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Review Article

Inorganic nanoparticles and the microbiome

Kunyu Qiu§Phillip G. Durham§Aaron C. Anselmo( )
Division of Pharmacoengineering and Molecular PharmaceuticsEshelman School of PharmacyUniversity of North Carolina at Chapel HillChapel HillNC27599USA

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

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Graphical Abstract

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 microbiota- modulating 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.

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.

3

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

4

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

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.

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.

7

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

8

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

9

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

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.

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.

12

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

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.

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.

15

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

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.

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.

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.

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.

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.

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.

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.

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.

24

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

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.

26

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

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.

28

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

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.

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.

31

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

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.

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.

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.

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.

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.

37

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

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.

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.

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.

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.

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.

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.

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.

45

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

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.

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.

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.

49

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

50

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

51

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

52

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

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.

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.

55

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

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.

57

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

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.

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.

60

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

61

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

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.

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.

64

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

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.

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.

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.

68

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

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.

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.

71

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

72

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

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.

74

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

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.

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.
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.

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.

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.

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.

81

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

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.

83

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

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.

85

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

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.; Koldovsky, P.; Koprowski, H.; Maaløe, O.; Melchers, F.; Rott, R. et al., Eds.; Springer: Berlin, Heidelberg, 1978; pp 1–35.
87
Neilands, J. Iron and its role in microbial physiology. In Microbial Iron Metabolism; Neilands, J. B. Ed.; Elsevier: Amsterdam, 1974; pp 3–34.https://doi.org/10.1016/B978-0-12-515250-1.50006-0
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.

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.

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.

91

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

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.
93

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

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.

95

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

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.
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.

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.

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.

100

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

101

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

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.

103

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

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.

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.

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.

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.

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.

109

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

110

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

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.

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.

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.

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.

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.

116

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

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

129

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

130

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

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.

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.

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.

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.

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.

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.

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.

138

Zimmermann. The potential of encapsulated iron compoundsin 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.

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.

141

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

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.

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.

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.

145

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

146

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

147

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

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.

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.

150

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

151

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

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.https://doi.org/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.

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.

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.

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.

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.

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.

Nano Research
Pages 4936-4954
Cite this article:
Qiu K, Durham PG, Anselmo AC. Inorganic nanoparticles and the microbiome. Nano Research, 2018, 11(10): 4936-4954. https://doi.org/10.1007/s12274-018-2137-2
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Received: 07 April 2018
Revised: 17 June 2018
Accepted: 22 June 2018
Published: 13 July 2018
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018
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