Dietary silver nanoparticles can disturb the gut microbiota in mice

Particle and Fibre Toxicology

Volumn 13, Issue 1, 2016, Pages

  van den Brule, Sybille ^a   Ambroise, Jérôme ^a   Lecloux, Hélène ^a   Levard, Clément ^b   Soulas, Romain ^c   De Temmerman, Pieter Jan ^d   Palmai Pallag, Mihaly ^a   Marbaix, Etienne ^e   Lison, Dominique ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b AIX MARSEILLE UNIVERSITY   (France)

^c CEA GRENOBLE   (France)

^d VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

^e DE DUVE INSTITUTE   (Belgium)

Author keywords

Bacteria; Dysbiosis; Food; Nanomaterials; NGS; Sulfidation; Toxicity

Indexed keywords

SILVER NANOPARTICLE; METAL NANOPARTICLE; SILVER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; BODY WEIGHT; CONTROLLED STUDY; DIETARY INTAKE; DIGESTIVE TRACT PARAMETERS; ENERGY DISPERSIVE X RAY SPECTROSCOPY; FECES ANALYSIS; FEMALE; FIRMICUTES; GUT INTEGRITY; INFLAMMATION; INTESTINE FLORA; LACHNOSPIRACEAE; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; POPULATION ABUNDANCE; POPULATION DENSITY; PRIORITY JOURNAL; SCANNING TRANSMISSION ELECTRON MICROSCOPY; TOXICITY TESTING; ANIMAL; CHEMISTRY; DOSE RESPONSE; INTESTINE; MICROBIOLOGY; MICROFLORA; SPECTROMETRY;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; INTESTINES; METAL NANOPARTICLES; MICE; MICROBIOTA; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; SILVER; SPECTROMETRY, X-RAY EMISSION;

EID: 84991746987     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-016-0149-1     Document Type: Article

References (126)

1. Chaudhry Q, Scotter M, Blackburn J, Ross B, Boxall A, Castle L, et al. Applications and implications of nanotechnologies for the food sector. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2008;25:241-58
2. Srinivas PR, Philbert M, Vu TQ, Huang Q, Kokini JL, Saltos E, et al. Nanotechnology research: applications in nutritional sciences. J Nutr. 2010;140:119-24
3. Hwang M, Lee EJ, Kweon SY, Park MS, Jeong JY, Um JH, et al. Risk assessment principle for engineered nanotechnology in food and drug. Toxicol Res. 2012;28:73-9
4. Consumer Products Inventory, http://www.nanotechproject.org/cpi/. Accessed 29 Jun 2016
5. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, et al. Nano-silver-a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology. 2009;3:109-38
6. Bohmert L, Niemann B, Lichtenstein D, Juling S, Lampen A. Molecular mechanism of silver nanoparticles in human intestinal cells. Nanotoxicology. 2015;9:852-60
7. van der Zande M, Vandebriel RJ, Van DE, Kramer E, Herrera RZ, Serrano-Rojero CS, et al. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano. 2012;6:7427-42
8. Lee JH, Kim YS, Song KS, Ryu HR, Sung JH, Park JD, et al. Biopersistence of silver nanoparticles in tissues from Sprague-Dawley rats. Part Fibre Toxicol. 2013;10:36
9. Ebabe ER, Gaillet S, Vide J, Romain C, Lauret C, Rugani N, et al. Dietary exposure to silver nanoparticles in Sprague-Dawley rats: effects on oxidative stress and inflammation. Food Chem Toxicol. 2013;60:297-301
10. Fondevila M, Herrer R, Casallas MC, Abecia L, Ducha JJ. Silver nanoparticles as a potential antimicrobial additive for weaned pigs. Anim Feed Sci Technol. 2009;150:259-69
11. Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, et al. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol. 2010;7:20
12. Shahare B, Yashpal M. Toxic effects of repeated oral exposure of silver nanoparticles on small intestine mucosa of mice. Toxicol Mech Methods. 2013;23:161-7
13. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, et al. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal Toxicol. 2008;20:575-83
14. Park K. Toxicokinetic differences and toxicities of silver nanoparticles and silver ions in rats after single oral administration. J Toxicol Environ Health A. 2013;76:1246-60
15. Bergin IL, Wilding LA, Morishita M, Walacavage K, Ault AP, Axson JL, et al. Effects of particle size and coating on toxicologic parameters, fecal elimination kinetics and tissue distribution of acutely ingested silver nanoparticles in a mouse model. Nanotoxicology. 2016;10:352-60
16. Park EJ, Bae E, Yi J, Kim Y, Choi K, Lee SH, et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol. 2010;30:162-8
17. Volker C, Oetken M, Oehlmann J. The biological effects and possible modes of action of nanosilver. Rev Environ Contam Toxicol. 2013;223:81-106
18. Aitken JD, Gewirtz AT. Gut microbiota in 2012: toward understanding and manipulating the gut microbiota. Nat Rev Gastroenterol Hepatol. 2013;10:72-4
19. Larsson E, Tremaroli V, Lee YS, Koren O, Nookaew I, Fricker A, et al. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut. 2012;61:1124-31
20. Maurice CF, Haiser HJ, Turnbaugh PJ. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell. 2013;152:39-50
21. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3:289-306
22. Kostic AD, Howitt MR, Garrett WS. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 2013;27:701-18
23. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222-7
24. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159:514-29
25. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541-6
26. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514:181-6
27. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature. 2015;519:92-6
28. Delzenne NM, Cani PD. Interaction between obesity and the gut microbiota: relevance in nutrition. Annu Rev Nutr. 2011;31:15-31
29. Huang YJ, Boushey HA. The microbiome in asthma. J Allergy Clin Immunol. 2015;135:25-30
30. Hadrup N, Loeschner K, Bergstrom A, Wilcks A, Gao X, Vogel U, et al. Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch Toxicol. 2012;86:543-51
31. Han X, Geller B, Moniz K, Das P, Chippindale AK, Walker VK. Monitoring the developmental impact of copper and silver nanoparticle exposure in Drosophila and their microbiomes. Sci Total Environ. 2014;487:822-9
32. Williams K, Milner J, Boudreau MD, Gokulan K, Cerniglia CE, Khare S. Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut-associated immune responses in the ileum of Sprague-Dawley rats. Nanotoxicology. 2015;9:279-89
33. Das P, McDonald JAK, Petrof EO, Allen-Vercoe E, Walker VK. Nanosilvermediated change in human intestinal microbiota. Journal of Nanomedicine & Nanotechnology. 2014;5:235
34. Wilding LA, Bassis CM, Walacavage K, Hashway S, Leroueil PR, Morishita M, et al. Repeated dose (28-day) administration of silver nanoparticles of varied size and coating does not significantly alter the indigenous murine gut microbiome. Nanotoxicology. 2016;10:513-20
35. Lozupone CA, Knight R. Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev. 2008;32:557-78
36. Kim A. Dysbiosis: a review highlighting obesity and inflammatory bowel disease. J Clin Gastroenterol. 2015;49 Suppl 1:S20-4
37. Lozupone C, Hamady M, Knight R. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics. 2006;7:371
38. Hur KY, Lee MS. Gut microbiota and metabolic disorders. Diabetes Metab J. 2015;39:198-203
39. Schippa S, Conte MP. Dysbiotic events in gut microbiota: impact on human health. Nutrients. 2014;6:5786-805
40. Jung WK, Koo HC, Kim KW, Shin S, Kim SH, Park YH. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl Environ Microbiol. 2008;74:2171-8
41. Pietroiusti A, Magrini A, Campagnolo L. New frontiers in nanotoxicology: gut microbiota/microbiome-mediated effects of engineered nanomaterials. Toxicol Appl Pharmacol. 2016;299:90-5
42. Frohlich EE, Frohlich E. Cytotoxicity of Nanoparticles Contained in Food on Intestinal Cells and the Gut Microbiota. Int J Mol Sci. 2016;17:509
43. Vandenberg LN, Welshons WV, Vom Saal FS, Toutain PL, Myers JP. Should oral gavage be abandoned in toxicity testing of endocrine disruptors? Environ Health. 2014;13:46
44. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, et al. Conducting a microbiome study. Cell. 2014;158:250-62
45. Salipante SJ, Kawashima T, Rosenthal C, Hoogestraat DR, Cummings LA, Sengupta DJ, et al. Performance comparison of Illumina and ion torrent next-generation sequencing platforms for 16S rRNA-based bacterial community profiling. Appl Environ Microbiol. 2014;80:7583-91
46. Jeraldo P, Chia N, Goldenfeld N. On the suitability of short reads of 16S rRNA for phylogeny-based analyses in environmental surveys. Environ Microbiol. 2011;13:3000-9
47. McCafferty J, Muhlbauer M, Gharaibeh RZ, Arthur JC, Perez-Chanona E, Sha W, et al. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J. 2013;7:2116-25
48. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009;77:2367-75
49. Bassis CM, Theriot CM, Young VB. Alteration of the murine gastrointestinal microbiota by tigecycline leads to increased susceptibility to Clostridium difficile infection. Antimicrob Agents Chemother. 2014;58:2767-74
50. Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y, Inoue H, et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol. 2015;15:100
51. Musso G, Gambino R, Cassader M. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes Care. 2010;33:2277-84
52. Mathur R, Barlow GM. Obesity and the microbiome. Expert Rev Gastroenterol Hepatol. 2015;9:1087-99
53. Lopez-Cepero AA, Palacios C. Association of the intestinal microbiota and obesity. P R Health Sci J. 2015;34:60-4
54. Sands SA, Tsau S, Yankee TM, Parker BL, Ericsson AC, LeVine SM. The effect of omeprazole on the development of experimental autoimmune encephalomyelitis in C57BL/6 J and SJL/J mice. BMC Res Notes. 2014;7:605
55. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One. 2014;9:e92193
56. Serino M, Luche E, Gres S, Baylac A, Berge M, Cenac C, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61:543-53
57. Rooks MG, Veiga P, Wardwell-Scott LH, Tickle T, Segata N, Michaud M, et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 2014;8:1403-17
58. Krych L, Nielsen DS, Hansen AK, Hansen CH. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and IFN-gamma level in NOD mice. Gut Microbes. 2015;6:101-9
59. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470-81
60. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011;60:2775-86
61. Levard C, Hotze EM, Colman BP, Dale AL, Truong L, Yang XY, et al. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ Sci Technol. 2013;47:13440-8
62. Levard C, Reinsch BC, Michel FM, Oumahi C, Lowry GV, Brown GE. Sulfidation processes of PVP-coated silver nanoparticles in aqueous solution: impact on dissolution rate. Environ Sci Technol. 2011;45:5260-6
63. Reinsch BC, Levard C, Li Z, Ma R, Wise A, Gregory KB, et al. Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ Sci Technol. 2012;46:6992-7000
64. Doolette CL, McLaughlin MJ, Kirby JK, Batstone DJ, Harris HH, Ge H, et al. Transformation of PVP coated silver nanoparticles in a simulated wastewater treatment process and the effect on microbial communities. Chem Cent J. 2013;7:46
65. Rick VA, Tappero R, Arai Y. Residence time effects on phase transformation of nanosilver in reduced soils. Environ Sci Pollut Res Int. 2014;21:7828-37
66. Chen S, Theodorou IG, Goode AE, Gow A, Schwander S, Zhang JJ, et al. High-resolution analytical electron microscopy reveals cell culture mediainduced changes to the chemistry of silver nanowires. Environ Sci Technol. 2013;47:13813-21
67. Ma BW, Bokulich NA, Castillo PA, Kananurak A, Underwood MA, Mills DA, et al. Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PLoS One. 2012;7:e47416
68. Burkowska-But A, Sionkowski G, Walczak M. Influence of stabilizers on the antimicrobial properties of silver nanoparticles introduced into natural water. J Environ Sci (China). 2014;26:542-9
69. Silva T, Pokhrel LR, Dubey B, Tolaymat TM, Maier KJ, Liu X. Particle size, surface charge and concentration dependent ecotoxicity of three organocoated silver nanoparticles: comparison between general linear modelpredicted and observed toxicity. Sci Total Environ. 2014;468-469:968-76
70. Kostic AD, Howitt MR, Garrett WS. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 2013;27:701-18
71. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222-7
72. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. 2014;159:514-29
73. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541-6
74. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514:181-6
75. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature. 2015;519:92-6
76. Delzenne NM, Cani PD. Interaction between obesity and the gut microbiota: relevance in nutrition. Annu Rev Nutr. 2011;31:15-31
77. Huang YJ, Boushey HA. The microbiome in asthma. J Allergy Clin Immunol. 2015;135:25-30
78. Hadrup N, Loeschner K, Bergstrom A, Wilcks A, Gao X, Vogel U, et al. Subacute oral toxicity investigation of nanoparticulate and ionic silver in rats. Arch Toxicol. 2012;86:543-51
79. Han X, Geller B, Moniz K, Das P, Chippindale AK, Walker VK. Monitoring the developmental impact of copper and silver nanoparticle exposure in Drosophila and their microbiomes. Sci Total Environ. 2014;487:822-9
80. Williams K, Milner J, Boudreau MD, Gokulan K, Cerniglia CE, Khare S. Effects of subchronic exposure of silver nanoparticles on intestinal microbiota and gut-associated immune responses in the ileum of Sprague-Dawley rats. Nanotoxicology. 2015;9:279-89
81. Das P, McDonald JAK, Petrof EO, Allen-Vercoe E, Walker VK. Nanosilvermediated change in human intestinal microbiota. Journal of Nanomedicine & Nanotechnology. 2014;5:235
82. Wilding LA, Bassis CM, Walacavage K, Hashway S, Leroueil PR, Morishita M, et al. Repeated dose (28-day) administration of silver nanoparticles of varied size and coating does not significantly alter the indigenous murine gut microbiome. Nanotoxicology. 2016;10:513-20
83. Lozupone CA, Knight R. Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev. 2008;32:557-78
84. Kim A. Dysbiosis: a review highlighting obesity and inflammatory bowel disease. J Clin Gastroenterol. 2015;49 Suppl 1:S20-4
85. Lozupone C, Hamady M, Knight R. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics. 2006;7:371
86. Hur KY, Lee MS. Gut microbiota and metabolic disorders. Diabetes Metab J. 2015;39:198-203
87. Schippa S, Conte MP. Dysbiotic events in gut microbiota: impact on human health. Nutrients. 2014;6:5786-805
88. Jung WK, Koo HC, Kim KW, Shin S, Kim SH, Park YH. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl Environ Microbiol. 2008;74:2171-8
89. Pietroiusti A, Magrini A, Campagnolo L. New frontiers in nanotoxicology: gut microbiota/microbiome-mediated effects of engineered nanomaterials. Toxicol Appl Pharmacol. 2016;299:90-5
90. Frohlich EE, Frohlich E. Cytotoxicity of Nanoparticles Contained in Food on Intestinal Cells and the Gut Microbiota. Int J Mol Sci. 2016;17:509
91. Vandenberg LN, Welshons WV, Vom Saal FS, Toutain PL, Myers JP. Should oral gavage be abandoned in toxicity testing of endocrine disruptors? Environ Health. 2014;13:46
92. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, et al. Conducting a microbiome study. Cell. 2014;158:250-62
93. Salipante SJ, Kawashima T, Rosenthal C, Hoogestraat DR, Cummings LA, Sengupta DJ, et al. Performance comparison of Illumina and ion torrent next-generation sequencing platforms for 16S rRNA-based bacterial community profiling. Appl Environ Microbiol. 2014;80:7583-91
94. Jeraldo P, Chia N, Goldenfeld N. On the suitability of short reads of 16S rRNA for phylogeny-based analyses in environmental surveys. Environ Microbiol. 2011;13:3000-9
95. McCafferty J, Muhlbauer M, Gharaibeh RZ, Arthur JC, Perez-Chanona E, Sha W, et al. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J. 2013;7:2116-25
96. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009;77:2367-75
97. Bassis CM, Theriot CM, Young VB. Alteration of the murine gastrointestinal microbiota by tigecycline leads to increased susceptibility to Clostridium difficile infection. Antimicrob Agents Chemother. 2014;58:2767-74
98. Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y, Inoue H, et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol. 2015;15:100
99. Musso G, Gambino R, Cassader M. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes Care. 2010;33:2277-84
100. Mathur R, Barlow GM. Obesity and the microbiome. Expert Rev Gastroenterol Hepatol. 2015;9:1087-99
101. Lopez-Cepero AA, Palacios C. Association of the intestinal microbiota and obesity. P R Health Sci J. 2015;34:60-4
102. Sands SA, Tsau S, Yankee TM, Parker BL, Ericsson AC, LeVine SM. The effect of omeprazole on the development of experimental autoimmune encephalomyelitis in C57BL/6 J and SJL/J mice. BMC Res Notes. 2014;7:605
103. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One. 2014;9:e92193
104. Serino M, Luche E, Gres S, Baylac A, Berge M, Cenac C, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut. 2012;61:543-53
105. Rooks MG, Veiga P, Wardwell-Scott LH, Tickle T, Segata N, Michaud M, et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 2014;8:1403-17
106. Krych L, Nielsen DS, Hansen AK, Hansen CH. Gut microbial markers are associated with diabetes onset, regulatory imbalance, and IFN-gamma level in NOD mice. Gut Microbes. 2015;6:101-9
107. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470-81
108. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011;60:2775-86
109. Levard C, Hotze EM, Colman BP, Dale AL, Truong L, Yang XY, et al. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ Sci Technol. 2013;47:13440-8
110. Levard C, Reinsch BC, Michel FM, Oumahi C, Lowry GV, Brown GE. Sulfidation processes of PVP-coated silver nanoparticles in aqueous solution: impact on dissolution rate. Environ Sci Technol. 2011;45:5260-6
111. Reinsch BC, Levard C, Li Z, Ma R, Wise A, Gregory KB, et al. Sulfidation of silver nanoparticles decreases Escherichia coli growth inhibition. Environ Sci Technol. 2012;46:6992-7000
112. Doolette CL, McLaughlin MJ, Kirby JK, Batstone DJ, Harris HH, Ge H, et al. Transformation of PVP coated silver nanoparticles in a simulated wastewater treatment process and the effect on microbial communities. Chem Cent J. 2013;7:46
113. Rick VA, Tappero R, Arai Y. Residence time effects on phase transformation of nanosilver in reduced soils. Environ Sci Pollut Res Int. 2014;21:7828-37
114. Chen S, Theodorou IG, Goode AE, Gow A, Schwander S, Zhang JJ, et al. High-resolution analytical electron microscopy reveals cell culture mediainduced changes to the chemistry of silver nanowires. Environ Sci Technol. 2013;47:13813-21
115. Ma BW, Bokulich NA, Castillo PA, Kananurak A, Underwood MA, Mills DA, et al. Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PLoS One. 2012;7:e47416
116. Burkowska-But A, Sionkowski G, Walczak M. Influence of stabilizers on the antimicrobial properties of silver nanoparticles introduced into natural water. J Environ Sci (China). 2014;26:542-9
117. Silva T, Pokhrel LR, Dubey B, Tolaymat TM, Maier KJ, Liu X. Particle size, surface charge and concentration dependent ecotoxicity of three organocoated silver nanoparticles: comparison between general linear modelpredicted and observed toxicity. Sci Total Environ. 2014;468-469:968-76
118. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4516-22
119. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-1
120. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996-8
121. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069-72
122. Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, et al. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol. 2013;531:371-444
123. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217
124. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics. 2012;28:2106-13
125. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7
126. Benjamini YHY. Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B. 1995;57:289-300