control adsorption from mixtures of natural organic matter and protein onto titanium dioxide nanoparticles. Environ. Sci. Technol. 52, 14158–14165 (2018). Mechanistic insight into the formation of a complex eco-corona that includes both natural organic matter and proteins, including characterization of simultaneous versus sequential exposure on resulting eco-corona composition.

    CAS  Google Scholar 

  25. 25.

    Mudunkotuwa, I. A. & Grassian, V. H. Biological and environmental media control oxide nanoparticle surface composition: the roles of biological components (proteins and amino acids), inorganic oxyanions and humic acid. Environ. Sci. Nano 2, 429–439 (2015).

    CAS  Google Scholar 

  26. 26.

    Wan, S. et al. The ‘sweet’ side of the protein corona: effects of glycosylation on nanoparticle–cell interactions. ACS Nano 9, 2157–2166 (2015).

    CAS  Google Scholar 

  27. 27.

    Ghazaryan, A., Landfester, K. & Mailänder, V. Protein deglycosylation can drastically affect the cellular uptake. Nanoscale 11, 10727–10737 (2019).

    CAS  Google Scholar 

  28. 28.

    Corbo, C., Molinaro, R., Tabatabaei, M., Farokhzad, O. C. & Mahmoudi, M. Personalized protein corona on nanoparticles and its clinical implications. Biomater. Sci. 5, 378–387 (2017).

    CAS  Google Scholar 

  29. 29.

    Chetwynd, A. J., Wheeler, K. E. & Lynch, I. Best practice in reporting corona studies: minimum information about Nanomaterial Biocorona Experiments (MINBE). Nano Today 28, 100758 (2019). Reporting guidelines to ensure high-fidelity data collection of protein corona composition to ensure reproducibility and maximize data re-usage for modelling studies in the long term.

    CAS  Google Scholar 

  30. 30.

    Gunawan, C., Lim, M., Marquis, C. P. & Amal, R. Nanoparticle–protein corona complexes govern the biological fates and functions of nanoparticles. J. Mater. Chem. B 2, 2060–2083 (2014).

    CAS  Google Scholar 

  31. 31.

    Lundqvist, M. et al. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc. Natl Acad. Sci. USA 105, 14265–14270 (2008).

    CAS  Google Scholar 

  32. 32.

    Zhang, H. et al. Quantitative proteomics analysis of adsorbed plasma proteins classifies nanoparticles with different surface properties and size. Proteomics 11, 4569–4577 (2011).

    CAS  Google Scholar 

  33. 33.

    Ruiz, G., Tripathi, K., Okyem, S. & Driskell, J. D. pH impacts the orientation of antibody adsorbed onto gold nanoparticles. Bioconjug. Chem. 30, 1182–1191 (2019).

    CAS  Google Scholar 

  34. 34.

    Mahmoudi, M. et al. Temperature: the ‘ignored’ factor at the nanobio interface. ACS Nano 7, 6555–6562 (2013).

    CAS  Google Scholar 

  35. 35.

    Goy-López, S. et al. Physicochemical characteristics of protein–NP bioconjugates: the role of particle curvature and solution conditions on human serum albumin conformation and fibrillogenesis inhibition. Langmuir 28, 9113–9126 (2012).

    Google Scholar 

  36. 36.

    Dutz, S., Wojahn, S., Gräfe, C., Weidner, A. & Clement, J. H. Influence of sterilization and preservation procedures on the integrity of serum protein-coated magnetic nanoparticles. Nanomaterials 7, 453 (2017).

    Google Scholar 

  37. 37.

    Eigenheer, R. et al. Silver nanoparticle protein corona composition compared across engineered particle properties and environmentally relevant reaction conditions. Environ. Sci. Nano 1, 238–247 (2014).

    CAS  Google Scholar 

  38. 38.

    Jayaram, D. T., Pustulka, S. M., Mannino, R. G., Lam, W. A. & Payne, C. K. Protein corona in response to flow: effect on protein concentration and structure. Biophys. J. 115, 209–216 (2018).

    CAS  Google Scholar 

  39. 39.

    Gonçalves, S. P. C. et al. in Nanomaterials Applications for Environmental Matrices, 265–304 (Elsevier, 2019).

  40. 40.

    Zhang, P. et al. Protein corona between nanoparticles and bacterial proteins in activated sludge: characterization and effect on nanoparticle aggregation. Bioresour. Technol. 250, 10–16 (2018).

    CAS  Google Scholar 

  41. 41.

    Surette, M. C. & Nason, J. A. Nanoparticle aggregation in a freshwater river: the role of engineered surface coatings. Environ. Sci. Nano 6, 540–553 (2019).

    CAS  Google Scholar 

  42. 42.

    Uddin, M. D. N., Desai, F. & Asmatulu, E. Engineered nanomaterials in the environment: bioaccumulation, biomagnification and biotransformation. Environ. Chem. Lett. 18, 1073–1083 (2020).

    CAS  Google Scholar 

  43. 43.

    Yue, Y. et al. Silver nanoparticle-protein interactions in intact rainbow trout gill cells. Environ. Sci. Nano 3, 1174–1185 (2016). Novel approach to characterization of the protein corona from rainbow trout gill cells to reveal nanoparticle fate through centrifugal subcellular fractionation and corona characterization of particles in the endosomes/lysosomes versus on those associated with the cell membrane, mitochondria and nucleus.

    CAS  Google Scholar 

  44. 44.

    Canesi, L. et al. Interactions of cationic polystyrene nanoparticles with marine bivalve hemocytes in a physiological environment: role of soluble hemolymph proteins. Environ. Res. 150, 73–81 (2016).

    CAS  Google Scholar 

  45. 45.

    Gebauer, J. S. et al. Impact of the nanoparticle–protein corona on colloidal stability and protein structure. Langmuir 28, 9673–9679 (2012).

    CAS  Google Scholar 

  46. 46.

    Xie, C. et al. Bacillus subtilis causes dissolution of ceria nanoparticles at the nano-bio interface. Environ. Sci. Nano 6, 216–223 (2019).

    CAS  Google Scholar 

  47. 47.

    Jayaram, D. T., Runa, S., Kemp, M. L. & Payne, C. K. Nanoparticle-induced oxidation of corona proteins initiates an oxidative stress response in cells. Nanoscale 9, 7595–7601 (2017).

    CAS  Google Scholar 

  48. 48.

    Martinolich, A. J., Park, G., Nakamoto, M. Y., Gate, R. E. & Wheeler, K. E. Structural and functional effects of Cu metalloprotein-driven silver nanoparticle dissolution. Environ. Sci. Technol. 46, 6355–6362 (2012).

    CAS  Google Scholar 

  49. 49.

    Albanese, A. et al. Secreted biomolecules alter the biological identity and cellular interactions of nanoparticles. ACS Nano 8, 5515–5526 (2014).

    CAS  Google Scholar 

  50. 50.

    Li, J. et al. Self-assembly of plant protein fibrils interacting with superparamagnetic iron oxide nanoparticles. Sci. Rep. 9, 8939 (2019).

    Google Scholar 

  51. 51.

    Akanbi, M. O., Hernandez, L. M., Mobarok, M. H., Veinot, J. G. C. & Tufenkji, N. QCM-D and NanoTweezer measurements to characterize the effect of soil cellulase on the deposition of PEG-coated TiO2 nanoparticles in model subsurface environments. Environ. Sci. Nano 5, 2172–2183 (2018).

    CAS  Google Scholar 

  52. 52.

    Canesi, L. et al. Biomolecular coronas in invertebrate species: implications in the environmental impact of nanoparticles. NanoImpact 8, 89–98 (2017).

    Google Scholar 

  53. 53.

    Nasser, F. & Lynch, I. Secreted protein eco-corona mediates uptake and impacts of polystyrene nanoparticles on Daphnia magna. J. Proteom. 137, 45–51 (2016).

    CAS  Google Scholar 

  54. 54.

    Pink, M., Verma, N., Kersch, C. & Schmitz-Spanke, S. Identification and characterization of small organic compounds within the corona formed around engineered nanoparticles. Environ. Sci. Nano. 5, 1420–1427 (2018).

    CAS  Google Scholar 

  55. 55.

    Balbi, T. et al. Photocatalytic Fe-doped n-TiO2: from synthesis to utilization of in vitro cell models for screening human and environmental nanosafety. Resour. Effic. Technol. 3, 158–165 (2017).

    Google Scholar 

  56. 56.

    Hayashi, Y. et al. Species differences take shape at nanoparticles: protein corona made of the native repertoire assists cellular interaction. Environ. Sci. Technol. 47, 14367–14375 (2013). Characterization of a species-specific response to the protein corona, whereby particles coated with native proteins were preferentially taken up compared to those with a non-native protein corona, highlighting the requirement for a more holistic approach to the eco-corona due to the wide species diversity in the environment.

    CAS  Google Scholar 

  57. 57.

    Natarajan, L., Jenifer, M. A. & Mukherjee, A. Eco-corona formation on the nanomaterials in the aquatic systems lessens their toxic impact: a comprehensive review. Environ. Res. 194, 110669 (2021).

    CAS  Google Scholar 

  58. 58.

    Ellis, L.-J. A. & Lynch, I. Mechanistic insights into toxicity pathways induced by nanomaterials in Daphnia magna from analysis of the composition of the acquired protein corona. Environ. Sci. Nano 7, 3343–3359 (2020). Eco-corona composition acquired by nanomaterials from biomolecules secreted into the medium by the organisms provides mechanistic insights into the organisms’ response to exposure to the nanomaterials.

    CAS  Google Scholar 

  59. 59.

    Bourgeault, A. et al. Interaction of TiO2 nanoparticles with proteins from aquatic organisms: the case of gill mucus from blue mussel. Environ. Sci. Pollut. Res. 24, 13474–13483 (2017).

    CAS  Google Scholar 

  60. 60.

    Della Torre, C. et al. Titanium dioxide nanoparticles modulate the toxicological response to cadmium in the gills of Mytilus galloprovincialis. J. Hazard. Mater. 297, 92–100 (2015).

    Google Scholar 

  61. 61.

    Alijagic, A., Benada, O., Kofroňová, O., Cigna, D. & Pinsino, A. Sea urchin extracellular proteins design a complex protein corona on titanium dioxide nanoparticle surface influencing immune cell behavior. Front. Immunol. 10, 2261 (2019).

    CAS  Google Scholar 

  62. 62.

    Hayashi, Y. et al. Nanosilver pathophysiology in earthworms: transcriptional profiling of secretory proteins and the implication for the protein corona. Nanotoxicology 10, 303–311 (2016). Transcriptional approaches are integrated with insights into the corona composition to reveal a mechanism of earthworm response to nanomaterials in their local environment.

    CAS  Google Scholar 

  63. 63.

    Hayashi, Y. et al. Female versus male biological identities of nanoparticles determine the interaction with immune cells in fish. Environ. Sci. Nano 4, 895–906 (2017).

    CAS  Google Scholar 

  64. 64.

    Gao, J., Lin, L., Wei, A. & Sepúlveda, M. S. Protein corona analysis of silver nanoparticles exposed to fish plasma. Environ. Sci. Technol. Lett. 4, 174–179 (2017).

    CAS  Google Scholar 

  65. 65.

    Canesi, L. & Procházková, P. in Nanoparticles and the Immune System: Safety and Effects 91–112 (Academic, 2013).

  66. 66.

    Ostermeyer, A.-K., Kostigen Mumuper, C., Semprini, L. & Radniecki, T. Influence of bovine serum albumin and alginate on silver nanoparticle dissolution and toxicity to Nitrosomonas europaea. Environ. Sci. Technol. 47, 14403–14410 (2013).

    CAS  Google Scholar 

  67. 67.

    Grintzalis, K., Lawson, T. N., Nasser, F., Lynch, I. & Viant, M. R. Metabolomic method to detect a metabolite corona on amino-functionalized polystyrene nanoparticles. Nanotoxicology 13, 783–794 (2019).

    CAS  Google Scholar 

  68. 68.

    Lee, J. Y. et al. Analysis of lipid adsorption on nanoparticles by nanoflow liquid chromatography–tandem mass spectrometry. Anal. Bioanal. Chem. 410, 6155–6164 (2018).

    CAS  Google Scholar 

  69. 69.

    Xu, S. et al. MiRNA extraction from cell-free biofluid using protein corona formed around carboxyl magnetic nanoparticles. ACS Biomater. Sci. Eng. 4, 654–662 (2018).

    CAS  Google Scholar 

  70. 70.

    Griffith, D. M., Jayaram, D. T., Spencer, D. M., Pisetsky, D. S. & Payne, C. K. DNA-nanoparticle interactions: Formation of a DNA corona and its effects on a protein corona. Biointerphases 15, 051006 (2020). One of the first papers to demonstrate that DNA forms a part of the biomolecular corona and may offer a potential method of genetic material transfer between organisms.

    CAS  Google Scholar 

  71. 71.

    Gorshkov, V., Bubis, J. A., Solovyeva, E. M., Gorshkov, M. V. & Kjeldsen, F. Protein corona formed on silver nanoparticles in blood plasma is highly selective and resistant to physicochemical changes of the solution. Environ. Sci. Nano 6, 1089–1098 (2019).

    CAS  Google Scholar 

  72. 72.

    Lundqvist, M. et al. The evolution of the protein corona around nanoparticles: a test study. ACS Nano 5, 7503–7509 (2011).

    CAS  Google Scholar 

  73. 73.

    Lynch, I., Dawson, K. A. & Linse, S. Detecting cryptic epitopes created by nanoparticles. Sci. STKE 327, pe14 (2006).

    Google Scholar 

  74. 74.

    Pisani, C. et al. The species origin of the serum in the culture medium influences the in vitro toxicity of silica nanoparticles to HepG2 cells. PLoS ONE 12, 1–17 (2017).

    Google Scholar 

  75. 75.

    Serpooshan, V. et al. Effect of cell sex on uptake of nanoparticles: the overlooked factor at the nanobio interface. ACS Nano 12, 2253–2266 (2018).

    CAS  Google Scholar 

  76. 76.

    Gardea-Torresdey, J. L., Rico, C. M. & White, J. C. Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environments. Environ. Sci. Technol. 48, 2526–2540 (2014).

    CAS  Google Scholar 

  77. 77.

    Unrine, J. M., Shoults-Wilson, W. A., Zhurbich, O., Bertsch, P. M. & Tsyusko, O. V. Trophic transfer of Au nanoparticles from soil along a simulated terrestrial food chain. Environ. Sci. Technol. 46, 9753–9760 (2012).

    CAS  Google Scholar 

  78. 78.

    Tangaa, S. R., Selck, H., Winther-Nielsen, M. & Khan, F. R. Trophic transfer of metal-based nanoparticles in aquatic environments: a review and recommendations for future research focus. Environ. Sci. Nano 3, 966–981 (2016).

    CAS  Google Scholar 

  79. 79.

    Walkey, C. D. et al. Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano 8, 2439–2455 (2014).

    CAS  Google Scholar 

  80. 80.

    Tavanti, F., Pedone, A. & Menziani, M. C. Competitive binding of proteins to gold nanoparticles disclosed by molecular dynamics simulations. J. Phys. Chem. C 119, 22172–22180 (2015).

    CAS  Google Scholar 

  81. 81.

    Findlay, M. R., Freitas, D. N., Mobed-Miremadi, M. & Wheeler, K. E. Machine learning provides predictive analysis into silver nanoparticle protein corona formation from physicochemical properties. Environ. Sci. Nano 5, 64–71 (2018).

    CAS  Google Scholar 

  82. 82.

    Ban, Z. et al. Machine learning predicts the functional composition of the protein corona and the cellular recognition of nanoparticles. Proc. Natl Acad. Sci. USA 117, 10492–10499 (2020).

    CAS  Google Scholar 

  83. 83.

    Duan, Y. et al. Prediction of protein corona on nanomaterials by machine learning using novel descriptors. NanoImpact 17, 100207 (2020).

    Google Scholar 

  84. 84.

    Hajipour, M. J., Laurent, S., Aghaie, A., Rezaee, F. & Mahmoudi, M. Personalized protein coronas: a ‘key’ factor at the nanobiointerface. Biomater. Sci. 2, 1210–1221 (2014).

    CAS  Google Scholar 

  85. 85.

    Tavakol, M. et al. Disease-related metabolites affect protein–nanoparticle interactions. Nanoscale 10, 7108–7115 (2018).

    CAS  Google Scholar 

  86. 86.

    Tekie, F. S. M. et al. Controlling evolution of protein corona: a prosperous approach to improve chitosan-based nanoparticle biodistribution and half-life. Sci. Rep. 10, 9664 (2020).

    Google Scholar 

  87. 87.

    Mosquera, J. et al. Reversible control of protein corona formation on gold nanoparticles using host–guest interactions. ACS Nano 14, 5382–5391 (2020).

    CAS  Google Scholar 

  88. 88.

    Williams, R. M. et al. Harnessing nanotechnology to expand the toolbox of chemical biology. Nat. Chem. Bio. 17, 129–137 (2021).

    CAS  Google Scholar 

  89. 89.

    Geitner, N. K. et al. Harmonizing across environmental nanomaterial testing media for increased comparability of nanomaterial datasets. Environ. Sci. Nano 7, 13–36 (2020).

    CAS  Google Scholar 

  90. 90.

    Blume, J. E. et al. Rapid, deep and precise profiling of the plasma proteome with multi-nanoparticle protein corona. Nat. Commun. 11, 3662 (2020).

    CAS  Google Scholar 

  91. 91.

    Liu, R., Jiang, W., Walkey, C. D., Chan, W. C. W. & Cohen, Y. Prediction of nanoparticles-cell association based on corona proteins and physicochemical properties. Nanoscale 7, 9664–9675 (2015).

    CAS  Google Scholar 

  92. 92.

    Singh, N. et al. In vivo protein corona on nanoparticles: does the control of all material parameters orient the biological behavior? Nanoscale Adv. 3, 2109–1229 (2021).

    Google Scholar 

  93. 93.

    Leong, H. S. et al. On the issue of transparency and reproducibility in nanomedicine. Nat. Nanotechnol. 14, 629–635 (2019).

    CAS  Google Scholar 

  94. 94.

    Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. How many species are there on Earth and in the ocean? PLoS Biol. 9, e1001127 (2011).

    CAS  Google Scholar 

  95. 95.

    The UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 45, D158–D169 (2017).

    Google Scholar 

  96. 96.

    Wigginton, N. S. et al. Binding of silver nanoparticles to bacterial proteins depends on surface modifications and inhibits enzymatic activity. Environ. Sci. Technol. 44, 2163–2168 (2010).

    CAS  Google Scholar 

  97. 97.

    Müller, L. K. et al. The transferability from animal models to humans: challenges regarding aggregation and protein corona formation of nanoparticles. Biomacromolecules 19, 374–385 (2018).

    Google Scholar 

  98. 98.

    Keller, A. A., McFerran, S., Lazareva, A. & Suh, S. Global life cycle releases of engineered nanomaterials. J. Nanopart. Res. 15, 1692 (2013).

    Google Scholar 

  99. 99.

    Bundschuh, M. et al. Nanoparticles in the environment: where do we come from, where do we go to. Environ. Sci. Eur. 30, 6 (2018).

    Google Scholar 

  100. 100.

    Pradas del Real, A. E. et al. Fate of Ag-NPs in sewage sludge after application on agricultural soils. Environ. Sci. Technol. 50, 1759–1768 (2016).

    CAS  Google Scholar 

  101. 101.

    Bakshi, M. et al. Assessing the impacts of sewage sludge amendment containing nano-TiO2 on tomato plants: a life cycle study. J. Hazard. Mater. 369, 191–198 (2019).

    CAS  Google Scholar 

  102. 102.

    Vieira, S. et al. Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands. ISME J. 14, 463–475 (2020).

    CAS  Google Scholar 

  103. 103.

    Zhang, P. et al. Nanomaterial transformation in the soil–plant system: implications for food safety and application in agriculture. Small 16, 2000705 (2020).

    CAS  Google Scholar 

  104. 104.

    Lv, J., Christie, P. & Zhang, S. Uptake, translocation, and transformation of metal-based nanoparticles in plants: recent advances and methodological challenges. Environ. Sci. Nano 6, 41–59 (2019).

    CAS  Google Scholar 

  105. 105.

    Giraldo, J. P., Wu, H., Newkirk, G. M. & Kruss, S. Nanobiotechnology approaches for engineering smart plant sensors. Nat. Nanotechnol. 14, 541–553 (2019).

    CAS  Google Scholar 

  106. 106.

    Natarajan, L. et al. Eco-corona formation lessens the toxic effects of polystyrene nanoplastics towards marine microalgae Chlorella sp. Environ. Res. 188, 109842 (2020).

    CAS  Google Scholar 

  107. 107.

    Grassi, G. et al. Interplay between extracellular polymeric substances (EPS) from a marine diatom and model nanoplastic through eco-corona formation. Sci. Total Environ. 725, 138457 (2020).

    CAS  Google Scholar 

  108. 108.

    Stamps, B. W. et al. Municipal solid waste landfills harbor distinct microbiomes. Front. Microbiol. 7, 335–336 (2016).

    Google Scholar 

  109. 109.

    Shaw, C. A. et al. Protein corona formation in bronchoalveolar fluid enhances diesel exhaust nanoparticle uptake and pro-inflammatory responses in macrophages. Nanotoxicology 10, 981–991 (2016).

    CAS  Google Scholar 

  110. 110.

    Zhang, Y. et al. Atmospheric microplastics: a review on current status and perspectives. Earth Sci. Rev. 203, 103118 (2020).

    CAS  Google Scholar 

  111. 111.

    Konduru, N. V. et al. Protein corona: implications for nanoparticle interactions with pulmonary cells. Part. Fibre Toxicol. 14, 42 (2017).

    Google Scholar 

  112. 112.

    Archer, S. D. J. & Pointing, S. B. Anthropogenic impact on the atmospheric microbiome. Nat. Microbiol. 5, 229–231 (2020).

    CAS  Google Scholar 

  113. 113.

    DeLeon-Rodriguez, N. et al. Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc. Natl Acad. Sci. USA 110, 2575–2580 (2013).

    CAS  Google Scholar 

  114. 114.

    Christner, B. C., Morris, C. E., Foreman, C. M., Cai, R. & Sands, D. C. Ubiquity of biological ice nucleators in snowfall. Science 319, 1214–1214 (2008).

    CAS  Google Scholar 

  115. 115.

    Keller, A. A. & Lazareva, A. Predicted releases of engineered nanomaterials: from global to regional to local. Environ. Sci. Technol. Lett. 1, 65–70 (2014).

    CAS  Google Scholar 

  116. 116.

    Surette, M. C., Nason, J. A. & Kaegi, R. The influence of surface coating functionality on the aging of nanoparticles in wastewater. Environ. Sci. Nano 6, 2470–2483 (2019).

    CAS  Google Scholar 

  117. 117.

    Wimmer, A., Markus, A. A. & Schuster, M. Silver nanoparticle levels in river water: real environmental measurements and modeling approaches—a comparative study. Environ. Sci. Technol. Lett. 6, 353–358 (2019).

    CAS  Google Scholar 

  118. 118.

    Kaegi, R. et al. Fate and transformation of silver nanoparticles in urban wastewater systems. Water Res. 47, 3866–3877 (2013).

    CAS  Google Scholar 

  119. 119.

    Sharma, V. K., Filip, J., Zboril, R. & Varma, R. S. Natural inorganic nanoparticles—formation, fate, and toxicity in the environment. Chem. Soc. Rev. 44, 8410–8423 (2015).

    CAS  Google Scholar 

  120. 120.

    Lespes, G., Faucher, S. & Slaveykova, V. I. Natural nanoparticles, anthropogenic nanoparticles, where is the frontier? Front. Environ. Sci. 8, 71 (2020).

  121. 121.

    Akdogan, Z. & Guven, B. Microplastics in the environment: a critical review of current understanding and identification of future research needs. Environ. Pollut. 254, 113011 (2019).

    CAS  Google Scholar 

  122. 122.

    Machado, A. A. et al. Microplastics as an emerging threat to terrestrial ecosystems. Glob. Change Biol. 24, 1405–1416 (2018).

    Google Scholar 

  123. 123.

    Dawson, A. et al. Uptake and depuration kinetics influence microplastic bioaccumulation and toxicity in Antarctic krill (Euphausia superba). Environ. Sci. Technol. 52, 3195–3201 (2018).

    CAS  Google Scholar 

  124. 124.

    Alava, J. J. Modeling the bioaccumulation and biomagnification potential of microplastics in a cetacean foodweb of the northeastern pacific: a prospective tool to assess the risk exposure to plastic particles. Front. Mar. Sci. 7, 566101 (2020).

    Google Scholar 

  125. 125.

    Gopinath, P. M. et al. Assessment on interactive prospectives of nanoplastics with plasma proteins and the toxicological impacts of virgin, coronated and environmentally released-nanoplastics. Sci. Rep. 9, 8860 (2019).

    Google Scholar 

  126. 126.

    Ma, Y. et al. Effects of nanoplastics and microplastics on toxicity, bioaccumulation, and environmental fate of phenanthrene in fresh water. Environ. Pollut. 219, 166–173 (2016).

    CAS  Google Scholar 

  127. 127.

    Guo, H., Zheng, X., Luo, X. & Mai, B. Leaching of brominated flame retardants (BFRs) from BFRs-incorporated plastics in digestive fluids and the influence of bird diets. J. Hazard. Mater. 393, 122397 (2020).

    CAS  Google Scholar 

  128. 128.

    Rochman, C. M., Hoh, E., Kurobe, T. & Teh, S. J. Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci. Rep. 3, 3263 (2013).

    Google Scholar 

  129. 129.

    Buchman, J. T. et al. Nickel enrichment of next-generation NMC nanomaterials alters material stability, causing unexpected dissolution behavior and observed toxicity to S. oneidensis MR-1 and D. magna. Environ. Sci. Nano 7, 571–587 (2020).

    CAS  Google Scholar 

  130. 130.

    Ma, Y., White, J. C., Dhankher, O. M. & Xing, B. Metal-based nanotoxicity and detoxification pathways in higher plants. Environ. Sci. Technol. 49, 7109–7122 (2015). Lays the groundwork for investigation of nanomaterial pathways through plants and induction of toxic responses and/or detoxification mechanisms that will inform future work in plant protein corona studies.

    CAS  Google Scholar 

Download references

Acknowledgements

K.E.W., K.M.F. and B.S.H. acknowledge support from the Henry Dreyfus Teacher-Scholar Awards Program, the Jean Dreyfus Lectureship for Undergraduate Institutions and the DeNardo Scholars Program, respectively. A.J.C. and I.L. acknowledge funding from the European Union Horizon 2020 project ACEnano (grant agreement no. 720952) and H2020 research infrastructure project NanoCommons (grant agreement no. 731032) and the Natural Environment Research Council (NE/N006569/1).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Korin E. Wheeler.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Nanotechnology thanks Ilaria Corsi and Kristin Schirmer for their contribution to the peer review of this work.

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

Verify currency and authenticity via CrossMark

Cite this article

Wheeler, K.E., Chetwynd, A.J., Fahy, K.M. et al. Environmental dimensions of the protein corona. Nat. Nanotechnol. 16, 617–629 (2021). https://doi.org/10.1038/s41565-021-00924-1

Download citation

Search

Quick links

Find nanotechnology articles, nanomaterial data and patents all in one place. Visit Nano by Nature Research