Skip to main content
SpringerLink
Log in

Inorganic nanoparticles and the microbiome

  • Review Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

Routine exposure to inorganic nanoparticles (NPs) that are incorporated into consumer products such as foods/drinks, packaging materials, pharmaceuticals, and personal care products (e.g. cosmetics, sunscreens, shampoos) occurs on a daily basis. The standard everyday use of these products facilitates interactions between the incorporated inorganic NPs, mammalian tissues (e.g. skin, gastrointestinal tract, oral cavity), and the community of microbes that resides on these tissues. Changes to the microbiome have been linked to the initiation/ progression of many diseases and there is a growing interest focused on understanding how inorganic NPs can initiate these changes. As these mechanisms are revealed and defined, it may be possible to rationally design microbiotamodulating therapies based on inorganic NPs. In this article, we will: (i) provide a background on inorganic NPs that are commonly found in consumer products such as those that incorporate titanium, zinc, silver, silica, or iron, (ii) discuss how NP properties, microbiota composition, and the physiological microenvironment can mediate the effects that inorganic NPs have on the microbiota, and (iii) highlight opportunities for inorganic NP therapies that are designed to interact with, and navigate, the microbiome.

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

Similar content being viewed by others

References

  1. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207–214.

  2. Gibson, G. R.; Roberfroid, M. B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401–1412.

    Google Scholar 

  3. Ubeda, C.; Pamer, E. G. Antibiotics, microbiota, and immune defense. Trends Immunol. 2012, 33, 459–466.

    Google Scholar 

  4. Belizário, J. E.; Napolitano, M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front. Microbiol. 2015, 6, 1050.

    Google Scholar 

  5. Carding, S.; Verbeke, K.; Vipond, D. T.; Corfe, B. M.; Owen, L. J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 2015, 26, 26191.

    Google Scholar 

  6. Wen, L.; Ley, R. E.; Volchkov, P. Y.; Stranges, P. B.; Avanesyan, L.; Stonebraker, A. C.; Hu, C. Y.; Wong, F. S.; Szot, G. L.; Bluestone, J. A. et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455, 1109–1113.

    Google Scholar 

  7. Manichanh, C.; Borruel, N.; Casellas, F.; Guarner, F. The gut microbiota in IBD. Nat. Rev. Gastroenterol. Hepatol. 2012, 9, 599–608.

    Google Scholar 

  8. Sears, C. L.; Garrett, W. S. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014, 15, 317–328.

    Google Scholar 

  9. Chang, C.; Lin, H. Dysbiosis in gastrointestinal disorders. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 3–15.

    Google Scholar 

  10. Derrien, M.; van Hylckama Vlieg, J. E. T. Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol. 2015, 23, 354–366.

    Google Scholar 

  11. Meadow, J. F.; Bateman, A. C.; Herkert, K. M.; O’Connor, T. K.; Green, J. L. Significant changes in the skin microbiome mediated by the sport of roller derby. PeerJ 2013, 1, e53.

    Google Scholar 

  12. Dickson, R. P.; Huffnagle, G. B. The lung microbiome: New principles for respiratory bacteriology in health and disease. PLoS Pathog. 2015, 11, e1004923.

    Google Scholar 

  13. David, L. A.; Maurice, C. F.; Carmody, R. N.; Gootenberg, D. B.; Button, J. E.; Wolfe, B. E.; Ling, A. V.; Devlin, A. S.; Varma, Y.; Fischbach, M. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563.

    Google Scholar 

  14. Arumugam, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D. R.; Fernandes, G. R.; Tap, J.; Bruls, T.; Batto, J. M. et al. Enterotypes of the human gut microbiome. Nature 2011, 473, 174–180.

    Google Scholar 

  15. Grice, E. A.; Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 2011, 9, 244–253.

    Google Scholar 

  16. Dewhirst, F. E.; Chen, T.; Izard, J.; Paster, B. J.; Tanner, A. C.; Yu, W.–H.; Lakshmanan, A.; Wade, W. G. The human oral microbiome. J. Bacteriol. 2010, 192, 5002–5017.

    Google Scholar 

  17. Man, W. H.; de Steenhuijsen Piters, W. A. A.; Bogaert, D. The microbiota of the respiratory tract: Gatekeeper to respiratory health. Nat. Rev. Microbiol. 2017, 15, 259–270.

    Google Scholar 

  18. Maier, L.; Pruteanu, M.; Kuhn, M.; Zeller, G.; Telzerow, A.; Anderson, E. E.; Brochado, A. R.; Fernandez, K. C.; Dose, H.; Mori, H. et al. Extensive impact of non–antibiotic drugs on human gut bacteria. Nature 2018, 555, 623–628.

    Google Scholar 

  19. McClements, D. J.; Xiao, H. Is nano safe in foods? Establishing the factors impacting the gastrointestinal fate and toxicity of organic and inorganic food–grade nanoparticles. npj Sci. Food 2017, 1, 6.

    Google Scholar 

  20. Vance, M. E.; Kuiken, T.; Vejerano, E. P.; McGinnis, S. P.; Hochella Jr, M. F.; Rejeski, D.; Hull, M. S. Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. Beilst. J. Nanotechnol. 2015, 6, 1769–1780.

    Google Scholar 

  21. Hajipour, M. J.; Fromm, K. M.; Ashkarran, A. A.; de Aberasturi, D. J.; de Larramendi, I. R.; Rojo, T.; Serpooshan, V.; Parak, W. J.; Mahmoudi, M. Antibacterial properties of nanoparticles. Trends Biotechnol. 2012, 30, 499–511.

    Google Scholar 

  22. Miller, K. P.; Wang, L.; Benicewicz, B. C.; Decho, A. W. Inorganic nanoparticles engineered to attack bacteria. Chem. Soc. Rev. 2015, 44, 7787–7807.

    Google Scholar 

  23. Bouwmeester, H.; van der Zande, M.; Jepson, M. A. Effects of food–borne nanomaterials on gastrointestinal tissues and microbiota. WIREs Nanomed. Nanobiotechnol. 2018, 10, e1481.

    Google Scholar 

  24. Raj, S.; Jose, S.; Sumod, U. S.; Sabitha, M. Nanotechnology in cosmetics: Opportunities and challenges. J. Pharm. Bioallied Sci. 2012, 4, 186–193.

    Google Scholar 

  25. Cushen, M.; Kerry, J.; Morris, M.; Cruz–Romero, M.; Cummins, E. Nanotechnologies in the food industry— Recent developments, risks and regulation. Trends Food Sci. Technol. 2012, 24, 30–46.

    Google Scholar 

  26. Lohse, S. E.; Murphy, C. J. Applications of colloidal inorganic nanoparticles: From medicine to energy. J. Am. Chem. Soc. 2012, 134, 15607–15620.

    Google Scholar 

  27. Auffan, M.; Rose, J.; Bottero, J.–Y.; Lowry, G. V.; Jolivet, J.–P.; Wiesner, M. R. Towards a definition of inorganic nanoparticles from an environmental, health and safety perspective. Nat. Nanotechnol. 2009, 4, 634–641.

    Google Scholar 

  28. Sun, Y.; Rogers, J. A. Inorganic semiconductors for flexible electronics. Adv. Mater. 2007, 19, 1897–1916.

    Google Scholar 

  29. Liong, M.; Lu, J.; Kovochich, M.; Xia, T.; Ruehm, S. G.; Nel, A. E.; Tamanoi, F.; Zink, J. I. Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano 2008, 2, 889–896.

    Google Scholar 

  30. Weir, A.; Westerhoff, P.; Fabricius, L.; Hristovski, K.; von Goetz, N. Titanium dioxide nanoparticles in food and personal care products. Environ. Sci. Technol. 2012, 46, 2242–2250.

    Google Scholar 

  31. Benn, T. M.; Westerhoff, P. Nanoparticle silver released into water from commercially available sock fabrics. Environ. Sci. Technol. 2008, 42, 4133–4139.

    Google Scholar 

  32. Testino, A.; Bellobono, I. R.; Buscaglia, V.; Canevali, C.; D'Arienzo, M.; Polizzi, S.; Scotti, R.; Morazzoni, F. Optimizing the photocatalytic properties of hydrothermal TiO2 by the control of phase composition and particle morphology. A systematic approach. J. Am. Chem. Soc. 2007, 129, 3564–3575.

    Google Scholar 

  33. Mahshid, S.; Askari, M.; Ghamsari, M. S. Synthesis of TiO2 nanoparticles by hydrolysis and peptization of titanium isopropoxide solution. J. Mater. Process. Technol. 2007, 189, 296–300.

    Google Scholar 

  34. Lee, S.; Cho, I.–S.; Lee, J. H.; Kim, D. H.; Kim, D. W.; Kim, J. Y.; Shin, H.; Lee, J.–K.; Jung, H. S.; Park, N.–G. et al. Two–step sol–gel method–based TiO2 nanoparticles with uniform morphology and size for efficient photo–energy conversion devices. Chem. Mater. 2010, 22, 1958–1965.

    Google Scholar 

  35. Bavykin, D. V.; Friedrich, J. M.; Walsh, F. C. Protonated titanates and TiO2 nanostructured materials: Synthesis, properties, and applications. Adv. Mater. 2006, 18, 2807–2824.

    Google Scholar 

  36. Kaida, T.; Kobayashi, K.; Adachi, M.; Suzuki, F. Optical characteristics of titanium oxide interference film and the film laminated with oxides and their applications for cosmetics. J. Cosmet. Sci. 2004, 55, 219–220.

    Google Scholar 

  37. Matsunaga, T.; Tomoda, R.; Nakajima, T.; Wake, H. Photoelectrochemical sterilization of microbial cells by semiconductor powders. FEMS Microbiol. Lett. 1985, 29, 211–214.

    Google Scholar 

  38. Markowska–Szczupak, A.; Ulfig, K.; Morawski, A. W. The application of titanium dioxide for deactivation of bioparticulates: An overview. Catal. Today 2011, 169, 249–257.

    Google Scholar 

  39. Pelaez, M.; Nolan, N. T.; Pillai, S. C.; Seery, M. K.; Falaras, P.; Kontos, A. G.; Dunlop, P. S. M.; Hamilton, J. W. J.; Byrne, J. A.; O'shea, K. et al. A review on the visible light active titanium dioxide photocatalysts for environmental applications. Appl. Catal. B: Environ. 2012, 125, 331–349.

    Google Scholar 

  40. Wong, M.–S.; Chu, W.–C.; Sun, D.–S.; Huang, H.–S.; Chen, J.–H.; Tsai, P.–J.; Lin, N.–T.; Yu, M.–S.; Hsu, S.–F.; Wang, S.–L. et al. Visible–light–induced bactericidal activity of a nitrogen–doped titanium photocatalyst against human pathogens. Appl. Environ. Microbiol. 2006, 72, 6111–6116.

    Google Scholar 

  41. Tong, T. Z.; Shereef, A.; Wu, J. S.; Binh, C. T. T.; Kelly, J. J.; Gaillard, J.–F.; Gray, K. A. Effects of material morphology on the phototoxicity of nano–TiO2 to bacteria. Environ. Sci. Technol. 2013, 47, 12486–12495.

    Google Scholar 

  42. Foster, H. A.; Ditta, I. B.; Varghese, S.; Steele, A. Photocatalytic disinfection using titanium dioxide: Spectrum and mechanism of antimicrobial activity. Appl. Microbiol. Biotechnol. 2011, 90, 1847–1868.

    Google Scholar 

  43. Maness, P.–C.; Smolinski, S.; Blake, D. M.; Huang, Z.; Wolfrum, E. J.; Jacoby, W. A. Bactericidal activity of photocatalytic TiO2 reaction: Toward an understanding of its killing mechanism. Appl. Environ. Microbiol. 1999, 65, 4094–4098.

    Google Scholar 

  44. Liu, L.–Y.; Sun, L.; Zhong, Z.–T.; Zhu, J.; Song, H.–Y. Effects of titanium dioxide nanoparticles on intestinal commensal bacteria. Nucl. Sci. Techniq. 2016, 27, 5.

    Google Scholar 

  45. Ciner, C. On the long run relationship between gold and silver prices A note. Global Finance J. 2001, 12, 299–303.

    Google Scholar 

  46. Zhu, J. J.; Liao, X. H.; Chen, H.–Y. Electrochemical preparation of silver dendrites in the presence of DNA. Mater. Res. Bull. 2001, 36, 1687–1692.

    Google Scholar 

  47. Salkar, R. A.; Jeevanandam, P.; Aruna, S. T.; Koltypin, Y.; Gedanken, A. The sonochemical preparation of amorphous silver nanoparticles. J. Mater. Chem. 1999, 9, 1333–1335.

    Google Scholar 

  48. Jiang, H. J.; Moon, K.–S.; Zhang, Z. Q.; Pothukuchi, S.; Wong, C. P. Variable frequency microwave synthesis of silver nanoparticles. J. Nanopart. Res. 2006, 8, 117–124.

    Google Scholar 

  49. Alexander, J. W. History of the medical use of silver. Surg. Infect. 2009, 10, 289–292.

    Google Scholar 

  50. Hill, W. R.; Pillsbury, D. M. Argyria: The Pharmacology of Silver; Williams & Wilkins Company: Baltimore, 1939.

    Google Scholar 

  51. Maillard, J.–Y.; Hartemann, P. Silver as an antimicrobial: Facts and gaps in knowledge. Crit. Rev. Microbiol. 2013, 39, 373–383.

    Google Scholar 

  52. Echegoyen, Y.; Nerín, C. Nanoparticle release from nanosilver antimicrobial food containers. Food Chem. Toxicol. 2013, 62, 16–22.

    Google Scholar 

  53. Matsumura, Y.; Yoshikata, K.; Kunisaki, S.–I.; Tsuchido, T. Mode of bactericidal action of silver zeolite and its comparison with that of silver nitrate. Appl. Environ. Microbiol. 2003, 69, 4278–4281.

    Google Scholar 

  54. Morones, J. R.; Elechiguerra, J. L.; Camacho, A.; Holt, K.; Kouri, J. B.; Ramírez, J. T.; Yacaman, M. J. The bactericidal effect of silver nanoparticles. Nanotechnology 2005, 16, 2346–2353.

    Google Scholar 

  55. Chen, X.; Schluesener, H. Nanosilver: A nanoproduct in medical application. Toxicol. Lett. 2008, 176, 1–12.

    Google Scholar 

  56. Tian, X.; Jiang, X. M.; Welch, C.; Croley, T. R.; Wong, T. Y.; Chen, C.; Fan, S. H.; Chong, Y.; Li, R. B.; Ge, C. C. et al. Bactericidal effects of silver nanoparticles on lactobacilli and the underlying mechanism. ACS Appl. Mater. Interfaces 2018, 10, 8443–8450.

    Google Scholar 

  57. Rai, M.; Yadav, A.; Gade, A. Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 2009, 27, 76–83.

    Google Scholar 

  58. Kim, J. S.; Kuk, E.; Yu, K. N.; Kim, J. H.; Park, S. J.; Lee, H. J.; Kim, S. H.; Park, Y. K.; Park, Y. H.; Hwang, C. Y. et al. Antimicrobial effects of silver nanoparticles. Nanomedicine 2007, 3, 95–101.

    Google Scholar 

  59. Espitia, P. J. P.; Soares, N. d. F. F.; dos Reis Coimbra, J. S.; de Andrade, N. J.; Cruz, R. S.; Medeiros, E. A. A. Zinc oxide nanoparticles: Synthesis, antimicrobial activity and food packaging applications. Food Bioprocess Technol. 2012, 5, 1447–1464.

    Google Scholar 

  60. Kołodziejczak–Radzimska, A.; Jesionowski, T. Zinc oxide—From synthesis to application: A review. Materials 2014, 7, 2833–2881.

    Google Scholar 

  61. Moezzi, A.; McDonagh, A. M.; Cortie, M. B. Zinc oxide particles: Synthesis, properties and applications. Chem. Eng. J. 2012, 185–186, 1–22.

    Google Scholar 

  62. Lu, P.–J.; Huang, S.–C.; Chen, Y.–P.; Chiueh, L.–C.; Shih, D. Y.–C. Analysis of titanium dioxide and zinc oxide nanoparticles in cosmetics. J. Food Drug Anal. 2015, 23, 587–594.

    Google Scholar 

  63. Frassinetti, S.; Bronzetti, G.; Caltavuturo, L.; Cini, M.; Della Croce, C. The role of zinc in life: A review. J. Environ. Pathol. Toxicol. Oncol. 2006, 25, 597–610.

    Google Scholar 

  64. Haxthausen, H.; Rasch, C. Some remarks on the bactericidal properties of zinc oxide. Bri. J. Dermatol. 1928, 40, 497–501.

    Google Scholar 

  65. Dwivedi, S.; Wahab, R.; Khan, F.; Mishra, Y. K.; Musarrat, J.; Al–Khedhairy, A. A. Reactive oxygen species mediated bacterial biofilm inhibition via zinc oxide nanoparticles and their statistical determination. PLoS One 2014, 9, e111289.

    Google Scholar 

  66. Liu, Y.; He, L.; Mustapha, A.; Li, H.; Hu, Z. Q.; Lin, M. Antibacterial activities of zinc oxide nanoparticles against Escherichia coli O157:H7. J. Appl. Microbiol. 2009, 107, 1193–1201.

    Google Scholar 

  67. Kasemets, K.; Ivask, A.; Dubourguier, H.–C.; Kahru, A. Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol. in Vitro 2009, 23, 1116–1122.

    Google Scholar 

  68. Yamamoto, O. Influence of particle size on the antibacterial activity of zinc oxide. Int. J. Inorgan. Mater. 2001, 3, 643–646.

    Google Scholar 

  69. Sawai, J.; Igarashi, H.; Hashimoto, A.; Kokugan, T.; Shimizu, M. Effect of particle size and heating temperature of ceramic powders on antibacterial activity of their slurries. J. Chem. Eng. Japan 1996, 29, 251–256.

    Google Scholar 

  70. Colon, G.; Ward, B. C.; Webster, T. J. Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. J. Biomed. Mater. Res. 2006, 78A, 595–604.

    Google Scholar 

  71. Gupta, A. K.; Gupta, M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26, 3995–4021.

    Google Scholar 

  72. Huber, D. L. Synthesis, properties, and applications of iron nanoparticles. Small 2005, 1, 482–501.

    Google Scholar 

  73. Hurrell, R.; Bothwell, T.; Cook, J. D.; Dary, O.; Davidsson, L.; Fairweather–Tait, S.; Hallberg, L.; Lynch, S.; Rosado, J.; Walter, T. et al. The usefulness of elemental iron for cereal flour fortification: A SUSTAIN Task Force report. Nutrit. Rev. 2002, 60, 391–406.

    Google Scholar 

  74. Tennant, D. R. Screening potential intakes of colour additives used in non–alcoholic beverages. Food Chem. Toxicol. 2008, 46, 1985–1993.

    Google Scholar 

  75. Hradil, D.; Grygar, T.; Hradilová, J.; Bezdička, P. Clay and iron oxide pigments in the history of painting. Appl. Clay Sci. 2003, 22, 223–236.

    Google Scholar 

  76. Forestier, S.; Hansenne, I. Cosmetic composition containing a mixture of metal oxide nanopigments and melanine pigments. U.S. Patent 5,695,747, December 9, 1997.

    Google Scholar 

  77. Jung, C. W.; Jacobs, P. Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: Ferumoxides, ferumoxtran, ferumoxsil. Magn. Reson. Imag. 1995, 13, 661–674.

    Google Scholar 

  78. Wang, Y.–X. J. Superparamagnetic iron oxide based MRI contrast agents: Current status of clinical application. Quant. Imaging Med. Surg. 2011, 1, 35–40.

    Google Scholar 

  79. Dixon, S. J.; Stockwell, B. R. The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 2014, 10, 9–17.

    Google Scholar 

  80. Auffan, M.; Achouak, W.; Rose, J.; Roncato, M.–A.; Chanéac, C.; Waite, D. T.; Masion, A.; Woicik, J. C.; Wiesner, M. R.; Bottero, J.–Y. Relation between the redox state of iron–based nanoparticles and their cytotoxicity toward Escherichia coli. Environ. Sci. Technol. 2008, 42, 6730–6735.

    Google Scholar 

  81. Touati, D. Iron and oxidative stress in bacteria. Arch. Biochem. Biophys. 2000, 373, 1–6.

    Google Scholar 

  82. Chatterjee, S.; Bandyopadhyay, A.; Sarkar, K. Effect of iron oxide and gold nanoparticles on bacterial growth leading towards biological application. J. Nanobiotechnol. 2011, 9, 34.

    Google Scholar 

  83. Diao, M. H.; Yao, M. S. Use of zero–valent iron nanoparticles in inactivating microbes. Water Res. 2009, 43, 5243–5251.

    Google Scholar 

  84. Borcherding, J.; Baltrusaitis, J.; Chen, H. H.; Stebounova, L.; Wu, C.–M.; Rubasinghege, G.; Mudunkotuwa, I. A.; Caraballo, J. C.; Zabner, J.; Grassian, V. H. et al. P. Iron oxide nanoparticles induce Pseudomonas aeruginosa growth, induce biofilm formation, and inhibit antimicrobial peptide function. Environ. Sci.: Nano 2014, 1, 123–132.

    Google Scholar 

  85. Ratledge, C.; Dover, L. G. Iron metabolism in pathogenic bacteria. Ann. Rev. Microbiol. 2000, 54, 881–941.

    Google Scholar 

  86. Bullen, J.; Rogers, H. J.; Griffiths, E. Role of iron in bacterial infection. In Current Topics in Microbiology and Immunology; Arber W.; Henle, W.; Hofschneider, P. H.; Humphrey, J. H.; Klein, J.; Koldovský, P.; Koprowski, H.; Maaløe, O.; Melchers, F.; Rott, R. et al., Eds.; Springer: Berlin, Heidelberg, 1978; pp 1–35.

    Google Scholar 

  87. Neilands, J. Iron and its role in microbial physiology. In Microbial Iron Metabolism; Neilands, J. B. Ed.; Elsevier: Amsterdam, 1974; pp 3–34.

    Google Scholar 

  88. Lee, C.; Kim, J. Y.; Lee, W. I.; Nelson, K. L.; Yoon, J.; Sedlak, D. L. Bactericidal effect of zero–valent iron nanoparticles on Escherichia coli. Environ. Sci. Technol. 2008, 42, 4927–4933.

    Google Scholar 

  89. Slowing, I. I.; Vivero–Escoto, J. L.; Wu, C.–W.; Lin, V. S.–Y. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv. Drug Delivery Rev. 2008, 60, 1278–1288.

    Google Scholar 

  90. Peters, R.; Kramer, E.; Oomen, A. G.; Herrera Rivera, Z. E.; Oegema, G.; Tromp, P. C.; Fokkink, R.; Rietveld, A.; Marvin, H. J.; Weigel, S. et al. Presence of nano–sized silica during in vitro digestion of foods containing silica as a food additive. ACS Nano 2012, 6, 2441–2451.

    Google Scholar 

  91. Fruijtier–Pölloth, C. The safety of nanostructured synthetic amorphous silica (SAS) as a food additive (E 551). Arch. Toxicol. 2016, 90, 2885–2916.

    Google Scholar 

  92. Ito, M.; Yamamoto, S.; Okada, A.; Ishiwata, Y. Silica gel for stabilization treatment of beer, a method of manufacturing the silica gel and a method of the stabilization treatment of beer. U.S. Patent 6,565,905, May 20, 2003.

    Google Scholar 

  93. Mierczynska–Vasilev, A.; Smith, P. Current state of knowledge and challenges in wine clarification. Austr. J. Grape Wine Res. 2015, 21, 615–626.

    Google Scholar 

  94. Villota, R.; Hawkes, J. G.; Cochrane, H. Food applications and the toxicological and nutritional implications of amorphous silicon dioxide. Crit. Rev. Food Sci. Nutr. 1986, 23, 289–321.

    Google Scholar 

  95. Rowe, R. C.; Sheskey, P. J.; Owen, S. C. Handbook of Pharmaceutical Excipients; Pharmaceutical Press: London, 2006.

    Google Scholar 

  96. Hansenne, I.; Rick, D. W. High SPF nontacky/nongreasy UV–photoprotecting compositions comprising particulates of MMA crosspolymers. U.S. Patent 6,432,389, August 13, 2002.

    Google Scholar 

  97. Dekkers, S.; Krystek, P.; Peters, R. J.; Lankveld, D. P.; Bokkers, B. G.; van Hoeven–Arentzen, P. H.; Bouwmeester, H.; Oomen, A. G. Presence and risks of nanosilica in food products. Nanotoxicology 2011, 5, 393–405.

    Google Scholar 

  98. Hetrick, E. M.; Shin, J. H.; Paul, H. S.; Schoenfisch, M. H. Anti–biofilm efficacy of nitric oxide–releasing silica nanoparticles. Biomaterials 2009, 30, 2782–2789.

    Google Scholar 

  99. Trewyn, B. G.; Whitman, C. M.; Lin, V. S.–Y. Morphological control of room–temperature ionic liquid templated mesoporous silica nanoparticles for controlled release of antibacterial agents. Nano Lett. 2004, 4, 2139–2143.

    Google Scholar 

  100. Li, L. L.; Wang, H. Enzyme–coated mesoporous silica nanoparticles as efficient antibacterial agents in vivo. Adv. Healthcare Mater. 2013, 2, 1351–1360.

    Google Scholar 

  101. Appendini, P.; Hotchkiss, J. H. Review of antimicrobial food packaging. Innov. Food Sci. Emerg. Technol. 2002, 3, 113–126.

    Google Scholar 

  102. Zhang, W.; Li, Y.; Niu, J. F.; Chen, Y. S. Photogeneration of reactive oxygen species on uncoated silver, gold, nickel, and silicon nanoparticles and their antibacterial effects. Langmuir 2013, 29, 4647–4651.

    Google Scholar 

  103. Jiang, W.; Mashayekhi, H.; Xing, B. S. Bacterial toxicity comparison between nano–and micro–scaled oxide particles. Environ. Pollut. 2009, 157, 1619–1625.

    Google Scholar 

  104. Chen, H. Q.; Zhao, R. F.; Wang, B.; Cai, C. X.; Zheng, L. N.; Wang, H. L.; Wang, M.; Ouyang, H.; Zhou, X. Y.; Chai, Z. F. et al. The effects of orally administered Ag, TiO2 and SiO2 nanoparticles on gut microbiota composition and colitis induction in mice. NanoImpact 2017, 8, 80–88.

    Google Scholar 

  105. Ley, R. E.; Turnbaugh, P. J.; Klein, S.; Gordon, J. I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022–1023.

    Google Scholar 

  106. Dudefoi, W.; Moniz, K.; Allen–Vercoe, E.; Ropers, M.–H.; Walker, V. K. Impact of food grade and nano–TiO2 particles on a human intestinal community. Food Chem. Toxicol. 2017, 106, 242–249.

    Google Scholar 

  107. Das, P.; McDonald, J. A.; Petrof, E. O.; Allen–Vercoe, E.; Walker, V. K. Nanosilver–mediated change in human intestinal microbiota. J. Nanomed. Nanotechnol. 2014, 5, 235.

    Google Scholar 

  108. Marcus, I. M.; Wilder, H. A.; Quazi, S. J.; Walker, S. L. Linking microbial community structure to function in representative simulated systems. Appl. Environ. Microbiol. 2013, 79, 2552–2559.

    Google Scholar 

  109. Shin, N.–R.; Whon, T. W.; Bae, J.–W. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015, 33, 496–503.

    Google Scholar 

  110. Waller, T.; Chen, C.; Walker, S. L. Food and industrial grade titanium dioxide impacts gut microbiota. Environ. Eng. Sci. 2017, 34, 537–550.

    Google Scholar 

  111. Taylor, A. A.; Marcus, I. M.; Guysi, R. L.; Walker, S. L. Metal oxide nanoparticles induce minimal phenotypic changes in a model colon gut microbiota. Environ. Eng. Sci. 2015, 32, 602–612.

    Google Scholar 

  112. Khan, S. T.; Ahamed, M.; Al–Khedhairy, A.; Musarrat, J. Biocidal effect of copper and zinc oxide nanoparticles on human oral microbiome and biofilm formation. Mater. Lett. 2013, 97, 67–70.

    Google Scholar 

  113. Matin, A.; Auger, E. A.; Blum, P. H.; Schultz, J. E. Genetic basis of starvation survival in nondifferentiating bacteria. Ann. Rev. Microbiol. 1989, 43, 293–314.

    Google Scholar 

  114. Cotter, P. D.; Hill, C. Surviving the acid test: Responses of gram–positive bacteria to low pH. Microbiol. Mol. Biol. Rev. 2003, 67, 429–453.

    Google Scholar 

  115. Jones, K.; Morton, J.; Smith, I.; Jurkschat, K.; Harding, A.–H.; Evans, G. Human in vivo and in vitro studies on gastrointestinal absorption of titanium dioxide nanoparticles. Toxicol. Lett. 2015, 233, 95–101.

    Google Scholar 

  116. Verma, A.; Stellacci, F. Effect of surface properties on nanoparticle–cell interactions. Small 2010, 6, 12–21.

    Google Scholar 

  117. Vandenberg, L. N.; Hauser, R.; Marcus, M.; Olea, N.; Welshons, W. V. Human exposure to bisphenol A (BPA). Reproduct. Toxicol. 2007, 24, 139–177.

    Google Scholar 

  118. Chen, L. G.; Guo, Y. Y.; Hu, C. Y.; Lam, P. K. S.; Lam, J. C. W.; Zhou, B. S. Dysbiosis of gut microbiota by chronic coexposure to titanium dioxide nanoparticles and bisphenol A: Implications for host health in zebrafish. Environ. Pollut. 2018, 234, 307–317.

    Google Scholar 

  119. Ma, Y. B.; Song, L. B.; Lei, Y.; Jia, P. P.; Lu, C. J.; Wu, J. F.; Xi, C. W.; Strauss, P.; Pei, D. S. Sex dependent effects of silver nanoparticles on the zebrafish gut microbiota. Environ. Sci.: Nano 2018, 5, 740–751.

    Google Scholar 

  120. Williams, K.; Milner, J.; Boudreau, M. D.; Gokulan, K.; Cerniglia, C. E.; Khare, S. Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gutassociated immune responses in the ileum of Sprague–Dawley rats. Nanotoxicology 2015, 9, 279–289.

    Google Scholar 

  121. Markle, J. G. M.; Frank, D. N.; Mortin–Toth, S.; Robertson, C. E.; Feazel, L. M.; Rolle–Kampczyk, U.; von Bergen, M.; McCoy, K. D.; Macpherson, A. J.; Danska, J. S. Sex differences in the gut microbiome drive hormone–dependent regulation of autoimmunity. Science 2013, 339, 1084–1088.

    Google Scholar 

  122. Org, E.; Mehrabian, M.; Parks, B. W.; Shipkova, P.; Liu, X. Q.; Drake, T. A.; Lusis, A. J. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes 2016, 7, 313–322.

    Google Scholar 

  123. Pal, S.; Tak, Y. K.; Song, J. M. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram–negative bacterium Escherichia coli. Appl. Environ. Microbiol. 2007, 73, 1712–1720.

    Google Scholar 

  124. Kvitek, L.; Panáček, A.; Soukupová, J.; Kolář, M.; Večeřová, R.; Prucek, R.; Holecová, M.; Zbořil, R. Effect of surfactants and polymers on stability and antibacterial activity of silver nanoparticles (NPs). J. Phys. Chem. C 2008, 112, 5825–5834.

    Google Scholar 

  125. Thiel, J.; Pakstis, L.; Buzby, S.; Raffi, M.; Ni, C.; Pochan, D. E. J.; Shah, S. I. Antibacterial properties of silver–doped titania. Small 2007, 3, 799–803.

    Google Scholar 

  126. van den Brûle, S.; Ambroise, J.; Lecloux, H.; Levard, C.; Soulas, R.; De Temmerman, P.–J.; Palmai–Pallag, M.; Marbaix, E.; Lison, D. Dietary silver nanoparticles can disturb the gut microbiota in mice. Particl. Fibre Toxicol. 2015, 13, 38.

    Google Scholar 

  127. Wilding, L. A.; Bassis, C. M.; Walacavage, K.; Hashway, S.; Leroueil, P. R.; Morishita, M.; Maynard, A. D.; Philbert, M. A.; Bergin, I. L. Repeated dose (28–day) administration of silver nanoparticles of varied size and coating does not significantly alter the indigenous murine gut microbiome. Nanotoxicology 2016, 10, 513–520.

    Google Scholar 

  128. Hadrup, N.; Loeschner, K.; Bergström, A.; Wilcks, A.; Gao, X. Y.; Vogel, U.; Frandsen, H. L.; Larsen, E. H.; Lam, H. R.; Mortensen, A. Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch. Toxicol. 2012, 86, 543–551.

    Google Scholar 

  129. Zazo, H.; Colino, C. I.; Lanao, J. M. Current applications of nanoparticles in infectious diseases. J. Control. Release 2016, 224, 86–102.

    Google Scholar 

  130. Acosta, E. Bioavailability of nanoparticles in nutrient and nutraceutical delivery. Curr. Opin. Colloid Interface Sci. 2009, 14, 3–15.

    Google Scholar 

  131. Zhao, C.–Y.; Tan, S.–X.; Xiao, X.–Y.; Qiu, X.–S.; Pan, J.–Q.; Tang, Z.–X. Effects of dietary zinc oxide nanoparticles on growth performance and antioxidative status in broilers. Biolog. Trace Elem. Res. 2014, 160, 361–367.

    Google Scholar 

  132. Black, M. M.; Baqui, A. H.; Zaman, K.; Persson, L. A.; El Arifeen, S.; Le, K.; McNary, S. W.; Parveen, M.; Hamadani, J. D.; Black, R. E. Iron and zinc supplementation promote motor development and exploratory behavior among Bangladeshi infants. Am. J. Clin. Nutr. 2004, 80, 903–910.

    Google Scholar 

  133. Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007, 2, 751–760.

    Google Scholar 

  134. Dostal, A.; Chassard, C.; Hilty, F. M.; Zimmermann, M. B.; Jaeggi, T.; Rossi, S.; Lacroix, C. Iron depletion and repletion with ferrous sulfate or electrolytic iron modifies the composition and metabolic activity of the gut microbiota in rats. J. Nutr. 2012, 142, 271–277.

    Google Scholar 

  135. Werner, T.; Wagner, S. J.; Martínez, I.; Walter, J.; Chang, J.–S.; Clavel, T.; Kisling, S.; Schuemann, K.; Haller, D. Depletion of luminal iron alters the gut microbiota and prevents Crohn’s disease–like ileitis. Gut 2011, 60, 325–333.

    Google Scholar 

  136. Jaeggi, T.; Kortman, G. A.; Moretti, D.; Chassard, C.; Holding, P.; Dostal, A.; Boekhorst, J.; Timmerman, H. M.; Swinkels, D. W.; Tjalsma, H. et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 2015, 64, 731–742.

    Google Scholar 

  137. Kortman, G. A. M.; Boleij, A.; Swinkels, D. W.; Tjalsma, H. Iron availability increases the pathogenic potential of Salmonella typhimurium and other enteric pathogens at the intestinal epithelial interface. PLoS One 2012, 7, e29968.

    Google Scholar 

  138. Zimmermann. The potential of encapsulated iron compounds in food fortification: A review. Int. J. Vitam. Nutr. Res. 2004, 74, 453–461.

  139. Pereira, D. I. A.; Bruggraber, S. F. A.; Faria, N.; Poots, L. K.; Tagmount, M. A.; Aslam, M. F.; Frazer, D. M.; Vulpe, C. D.; Anderson, G. J.; Powell, J. J. Nanoparticulate iron(III) oxo–hydroxide delivers safe iron that is well absorbed and utilised in humans. Nanomed.: Nanotechnol. Biol. Med. 2014, 10, 1877–1886.

    Google Scholar 

  140. Pereira, D. I. A.; Aslam, M. F.; Frazer, D. M.; Schmidt, A.; Walton, G. E.; McCartney, A. L.; Gibson, G. R.; Anderson, G. J.; Powell, J. J. Dietary iron depletion at weaning imprints low microbiome diversity and this is not recovered with oral nano Fe(III). MicrobiologyOpen 2015, 4, 12–27.

    Google Scholar 

  141. Poulsen, H. D. Zinc oxide for weanling piglets. Acta Agricult. Scandin. A–Anim. Sci. 1995, 45, 159–167.

    Google Scholar 

  142. Cho, J. H.; Upadhaya, S. D.; Kim, I. H. Effects of dietary supplementation of modified zinc oxide on growth performance, nutrient digestibility, blood profiles, fecal microbial shedding and fecal score in weanling pigs. Anim. Sci. J. 2015, 86, 617–623.

    Google Scholar 

  143. Xia, T.; Lai, W. Q.; Han, M. M.; Han, M.; Ma, X.; Zhang, L. Y. Dietary ZnO nanoparticles alters intestinal microbiota and inflammation response in weaned piglets. Oncotarget 2017, 8, 64878–64891.

    Google Scholar 

  144. Huang, H. C.; Barua, S.; Sharma, G.; Dey, S. K.; Rege, K. Inorganic nanoparticles for cancer imaging and therapy. J. Control. Release 2011, 155, 344–357.

    Google Scholar 

  145. Na, H. B.; Song, I. C.; Hyeon, T. Inorganic nanoparticles for MRI contrast agents. Adv. Mater. 2009, 21, 2133–2148.

    Google Scholar 

  146. Anselmo, A. C.; Mitragotri, S. Nanoparticles in the clinic. Bioeng. Transl. Med. 2016, 1, 10–29.

    Google Scholar 

  147. Anselmo, A. C.; Mitragotri, S. A review of clinical translation of inorganic nanoparticles. AAPS J. 2015, 17, 1041–1054.

    Google Scholar 

  148. Mitragotri, S.; Anderson, D. G.; Chen, X. Y.; Chow, E. K.; Ho, D.; Kabanov, A. V.; Karp, J. M.; Kataoka, K.; Mirkin, C. A.; Petrosko, S. H. et al. Accelerating the translation of nanomaterials in biomedicine. ACS Nano 2015, 9, 6644–6654.

    Google Scholar 

  149. Kohanski, M. A.; Dwyer, D. J.; Collins, J. J. How antibiotics kill bacteria: From targets to networks. Nat. Rev. Microbiol. 2010, 8, 423–435.

    Google Scholar 

  150. Sommer, M. O.; Dantas, G. Antibiotics and the resistant microbiome. Curr. Opin. Microbiol. 2011, 14, 556–563.

    Google Scholar 

  151. Kelly, C. P.; LaMont, J. T. Clostridium difficile—More difficult than ever. N Engl. J. Med. 2008, 359, 1932–1940.

    Google Scholar 

  152. Vargason, A. M.; Anselmo, A. C. Clinical translation of microbe–based therapies: Current clinical landscape and preclinical outlook. Bioeng. Transl. Med., in press, DOI: 10.1002/btm2.10093.

  153. Khanna, S.; Pardi, D. S.; Kelly, C. R.; Kraft, C. S.; Dhere, T.; Henn, M. R.; Lombardo, M. J.; Vulic, M.; Ohsumi, T.; Winkler, J. et al. A Novel microbiome therapeutic increases gut microbial diversity and prevents recurrent Clostridium difficile infection. J. Infect. Dis. 2016, 214, 173–181.

    Google Scholar 

  154. Kim, D.; Kwon, S. J.; Wu, X.; Sauve, J.; Lee, I.; Nam, J.; Kim, J.; Dordick, J. S. Selective killing of pathogenic bacteria by antimicrobial silver nanoparticle—Cell wall binding domain conjugates. ACS Appl. Mater. Interfaces 2018, 10, 13317–13324.

    Google Scholar 

  155. Borovička, J.; Metheringham, W. J.; Madden, L. A.; Walton, C. D.; Stoyanov, S. D.; Paunov, V. N. Photothermal colloid antibodies for shape–selective recognition and killing of microorganisms. J. Am. Chem. Soc. 2013, 135, 5282–5285.

    Google Scholar 

  156. Shahverdi, A. R.; Fakhimi, A.; Shahverdi, H. R.; Minaian, S. Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomed.: Nanotechnol. Biol. Med. 2007, 3, 168–171.

    Google Scholar 

  157. Qiu, Z. G.; Yu, Y. M.; Chen, Z. L.; Jin, M.; Yang, D.; Zhao, Z. G.; Wang, J. F.; Shen, Z. Q.; Wang, X. W.; Qian, D. et al. Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proc. Natl. Acad. Sci. USA 2012, 109, 4944–4949.

    Google Scholar 

  158. Wang, X. L.; Yang, F. X.; Zhao, J.; Xu, Y.; Mao, D. Q.; Zhu, X.; Luo, Y.; Alvarez, P. J. J. Bacterial exposure to ZnO nanoparticles facilitates horizontal transfer of antibiotic resistance genes. NanoImpact 2018, 10, 61–67.

    Google Scholar 

Download references

Author information

Author notes

  1. Kunyu Qiu and Phillip G. Durham contributed equally to this work.

Authors and Affiliations

  1. Division of Pharmacoengineering and Molecular Pharmaceutics, Eshelman School of Pharmacy, University of North Carolina at Chapel Hill, Chapel Hill, NC, 27599, USA

    Kunyu Qiu, Phillip G. Durham & Aaron C. Anselmo

Authors
  1. Kunyu Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phillip G. Durham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aaron C. Anselmo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aaron C. Anselmo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiu, K., Durham, P.G. & Anselmo, A.C. Inorganic nanoparticles and the microbiome. Nano Res. 11, 4936–4954 (2018). https://doi.org/10.1007/s12274-018-2137-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-018-2137-2

Keywords

Search

Navigation