The effects of micronutrient deficiencies on bacterial species from the human gut microbiota

Science Translational Medicine

Volumn 9, Issue 390, 2017, Pages

  Hibberd, Matthew C ^a   Wu, Meng ^a   Rodionov, Dmitry A ^b,c   Li, Xiaoqing ^c   Cheng, Jiye ^a   Griffin, Nicholas W ^a   Barratt, Michael J ^a   Giannone, Richard J ^d   Hettich, Robert L ^d   Osterman, Andrei L ^c   Gordon, Jeffrey I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^c BURNHAM INSTITUTE   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLIC ACID; IRON; RETINOL; ZINC; BACTERIAL PROTEIN; REPRESSOR PROTEIN; TRACE ELEMENT;

ACRR GENE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTEROIDES VULGATUS; BILE ACID METABOLISM; BINDING SITE; CONTROLLED STUDY; GENE; GENETIC COMPLEMENTATION; GNOTOBIOTICS; INTESTINE FLORA; MALE; MASS SPECTROMETRY; MICROBIAL COMMUNITY; MICRONUTRIENT DEFICIENCY; MOLECULAR CLONING; MOUSE; NONHUMAN; NUTRITIONAL DEFICIENCY; PRIORITY JOURNAL; RETINOL DEFICIENCY; RNA SEQUENCE; TRANSPOSON; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; BACTERIUM; BACTEROIDETES; DEFICIENCY; DRUG EFFECTS; GENETICS; GERMFREE ANIMAL; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; PHYSIOLOGY;

ANIMALS; BACTERIA; BACTERIAL PROTEINS; BACTEROIDETES; GASTROINTESTINAL MICROBIOME; GERM-FREE LIFE; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; MICRONUTRIENTS; REPRESSOR PROTEINS; VITAMIN A;

EID: 85019419979     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aal4069     Document Type: Article

References (66)

1. R. L. Bailey, K. P. West Jr., R. E. Black, The epidemiology of global micronutrient deficiencies. Ann. Nutr. Metab. 66, 22-33 (2015).
2. Institute of Medicine Committee on Micronutrient Deficiencies; C. P. Howson, E. T. Kennedy, A. Horwitz, Eds., Prevention of Micronutrient Deficiencies: Tools for Policymakers and Public Health Workers (National Academy Press, 1998).
3. R. E. Black, L. H. Allen, Z. A. Bhutta, L. E. Caulfield, M. de Onis, M. Ezzati, C. Mathers, J. Rivera; Maternal and Child Undernutrition Study Group, Maternal and child undernutrition: Global and regional exposures and health consequences. Lancet 371, 243-260 (2008).
4. B. A. Underwood, Hypovitaminosis A: International programmatic issues. J. Nutr. 124, 1467S-1472S (1994).
5. World Health Organization, Guideline: Vitamin A Supplementation in Infants and Children 6-59 Months of Age (World Health Organization, 2011).
6. E. H. Harrison, Enzymes catalysing the hydrolysis of retinyl esters. Biochim. Biophys. Acta 1170, 99-108 (1993).
7. E. Mayo-Wilson, A. Imdad, K. Herzer, M. Y. Yakoob, Z. A. Bhutta, Vitamin A supplements for preventing mortality, illness, and blindness in children aged under 5: Systematic review and meta-Analysis. BMJ 343, d5094 (2011).
8. R. A. Salam, C. MacPhail, J. K. Das, Z. A. Bhutta, Effectiveness of micronutrient powders (MNP) in women and children. BMC Public Health 3 (suppl. 13), S22 (2013).
9. T. Gera and H. P. S. Sachdev, Effect of iron supplementation on incidence of infectious illness in children: Systematic review. BMJ 325, 1142 (2002).
10. T. Jaeggi, G. A. M. Kortman, D. Moretti, C. Chassard, P. Holding, A. Dostal, J. Boekhorst, H. M. Timmerman, D. W. Swinkels, H. Tjalsma, J. Njenga, A. Mwangi, J. Kvalsvig, C. Lacroix, M. B. Zimmermann, Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 64, 731-742 (2014).
11. S. Sazawal, R. E. Black, M. Ramsan, H. M. Chwaya, R. J. Stoltzfus, A. Dutta, U. Dhingra, I. Kabole, S. Deb, M. K. Othman, F. M. Kabole, Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: Community-based, randomised, placebo-controlled trial. Lancet 367, 133-143 (2006).
12. J. Veenemans, P. Milligan, A. M. Prentice, L. R. A. Schouten, N. Inja, A. C. van der Heijden, L. C. C. de Boer, E. J. S. Jansen, A. E. Koopmans, W. T. M. Enthoven, R. J. Kraaijenhagen, A. Y. Demir, D. R. A. Uges, E. V. Mbugi, H. F. J. Savelkoul, H. Verhouf, Effect of supplementation with zinc and other micronutrients on malaria in Tanzanian children: A randomised trial. PLOS Med. 8, e1001125 (2011).
13. H.Drakesmith, A.M. Prentice, Hepcidin and the iron-infection axis. Science 338, 768-772 (2012).
14. S. Soofi, S. Cousens, S. P. Iqbal, T. Akhund, J. Khan, I. Ahmed, A. K. M. Zaidi, Z. A. Bhutta, Effect of provision of daily zinc and iron with several micronutrients on growth and morbidity among young children in Pakistan: A cluster-randomised trial. Lancet 382, 29-40 (2013).
15. S. Subramanian, S. Huq, T. Yatsunenko, R. Haque, M. Mahfuz, M. A. Alam, A. Benezra, J. DeStefano, M. F. Meier, B. D. Muegge, M. J. Barratt, Q. Zhang, M. A. Province, W. A. Petri Jr., T. Ahmed, J. I. Gordon, Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 509, 417-421 (2014).
16. L. V. Blanton, M. R. Charbonneau, T. Salih, M. J. Barratt, S. Venkatesh, O. Ilkaveya, S. Subramanian, M. J. Manary, I. Trehan, J. M. Jorgensen, Y.-M. Fan, B. Henrissat, S. A. Leyn, D. A. Rodionov, A. L. Osterman, K. M. Maleta, C. B. Newgard, P. Ashorn, K. G. Dewey, J. I. Gordon, Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351, aad3311 (2016).
17. J. D. Planer, Y. Peng, A. L. Kau, L. V. Blanton, I. M. Ndao, P. I. Tarr, B. B. Warner, J. I. Gordon, Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature 534, 263-266 (2016).
18. L. V. Blanton, M. J. Barratt, M. R. Charbonneau, T. Ahmed, J. I. Gordon, Childhood undernutrition, the gut microbiota, and microbiota-directed therapeutics. Science 352, 1533 (2016).
19. S. Mandal, K. M. Godfrey, D. McDonald, W. V. Treuren, J. V. Bjørnholt, T. Midtvedt, B. Moen, K. Rudi, R. Knight, A. L. Brantsæter, S. D. Peddada, M. Eggesbø, Fat and vitamin intakes during pregnancy have stronger relations with a pro-inflammatory maternal microbiota than does carbohydrate intake. Microbiome 4, 55 (2016).
20. B. S. Reddy, J. R. Pleasants, D. R. Zimmerman, B. S. Wostmann, Iron and copper utilization in rabbits as affected by diet and germfree status. J. Nutr. 87, 189-196 (1965).
21. B. S. Reddy, J. R. Pleasants, B. S. Wostmann, Effect of intestinal microflora on iron and zinc metabolism, and on activities of metalloenzymes in rats. J. Nutr. 102, 101-107 (1972).
22. J. G. Bieri, E. G. McDaniel, W. E. Rogers Jr., Survival of germfree rats without vitamin A. Science 163, 574-575 (1969).
23. W. E. Rogers Jr., J. G. Bieri, E. G. McDaniel, Vitamin A deficiency in the germfree state. Fed. Proc. 30, 1773-1778 (1971).
24. J. C. Smith, E. G. McDaniel, L. D. McBean, F. S. Doft, J. A. Halsted, Effect of microorganisms upon zinc metabolism using germfree and conventional rats. J. Nutr. 102, 711-719 (1972).
25. H. K. Biesalski, Nutrition meets the microbiome: Micronutrients and the microbiota. Ann. N Y. Acad. Sci. 1372, 53-64 (2016).
26. J. M. Carrothers, M. A. York, S. L. Brooker, K. A. Lackey, J. E. Williams, B. Shafii, W. J. Price, M. L. Settles, M. A. McGuire, M. K. McGuire, Fecal microbial community structure is stable over time and related to variation in macronutrient and micronutrient intakes in lactating women. J. Nutr. 145, 2379-2388 (2015).
27. T. Lee, T. Clavel, K. Smirnov, A. Schmidt, I. Lagkouvardos, A. Walker, M. Lucio, B. Michalke, P. Schmitt-Kopplin, R. Fedorak, D. Haller, Oral versus intravenous iron replacement therapy distinctly alters the gut microbiota and metabolome in patients with IBD. Gut 66, 863-871 (2017).
28. T. Werner, S. J. Wagner, I. Martínez, J. Walter, J.-S. Chang, T. Clavel, S. Kisling, K. Schuemann, D. Haller, Depletion of luminal iron alters the gut microbiota and prevents Crohns disease-like ileitis. Gut 60, 325-333 (2011).
29. L. Liu, X.-H. Tang, L. J. Gudas, Homeostasis of retinol in lecithin: Retinol acyltransferase gene knockout mice fed a high retinol diet. Biochem. Pharmacol. 75, 2316-2324 (2008).
30. E. Hernandez-Alvarez, B. I. Pérez-Sacristán, I. Blanco-Navarro, E. Donoso-Navarro, R. A. Silvestre-Mardomingo, F. Granado-Lorencio, Analysis of microsamples of human faeces: A non-invasive approach to study the bioavailability of fat-soluble bioactive compounds. Eur. J. Nutr. 54, 1371-1378 (2015).
31. A. L. Goodman, N. P. McNulty, Y. Zhao, D. Leip, R. D. Mitra, C. A. Lozupone, R. Knight, J. I. Gordon, Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279-289 (2009).
32. M. Wu, N. P. McNulty, D. A. Rodionov, M. S. Khoroshkin, N. W. Griffin, J. Cheng, P. Latreille, R. A. Kerstetter, N. Terrapon, B. Henrissat, A. L. Osterman, J. I. Gordon, Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350, aac5992 (2015).
33. D. N. Crowell, M. S. Anderson, C. R. Raetz, Molecular cloning of the genes for lipid A disaccharide synthase and UDP-N-Acetylglucosamine acyltransferase in Escherichia coli. J. Bacteriol. 168, 152-159 (1986).
34. D. Ma, D. N. Cook, M. Alberti, N. G. Pon, H. Nikaido, J. E. Hearst, Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J. Bacteriol. 175, 6299-6313 (1993).
35. H. I. Zgurskaya, H. Nikaido, Bypassing the periplasm: Reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 7190-7195 (1999).
36. D. Du, Z. Wang, N. R. James, J. E. Voss, E. Klimont, T. Ohene-Agyei, H. Venter, W. Chiu, B. F. Luisi, Structure of the AcrAB-TolC multidrug efflux pump. Nature 509, 512-515 (2014).
37. J.-S. Kim, H. Jeong, S. Song, H.-Y. Kim, K. Lee, J. Hyun, N.-C. Ha, Structure of the tripartite multidrug efflux pump AcrAB-TolC suggests an alternative assembly mode. Mol. Cells 38, 180-186 (2015).
38. D. Ma, M. Alberti, C. Lynch, H. Nikaido, J. E. Hearst, The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 19, 101-112 (1996).
39. A. Raczkowska, J. Trzos, O. Lewandowska, M. Nieckarz, K. Brzostek, Expression of the AcrAB Components of the AcrAB-TolC multidrug efflux pump of Yersinia enterocolitica is subject to dual regulation by OmpR. PLOS ONE 10, e0124248 (2015).
40. E. C. Martens, H. C. Chiang, J. I. Gordon, Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447-457 (2008).
41. T. E. Renau, R. Léger, E. M. Flamme, J. Sangalang, M. W. She, R. Yen, C. L. Gannon, D. Griffith, S. Chamberland, O. Lomovskaya, S. J. Hecker, V. J. Lee, T. Ohta, K. Nakayama, Inhibitors of efflux pumps in Pseudomonas aeruginosa potentiate the activity of the fluoroquinolone antibacterial levofloxacin. J. Med. Chem. 42, 4928-4931 (1999).
42. S. I. Sayin, A. Wahlström, J. Felin, S. Jäntti, H.-U. Marschall, K. Bamberg, B. Angelin, T. Hyötyläinen, M. Orešič, F. Bäckhed, Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 17, 225-235 (2013).
43. N. Dey, V. E. Wagner, L. V. Blanton, J. Cheng, L. Fontana, R. Haque, T. Ahmed, J. I. Gordon, Regulators of gut motility revealed by a gnotobiotic model of diet-microbiome interactions related to travel. Cell 163, 95-107 (2015).
44. D. G. Thanassi, L. W. Cheng, H. Nikaido, Active efflux of bile salts by Escherichia coli. J. Bacteriol. 179, 2512-2518 (1997).
45. F. E. Rey, J. J. Faith, J. Bain, M. J. Muehlbauer, R. D. Stevens, C. B. Newgard, J. I. Gordon, Dissecting the in vivo metabolic potential of two human gut acetogens. J. Biol. Chem. 285, 22082-22090 (2010).
46. J. J. Faith, N. P. McNulty, F. E. Rey, J. I. Gordon, Predicting a human gut microbiotas response to diet in gnotobiotic mice. Science 333, 101-104 (2011).
47. N. P. McNulty, T. Yatsunenko, A. Hsiao, J. J. Faith, B. D. Muegge, A. L. Goodman, B. Henrissat, R. Oozeer, S. Cools-Portier, G. Gobert, C. Chervaux, D. Knights, C. A. Lozupone, R. Knight, A. E. Duncan, J. R. Bain, M. J. Muehlbauer, C. B. Newgard, A. C. Heath, J. I. Gordon, The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci. Transl. Med. 3, 106ra106 (2011).
48. N. P. McNulty, M. Wu, A. R. Erickson, E. C. Martens, N. A. Pudlo, B. D. Muegge, B. Henrissat, R. L. Hettich, J. I. Gordon, Effects of diet on resource utilization by a defined model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLOS Biol. 11, e1001637 (2013).
49. A. L. Goodman, G. Kallstrom, J. J. Faith, A. Reyes, A. Moore, G. Dantas, J. I. Gordon, Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl. Acad. Sci. U.S.A. 108, 6252-6257 (2011).
50. J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-Throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
51. R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).
52. B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
53. M. I. Love, W. Huber, S. Anders, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
54. R. Overbeek, R. Olson, G. D. Pusch, G. J. Olsen, J. J. Davis, T. Disz, R. A. Edwards, S. Gerdes, B. Parrello, M. Shukla, V. Vonstein, A. R. Wattam, F. Xia, R. Stevens, The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 42, D206-D214 (2013).
55. G. Yu, L.-G. Wang, Y. Han, Q.-Y. He, clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS 16, 284-287 (2012).
56. W. Luo, M. S. Friedman, K. Shedden, K. D. Hankenson, P. J. Woolf, GAGE: Generally applicable gene set enrichment for pathways analysis. BMC Bioinformatics 10, 161 (2009).
57. D. L. Tabb, C. G. Fernando, M. C. Chambers, MyriMatch: Highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661 (2007).
58. Z.-Q. Ma, S. Dasari, M. C. Chambers, M. D. Litton, S. M. Sobecki, L. J. Zimmerman, P. J. Halvey, B. Schilling, P. M. Drake, B. W. Gibson, D. L. Tabb, IDPicker 2.0: Improved protein assembly with high discrimination peptide information filtering. J. Proteome Res. 8, 3872-3781 (2009).
59. Q. Xu, M. G. Resch, K. Podkaminer, S. Yang, J. O. Baker, B. S. Donohoe, C. Wilson, D. M. Klingeman, D. G. Olson, S. R. Decker, R. J. Giannone, R. L. Hettich, S. D. Brown, L. R. Lynd, E. A. Bayer, M. E. Himmel, Y. J. Bomble, Dramatic performance of Clostridium thermocellum explained by its wide range of cellulose modalities. Sci. Adv. 2, e1501254 (2016).
60. T. Taverner, Y. V. Karpievitch, A. D. Polpitiya, J. N. Brown, A. R. Dabney, G. A. Anderson, R. D. Smith, DanteR: An extensible R-based tool for quantitative analysis of-omics data. Bioinformatics 28, 2404-2406 (2012).
61. P. S. Novichkov, D. A. Rodionov, E. D. Stavrovskaya, E. S. Novichkova, A. E. Kazakov, M. S. Gelfand, A. P. Arkin, A. A. Mironov, I. Dubchak, RegPredict: An integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res. 38, W299-W307 (2010).
62. D. A. Rodionov, Comparative genomic reconstruction of transcriptional regulatory networks in bacteria. Chem. Rev. 107, 3467-3497 (2007).
63. G. E. Crooks, G. Hon, J.-M. Chandonia, S. E. Brenner, WebLogo: A sequence logo generator. Genome Res. 14, 1188-1190 (2004).
64. E. Mossessova, C. D. Lima, Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876 (2000).
65. C. Chang, C. Tesar, X. Li, Y. Kim, D. A. Rodionov, A. Joachimiak, A novel transcriptional regulator of L-Arabinose utilization in human gut bacteria. Nucleic Acids Res. 43, 10546-10559 (2015).
66. D. A. Ravcheev, X. Li, H. Latif, K. Zengler, S. A. Leyn, Y. D. Korostelev, A. E. Kazakov, P. S. Novichkov, A. L. Osterman, D. A. Rodionov, Transcriptional regulation of central carbon and energy metabolism in bacteria by redox-responsive repressor Rex. J. Bacteriol. 194, 1145-1157 (2012).