Protein-and zinc-deficient diets modulate the murine microbiome and metabolic phenotype

American Journal of Clinical Nutrition

Volumn 104, Issue 5, 2016, Pages 1253-1262

  Mayneris Perxachs, Jordi ^a   Bolick, David T ^b   Leng, Joy ^d   Medlock, Greg L ^c   Kolling, Glynis L ^a   Papin, Jason A ^b   Swann, Jonathan R ^a   Guerrant, Richard L ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF VIRGINIA   (United States)

^c University of Virginia   (United States)

^d UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Malnutrition; Metabolome metabolic phenotype; Metabolome metabonomics; Microbiome microbiota; Protein deficiency; Undernutrition; Zinc deficiency

Indexed keywords

CHOLINE; MYELOPEROXIDASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; BACTERIAL DNA; PEROXIDASE; PROTEIN INTAKE; RNA 16S; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEROIDETES; CONTROLLED STUDY; DIETARY INTAKE; ENTERITIS; FECES MICROFLORA; FIRMICUTES; GROWTH DISORDER; INTESTINE FLORA; KWASHIORKOR; MALE; METABOLOME; MOUSE; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTON NUCLEAR MAGNETIC RESONANCE; URINE SAMPLING; VERRUCOMICROBIA; ZINC DEFICIENCY; ADMINISTRATION AND DOSAGE; ANIMAL; C57BL MOUSE; DEFICIENCY; DIET; DNA SEQUENCE; FECES; GASTROINTESTINAL TRACT; GENETICS; ISOLATION AND PURIFICATION; MALNUTRITION; METABOLISM; METABOLOMICS; MICROBIOLOGY; PROTEIN INTAKE; WEANING;

ANIMALS; DIET; DIETARY PROTEINS; DNA, BACTERIAL; FECES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; LIPOCALIN-2; MALE; MALNUTRITION; METABOLOMICS; MICE; MICE, INBRED C57BL; PEROXIDASE; PROTEIN DEFICIENCY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; WEANING; ZINC;

EID: 84994223635     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.116.131797     Document Type: Article

References (25)

1. Prestes-Carneiro LE, Laraya RD, Silva PR, Moliterno RA, Felipe I, Mathias PC. Long-term effect of early protein malnutrition on growth curve, hematological parameters and macrophage function of rats. J Nutr Sci Vitaminol (Tokyo) 2006;52:414-20.
2. Belluscio LM, Berardino BG, Ferroni NM, Ceruti JM, Canepa ET. Early protein malnutrition negatively impacts physical growth and neurological reflexes and evokes anxiety and depressive-like behaviors. Physiol Behav 2014;129:237-54.
3. Ghosh TS, Gupta SS, Bhattacharya T, Yadav D, Barik A, Chowdhury A, Das B, Mande SS, Nair GB. Gut microbiomes of Indian children of varying nutritional status. PLoS One 2014;9:e95547.
4. Mayneris-Perxachs J, Lima AA, Guerrant RL, Leite AM, Moura AF, Lima NL, Soares AM, Havt A, Moore SR, Pinkerton R, et al. Urinary N-methylnicotinamide and beta-aminoisobutyric acid predict catch-up growth in undernourished Brazilian children. Sci Rep 2016;6:19780.
5. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013;339:548-54.
6. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD, et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 2014;510:417-21.
7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
8. Aronesty E. Comparison of sequencing utility programs. Durham (NC): 2011.
9. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460-1.
10. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012;6: 610-8.
11. Lozupone CA, Hamady M, Kelley ST, Knight R. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 2007; 73:1576-85.
12. Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2013;2:16.
13. Bartelt LA, Roche J, Kolling G, Bolick D, Noronha F, Naylor C, Hoffman P, Warren C, Singer S, Guerrant R. Persistent G. lamblia impairs growth in a murine malnutrition model. J Clin Invest 2013;123: 2672-84.
14. Bolick DT, Kolling GL, Moore JH 2nd, de Oliveira LA, Tung K, Philipson C, Viladomiu M, Hontecillas R, Bassaganya-Riera J, Guerrant RL. Zinc deficiency alters host response and pathogen virulence in a mouse model of enteroaggregative escherichia coli-induced diarrhea. Gut Microbes 2014;5:618-27.
15. Hoy YE, Bik EM, Lawley TD, Holmes SP, Monack DM, Theriot JA, Relman DA. Variation in taxonomic composition of the fecal microbiota in an inbred mouse strain across individuals and time. PLoS One 2015;10:e0142825.
16. DerrienM, Vaughan EE, Plugge CM, de VosWM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004;54:1469-76.
17. Banoglu E, Jha GG, King RS. Hepatic microsomal metabolism of indole to indoxyl, a precursor of indoxyl sulfate. Eur J Drug Metab Pharmacokinet 2001;26:235-40.
18. Teufel R, Mascaraque V, Ismail W, Voss M, Perera J, Eisenreich W, Haehnel W, Fuchs G. Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc Natl Acad Sci USA 2010;107:14390-5.
19. Shibata K, Onodera M, Aihara S. High-performance liquid chromatographic measurement of tryptophan in blood, tissues, urine, and foodstuffs with electrochemical and fluorometric detections. Agric Biol Chem 1991;55:1475-81.
20. Nakagawa I, Takahashi T, Suzuki T, Kobayashi K. Amino acid requirements of children: minimal needs of tryptophan, arginine and histidine based on nitrogen balance method. J Nutr 1963;80:305-10.
21. Giugliano R, Millward DJ. The effects of severe zinc deficiency on protein turnover in muscle and thymus. Br J Nutr 1987;57: 139-55.
22. Brand IA, Kleineke J. Intracellular zinc movement and its effect on the carbohydrate metabolism of isolated rat hepatocytes. J Biol Chem 1996;271:1941-9.
23. Reed S, Neuman H, Moscovich S, Glahn RP, Koren O, Tako E. Chronic zinc deficiency alters chick gut microbiota composition and function. Nutrients 2015;7:9768-84.
24. Fernandez-Prada C, Tall BD, Elliott SE, Hoover DL, Nataro JP, Venkatesan MM. Hemolysin-positive enteroaggregative and cell-detaching Escherichia coli strains cause oncosis of human monocyte-derived macrophages and apoptosis of murine J774 cells. Infect Immun 1998; 66:3918-24.
25. Yatsunyk LA, Easton JA, Kim LR, Sugarbaker SA, Bennett B, Breece RM, Vorontsov, II, Tierney DL, Crowder MW, Rosenzweig AC. Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. J Biol Inorg Chem 2008;13:271-88.