1887

Abstract

Upon entering the human gastrointestinal tract, foodborne bacterial enteropathogens encounter, among numerous other stress conditions, nutrient competition with the host organism and the commensal microbiota. The main carbon, nitrogen and energy sources exploited by pathogens during proliferation in, and colonization of, the gut have, however, not been identified completely. In recent years, a huge body of literature has provided evidence that most enteropathogens are equipped with a large set of specific metabolic pathways to overcome nutritional limitations , thus increasing bacterial fitness during infection. These adaptations include the degradation of -inositol, ethanolamine cleaved from phospholipids, fucose derived from mucosal glycoconjugates, 1,2-propanediol as the fermentation product of fucose or rhamnose and several other metabolites not accessible for commensal bacteria or present in competition-free microenvironments. Interestingly, the data reviewed here point to common metabolic strategies of enteric pathogens allowing the exploitation of nutrient sources that not only are present in the gut lumen, the mucosa or epithelial cells, but also are abundant in food. An increased knowledge of the metabolic strategies developed by enteropathogens is therefore a key factor to better control foodborne diseases.

Funding
This study was supported by the:
  • German Research Foundation (Deutsche Forschungsgemeinschaft)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.078105-0
2014-06-01
2022-01-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/6/1020.html?itemId=/content/journal/micro/10.1099/mic.0.078105-0&mimeType=html&fmt=ahah

References

  1. Abu Kwaik Y., Bumann D. ( 2013). Microbial quest for food in vivo: ‘nutritional virulence’ as an emerging paradigm. Cell Microbiol 15:882–890 [View Article][PubMed]
    [Google Scholar]
  2. Almagro-Moreno S., Boyd E. F. ( 2009a). Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9:118 [View Article][PubMed]
    [Google Scholar]
  3. Almagro-Moreno S., Boyd E. F. ( 2009b). Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77:3807–3816 [View Article][PubMed]
    [Google Scholar]
  4. Alteri C. J., Mobley H. L. ( 2012). Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15:3–9 [View Article][PubMed]
    [Google Scholar]
  5. Alteri C. J., Smith S. N., Mobley H. L. ( 2009). Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5:e1000448 [View Article][PubMed]
    [Google Scholar]
  6. Ashida H., Miyake A., Kiyohara M., Wada J., Yoshida E., Kumagai H., Katayama T., Yamamoto K. ( 2009). Two distinct α-l-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19:1010–1017 [View Article][PubMed]
    [Google Scholar]
  7. Backhed F., Ley R. E., Sonnenburg J. L., Peterson D. A., Gordon J. I. ( 2005). Host-bacterial mutualism in the human intestine. Science 307:1915–1920 [View Article][PubMed]
    [Google Scholar]
  8. Badía J., Ros J., Aguilar J. ( 1985). Fermentation mechanism of fucose and rhamnose in Salmonella typhimurium and Klebsiella pneumoniae . J Bacteriol 161:435–437[PubMed]
    [Google Scholar]
  9. Barrett E. L., Clark M. A. ( 1987). Tetrathionate reduction and production of hydrogen sulfide from thiosulfate. Microbiol Rev 51:192–205[PubMed]
    [Google Scholar]
  10. Barthel M., Hapfelmeier S., Quintanilla-Martínez L., Kremer M., Rohde M., Hogardt M., Pfeffer K., Rüssmann H., Hardt W. D. ( 2003). Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71:2839–2858 [View Article][PubMed]
    [Google Scholar]
  11. Becker D. J., Lowe J. B. ( 2003). Fucose: biosynthesis and biological function in mammals. Glycobiology 13:41R–53R [View Article][PubMed]
    [Google Scholar]
  12. Becker D., Selbach M., Rollenhagen C., Ballmaier M., Meyer T. F., Mann M., Bumann D. ( 2006). Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 440:303–307 [View Article][PubMed]
    [Google Scholar]
  13. Behari J., Youngman P. ( 1998). Regulation of hly expression in Listeria monocytogenes by carbon sources and pH occurs through separate mechanisms mediated by PrfA. Infect Immun 66:3635–3642[PubMed]
    [Google Scholar]
  14. Bertin Y., Girardeau J. P., Chaucheyras-Durand F., Lyan B., Pujos-Guillot E., Harel J., Martin C. ( 2011). Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol 13:365–377 [View Article][PubMed]
    [Google Scholar]
  15. Bode L. ( 2006). Recent advances on structure, metabolism, and function of human milk oligosaccharides. J Nutr 136:2127–2130[PubMed]
    [Google Scholar]
  16. Borezee E., Pellegrini E., Berche P. ( 2000). OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect Immun 68:7069–7077 [View Article][PubMed]
    [Google Scholar]
  17. Bry L., Falk P. G., Midtvedt T., Gordon J. I. ( 1996). A model of host-microbial interactions in an open mammalian ecosystem. Science 273:1380–1383 [View Article][PubMed]
    [Google Scholar]
  18. Buchrieser C., Rusniok C., Kunst F., Cossart P., Glaser P. Listeria Consortium ( 2003). Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: clues for evolution and pathogenicity. FEMS Immunol Med Microbiol 35:207–213 [View Article][PubMed]
    [Google Scholar]
  19. Carnell S. C., Bowen A., Morgan E., Maskell D. J., Wallis T. S., Stevens M. P. ( 2007). Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. Microbiology 153:1940–1952 [View Article][PubMed]
    [Google Scholar]
  20. Chang D. E., Smalley D. J., Tucker D. L., Leatham M. P., Norris W. E., Stevenson S. J., Anderson A. B., Grissom J. E., Laux D. C. & other authors ( 2004). Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101:7427–7432 [View Article][PubMed]
    [Google Scholar]
  21. Chatterjee S. S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T. ( 2006). Intracellular gene expression profile of Listeria monocytogenes . Infect Immun 74:1323–1338 [View Article][PubMed]
    [Google Scholar]
  22. Chaudhuri R. R., Peters S. E., Pleasance S. J., Northen H., Willers C., Paterson G. K., Cone D. B., Allen A. G., Owen P. J. & other authors ( 2009). Comprehensive identification of Salmonella enterica serovar typhimurium genes required for infection of BALB/c mice. PLoS Pathog 5:e1000529 [View Article][PubMed]
    [Google Scholar]
  23. Chaudhuri R. R., Morgan E., Peters S. E., Pleasance S. J., Hudson D. L., Davies H. M., Wang J., van Diemen P. M., Buckley A. M. & other authors ( 2013). Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 9:e1003456 [View Article][PubMed]
    [Google Scholar]
  24. Chen Y. M., Zhu Y., Lin E. C. ( 1987). NAD-linked aldehyde dehydrogenase for aerobic utilization of l-fucose and l-rhamnose by Escherichia coli . J Bacteriol 169:3289–3294[PubMed]
    [Google Scholar]
  25. Chen P. E., Cook C., Stewart A. C., Nagarajan N., Sommer D. D., Pop M., Thomason B., Thomason M. P., Lentz S. & other authors ( 2010). Genomic characterization of the Yersinia genus. Genome Biol 11:R1 [View Article][PubMed]
    [Google Scholar]
  26. Cheng S., Sinha S., Fan C., Liu Y., Bobik T. A. ( 2011). Genetic analysis of the protein shell of the microcompartments involved in coenzyme B12-dependent 1,2-propanediol degradation by Salmonella. J Bacteriol 193:1385–1392[PubMed] [CrossRef]
    [Google Scholar]
  27. Cocks G. T., Aguilar T., Lin E. C. ( 1974). Evolution of l-1,2-propanediol catabolism in Escherichia coli by recruitment of enzymes for l-fucose and l-lactate metabolism. J Bacteriol 118:83–88[PubMed]
    [Google Scholar]
  28. Conner C. P., Heithoff D. M., Julio S. M., Sinsheimer R. L., Mahan M. J. ( 1998). Differential patterns of acquired virulence genes distinguish Salmonella strains. Proc Natl Acad Sci U S A 95:4641–4645 [View Article][PubMed]
    [Google Scholar]
  29. Contag C. H., Contag P. R., Mullins J. I., Spilman S. D., Stevenson D. K., Benaron D. A. ( 1995). Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 18:593–603 [View Article][PubMed]
    [Google Scholar]
  30. Corazziari E. S. ( 2009). Intestinal mucus barrier in normal and inflamed colon. J Pediatr Gastroenterol Nutr 48:Suppl. 2S54–S55 [View Article][PubMed]
    [Google Scholar]
  31. Cordero-Alba M., Bernal-Bayard J., Ramos-Morales F. ( 2012). SrfJ, a Salmonella type III secretion system effector regulated by PhoP, RcsB, and IolR. J Bacteriol 194:4226–4236 [View Article][PubMed]
    [Google Scholar]
  32. Cummings J. H., Macfarlane G. T. ( 1991). The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70:443–459 [View Article][PubMed]
    [Google Scholar]
  33. Cummings J. H., Pomare E. W., Branch W. J., Naylor C. P., Macfarlane G. T. ( 1987). Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227 [View Article][PubMed]
    [Google Scholar]
  34. Dainty R. H., Shaw B. G., De Boer K. A., Scheps E. S. ( 1975). Protein changes caused by bacterial growth on beef. J Appl Bacteriol 39:73–81 [View Article][PubMed]
    [Google Scholar]
  35. Dalebroux Z. D., Svensson S. L., Gaynor E. C., Swanson M. S. ( 2010). ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 74:171–199 [View Article][PubMed]
    [Google Scholar]
  36. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J. B., Massart S., Collini S., Pieraccini G., Lionetti P. ( 2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107:14691–14696 [View Article][PubMed]
    [Google Scholar]
  37. Deriu E., Liu J. Z., Pezeshki M., Edwards R. A., Ochoa R. J., Contreras H., Libby S. J., Fang F. C., Raffatellu M. ( 2013). Probiotic bacteria reduce Salmonella typhimurium intestinal colonization by competing for iron. Cell Host Microbe 14:26–37 [View Article][PubMed]
    [Google Scholar]
  38. Derrien M., Vaughan E. E., Plugge C. M., de Vos W. M. ( 2004). Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476 [View Article][PubMed]
    [Google Scholar]
  39. Dobrindt U., Hochhut B., Hentschel U., Hacker J. ( 2004). Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424 [View Article][PubMed]
    [Google Scholar]
  40. Dominguez-Bello M. G., Costello E. K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. ( 2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 107:11971–11975 [View Article][PubMed]
    [Google Scholar]
  41. Dupuy B., Daube G., Popoff M. R., Cole S. T. ( 1997). Clostridium perfringens urease genes are plasmid borne. Infect Immun 65:2313–2320[PubMed]
    [Google Scholar]
  42. Eisenreich W., Dandekar T., Heesemann J., Goebel W. ( 2010). Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8:401–412 [View Article][PubMed]
    [Google Scholar]
  43. Eylert E., Schär J., Mertins S., Stoll R., Bacher A., Goebel W., Eisenreich W. ( 2008). Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69:1008–1017 [View Article][PubMed]
    [Google Scholar]
  44. Fabich A. J., Jones S. A., Chowdhury F. Z., Cernosek A., Anderson A., Smalley D., McHargue J. W., Hightower G. A., Smith J. T. & other authors ( 2008). Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76:1143–1152 [View Article][PubMed]
    [Google Scholar]
  45. Forsythe S. J., Parker D. S. ( 1985). Nitrogen metabolism by the microbial flora of the rabbit caecum. J Appl Bacteriol 58:363–369 [View Article][PubMed]
    [Google Scholar]
  46. Fox K. A., Ramesh A., Stearns J. E., Bourgogne A., Reyes-Jara A., Winkler W. C., Garsin D. A. ( 2009). Multiple posttranscriptional regulatory mechanisms partner to control ethanolamine utilization in Enterococcus faecalis . Proc Natl Acad Sci U S A 106:4435–4440 [View Article][PubMed]
    [Google Scholar]
  47. Freter R., Brickner H., Botney M., Cleven D., Aranki A. ( 1983). Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun 39:676–685[PubMed]
    [Google Scholar]
  48. Fuchs T. M., Eisenreich W., Heesemann J., Goebel W. ( 2012a). Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats. FEMS Microbiol Rev 36:435–462 [View Article][PubMed]
    [Google Scholar]
  49. Fuchs T. M., Eisenreich W., Kern T., Dandekar T. ( 2012b). Toward a systemic understanding of Listeria monocytogenes metabolism during infection. Front Microbiol 3:23 [View Article][PubMed]
    [Google Scholar]
  50. Gantois I., Ducatelle R., Pasmans F., Haesebrouck F., Hautefort I., Thompson A., Hinton J. C., Van Immerseel F. ( 2006). Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946–949 [View Article][PubMed]
    [Google Scholar]
  51. Garsin D. A. ( 2010). Ethanolamine utilization in bacterial pathogens: roles and regulation. Nat Rev Microbiol 8:290–295 [View Article][PubMed]
    [Google Scholar]
  52. Giel J. L., Sorg J. A., Sonenshein A. L., Zhu J. ( 2010). Metabolism of bile salts in mice influences spore germination in Clostridium difficile . PLoS ONE 5:e8740 [View Article][PubMed]
    [Google Scholar]
  53. Gill S. R., Pop M., Deboy R. T., Eckburg P. B., Turnbaugh P. J., Samuel B. S., Gordon J. I., Relman D. A., Fraser-Liggett C. M., Nelson K. E. ( 2006). Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359 [View Article][PubMed]
    [Google Scholar]
  54. Golding G. R., Olson A. B., Doublet B., Cloeckaert A., Christianson S., Graham M. R., Mulvey M. R. ( 2007). The effect of the Salmonella genomic island 1 on in vitro global gene expression in Salmonella enterica serovar Typhimurium LT2. Microbes Infect 9:21–27 [View Article][PubMed]
    [Google Scholar]
  55. Gu Y., Ding Y., Ren C., Sun Z., Rodionov D. A., Zhang W., Yang S., Yang C., Jiang W. ( 2010). Reconstruction of xylose utilization pathway and regulons in Firmicutes. BMC Genomics 11:255 [View Article][PubMed]
    [Google Scholar]
  56. Hansson G. C. ( 2012). Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol 15:57–62 [View Article][PubMed]
    [Google Scholar]
  57. Haros M., Carlsson N. G., Almgren A., Larsson-Alminger M., Sandberg A. S., Andlid T. ( 2009). Phytate degradation by human gut isolated Bifidobacterium pseudocatenulatum ATCC27919 and its probiotic potential. Int J Food Microbiol 135:7–14 [View Article][PubMed]
    [Google Scholar]
  58. Harvey P. C., Watson M., Hulme S., Jones M. A., Lovell M., Berchieri A. Jr, Young J., Bumstead N., Barrow P. ( 2011). Salmonella enterica serovar Typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect Immun 79:4105–4121 [View Article][PubMed]
    [Google Scholar]
  59. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M. L., Lucchini S., Danino V., Bongaerts R. J. M., Ahmad N., Rhen M., Hinton J. C. D. ( 2008). During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10:958–984 [View Article][PubMed]
    [Google Scholar]
  60. Havemann G. D., Sampson E. M., Bobik T. A. ( 2002). PduA is a shell protein of polyhedral organelles involved in coenzyme B12-dependent degradation of 1,2-propanediol in Salmonella enterica serovar Typhimurium LT2. J Bacteriol 184:1253–1261 [View Article][PubMed]
    [Google Scholar]
  61. Heithoff D. M., Conner C. P., Hentschel U., Govantes F., Hanna P. C., Mahan M. J. ( 1999). Coordinate intracellular expression of Salmonella genes induced during infection. J Bacteriol 181:799–807[PubMed]
    [Google Scholar]
  62. Hensel M., Hinsley A. P., Nikolaus T., Sawers G., Berks B. C. ( 1999a). The genetic basis of tetrathionate respiration in Salmonella typhimurium . Mol Microbiol 32:275–287 [View Article][PubMed]
    [Google Scholar]
  63. Hensel M., Nikolaus T., Egelseer C. ( 1999b). Molecular and functional analysis indicates a mosaic structure of Salmonella pathogenicity island 2. Mol Microbiol 31:489–498 [View Article][PubMed]
    [Google Scholar]
  64. Hooper L. V., Gordon J. I. ( 2001). Glycans as legislators of host–microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11:1R–10R [View Article][PubMed]
    [Google Scholar]
  65. Hooper L. V., Xu J., Falk P. G., Midtvedt T., Gordon J. I. ( 1999). A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci U S A 96:9833–9838 [View Article][PubMed]
    [Google Scholar]
  66. Hooper L. V., Midtvedt T., Gordon J. I. ( 2002). How host–microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307 [View Article][PubMed]
    [Google Scholar]
  67. Hugdahl M. B., Beery J. T., Doyle M. P. ( 1988). Chemotactic behavior of Campylobacter jejuni . Infect Immun 56:1560–1566[PubMed]
    [Google Scholar]
  68. Jackson T. C.,, Acuff G. R., Dickson J. D. ( 1997). Meat, poultry, and seafood. Food Microbiology: Fundamentals and Frontiers83–100 Doyle M. P., Beuchat L. R., Montville T. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  69. Jay J. ( 2000). Modern Food Microbiology, 6th edn. Gaithersburg, MD: Aspen; [View Article]
    [Google Scholar]
  70. Johansson M. E., Phillipson M., Petersson J., Velcich A., Holm L., Hansson G. C. ( 2008). The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105:15064–15069 [View Article][PubMed]
    [Google Scholar]
  71. Johansson M. E., Larsson J. M., Hansson G. C. ( 2011). The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host–microbial interactions. Proc Natl Acad Sci U S A 108:Suppl. 14659–4665 [View Article][PubMed]
    [Google Scholar]
  72. Jones S. A., Chowdhury F. Z., Fabich A. J., Anderson A., Schreiner D. M., House A. L., Autieri S. M., Leatham M. P., Lins J. J. & other authors ( 2007). Respiration of Escherichia coli in the mouse intestine. Infect Immun 75:4891–4899 [View Article][PubMed]
    [Google Scholar]
  73. Joseph B., Przybilla K., Stühler C., Schauer K., Slaghuis J., Fuchs T. M., Goebel W. ( 2006). Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188:556–568 [View Article][PubMed]
    [Google Scholar]
  74. Juge N. ( 2012). Microbial adhesins to gastrointestinal mucus. Trends Microbiol 20:30–39 [View Article][PubMed]
    [Google Scholar]
  75. Kaiser P., Diard M., Stecher B., Hardt W. D. ( 2012). The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen’s virulence factors, and the host’s mucosal immune response. Immunol Rev 245:56–83 [View Article][PubMed]
    [Google Scholar]
  76. Karpathy S. E., Qin X., Gioia J., Jiang H., Liu Y., Petrosino J. F., Yerrapragada S., Fox G. E., Haake S. K. & other authors ( 2007). Genome sequence of Fusobacterium nucleatum subspecies polymorphum – a genetically tractable fusobacterium. PLoS ONE 2:e659 [View Article][PubMed]
    [Google Scholar]
  77. Katayama T., Sakuma A., Kimura T., Makimura Y., Hiratake J., Sakata K., Yamanoi T., Kumagai H., Yamamoto K. ( 2004). Molecular cloning and characterization of Bifidobacterium bifidum 1,2-α-l-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol 186:4885–4893 [View Article][PubMed]
    [Google Scholar]
  78. Keeney K. M., Finlay B. B. ( 2011). Enteric pathogen exploitation of the microbiota-generated nutrient environment of the gut. Curr Opin Microbiol 14:92–98 [View Article][PubMed]
    [Google Scholar]
  79. Kelly A., Goldberg M. D., Carroll R. K., Danino V., Hinton J. C., Dorman C. J. ( 2004). A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150:2037–2053 [View Article][PubMed]
    [Google Scholar]
  80. Kendall M. M., Gruber C. C., Parker C. T., Sperandio V. ( 2012). Ethanolamine controls expression of genes encoding components involved in interkingdom signaling and virulence in enterohemorrhagic Escherichia coli O157 : H7. MBio 3:e00050-12 [View Article][PubMed]
    [Google Scholar]
  81. Klose K. E., Mekalanos J. J. ( 1997). Simultaneous prevention of glutamine synthesis and high-affinity transport attenuates Salmonella typhimurium virulence. Infect Immun 65:587–596[PubMed]
    [Google Scholar]
  82. Klumpp J., Fuchs T. M. ( 2007). Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology 153:1207–1220 [View Article][PubMed]
    [Google Scholar]
  83. Kobata A. ( 2010). Structures and application of oligosaccharides in human milk. Proc Jpn Acad, Ser B, Phys Biol Sci 86:731–747 [View Article][PubMed]
    [Google Scholar]
  84. Kofoid E., Rappleye C., Stojiljkovic I., Roth J. ( 1999). The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. J Bacteriol 181:5317–5329[PubMed]
    [Google Scholar]
  85. Korbel J. O., Doerks T., Jensen L. J., Perez-Iratxeta C., Kaczanowski S., Hooper S. D., Andrade M. A., Bork P. ( 2005). Systematic association of genes to phenotypes by genome and literature mining. PLoS Biol 3:e134 [View Article][PubMed]
    [Google Scholar]
  86. Kröger C., Fuchs T. M. ( 2009). Characterization of the myo-inositol utilization island of Salmonella enterica serovar Typhimurium. J Bacteriol 191:545–554 [View Article][PubMed]
    [Google Scholar]
  87. Kröger C., Srikumar S., Ellwart J., Fuchs T. M. ( 2011). Bistability in myo-inositol utilization by Salmonella enterica serovar Typhimurium. J Bacteriol 193:1427–1435 [View Article][PubMed]
    [Google Scholar]
  88. Lamichhane-Khadka R., Benoit S. L., Maier S. E., Maier R. J. ( 2013). A link between gut community metabolism and pathogenesis: molecular hydrogen-stimulated glucarate catabolism aids Salmonella virulence. Open Biol 3:130146 [View Article][PubMed]
    [Google Scholar]
  89. Lawhon S. D., Frye J. G., Suyemoto M., Porwollik S., McClelland M., Altier C. ( 2003). Global regulation by CsrA in Salmonella typhimurium . Mol Microbiol 48:1633–1645 [View Article][PubMed]
    [Google Scholar]
  90. Lawley T. D., Chan K., Thompson L. J., Kim C. C., Govoni G. R., Monack D. M. ( 2006). Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2:e11 [View Article][PubMed]
    [Google Scholar]
  91. Lawrence J. G., Roth J. R. ( 1996). Evolution of coenzyme B12 synthesis among enteric bacteria: evidence for loss and reacquisition of a multigene complex. Genetics 142:11–24[PubMed]
    [Google Scholar]
  92. Le Bouguénec C., Schouler C. ( 2011). Sugar metabolism, an additional virulence factor in enterobacteria. Int J Med Microbiol 301:1–6 [View Article][PubMed]
    [Google Scholar]
  93. Lindenstrauß, A. (2012).Distribution of virulence factors in Enterococcus faecalis and its adaptation to conditions in the intestinal tract
  94. Lupp C., Robertson M. L., Wickham M. E., Sekirov I., Champion O. L., Gaynor E. C., Finlay B. B. ( 2007). Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:119–129 [View Article][PubMed]
    [Google Scholar]
  95. Maadani A., Fox K. A., Mylonakis E., Garsin D. A. ( 2007). Enterococcus faecalis mutations affecting virulence in the Caenorhabditis elegans model host. Infect Immun 75:2634–2637 [View Article][PubMed]
    [Google Scholar]
  96. Maccaferri S., Biagi E., Brigidi P. ( 2011). Metagenomics: key to human gut microbiota. Dig Dis 29:525–530 [View Article][PubMed]
    [Google Scholar]
  97. Maier R. J. ( 2005). Use of molecular hydrogen as an energy substrate by human pathogenic bacteria. Biochem Soc Trans 33:83–85 [View Article][PubMed]
    [Google Scholar]
  98. Maier R. J., Olczak A., Maier S., Soni S., Gunn J. ( 2004). Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect Immun 72:6294–6299 [View Article][PubMed]
    [Google Scholar]
  99. Maier L., Vyas R., Cordova C. D., Lindsay H., Schmidt T. S. B., Brugiroux S., Periaswamy B., Bauer R., Sturm A. & other authors ( 2013). Microbiota-derived hydrogen fuels Salmonella Typhimurium invasion of the gut ecosystem. Cell Host Microbe 14:641–651 [View Article][PubMed]
    [Google Scholar]
  100. Maltby R., Leatham-Jensen M. P., Gibson T., Cohen P. S., Conway T. ( 2013). Nutritional basis for colonization resistance by human commensal Escherichia coli strains HS and Nissle 1917 against E. coli O157 : H7 in the mouse intestine. PLoS ONE 8:e53957 [View Article][PubMed]
    [Google Scholar]
  101. Marteyn B., West N. P., Browning D. F., Cole J. A., Shaw J. G., Palm F., Mounier J., Prévost M.-C., Sansonetti P., Tang C. M. ( 2010). Modulation of Shigella virulence in response to available oxygen in vivo . Nature 465:355–358 [View Article][PubMed]
    [Google Scholar]
  102. Martin F. P., Wang Y., Yap I. K., Sprenger N., Lindon J. C., Rezzi S., Kochhar S., Holmes E., Nicholson J. K. ( 2009). Topographical variation in murine intestinal metabolic profiles in relation to microbiome speciation and functional ecological activity. J Proteome Res 8:3464–3474 [View Article][PubMed]
    [Google Scholar]
  103. Martins dos Santos V., Müller M., de Vos W. M. ( 2010). Systems biology of the gut: the interplay of food, microbiota and host at the mucosal interface. Curr Opin Biotechnol 21:539–550 [View Article][PubMed]
    [Google Scholar]
  104. Matsumoto M., Kibe R., Ooga T., Aiba Y., Kurihara S., Sawaki E., Koga Y., Benno Y. ( 2012). Impact of intestinal microbiota on intestinal luminal metabolome. Sci Rep 2:233 [View Article][PubMed]
    [Google Scholar]
  105. Maynard C. L., Elson C. O., Hatton R. D., Weaver C. T. ( 2012). Reciprocal interactions of the intestinal microbiota and immune system. Nature 489:231–241 [View Article][PubMed]
    [Google Scholar]
  106. McCormick B. A., Stocker B. A., Laux D. C., Cohen P. S. ( 1988). Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice. Infect Immun 56:2209–2217[PubMed]
    [Google Scholar]
  107. McGuckin M. A., Lindén S. K., Sutton P., Florin T. H. ( 2011). Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265–278 [View Article][PubMed]
    [Google Scholar]
  108. McNeil N. I. ( 1984). The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39:338–342[PubMed]
    [Google Scholar]
  109. Miller C. P., Bohnhoff M. ( 1963). Changes in the mouse’s enteric microflora associated with enhanced susceptibility to Salmonella infection following streptomycin treatment. J Infect Dis 113:59–66 [View Article][PubMed]
    [Google Scholar]
  110. Miura T., Okamoto K., Yanase H. ( 2005). Purification and characterization of extracellular 1,2-α-l-fucosidase from Bacillus cereus . J Biosci Bioeng 99:629–635 [View Article][PubMed]
    [Google Scholar]
  111. Muraoka W. T., Zhang Q. ( 2011). Phenotypic and genotypic evidence for l-fucose utilization by Campylobacter jejuni . J Bacteriol 193:1065–1075 [View Article][PubMed]
    [Google Scholar]
  112. Ng K. M., Ferreyra J. A., Higginbottom S. K., Lynch J. B., Kashyap P. C., Gopinath S., Naidu N., Choudhury B., Weimer B. C. & other authors ( 2013). Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:96–99 [View Article][PubMed]
    [Google Scholar]
  113. Nicholson J. K., Holmes E., Kinross J., Burcelin R., Gibson G., Jia W., Pettersson S. ( 2012). Host-gut microbiota metabolic interactions. Science 336:1262–1267 [View Article][PubMed]
    [Google Scholar]
  114. Njoroge J. W., Nguyen Y., Curtis M. M., Moreira C. G., Sperandio V. ( 2012). Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli . MBio 3:e00280–12 [View Article][PubMed]
    [Google Scholar]
  115. Obradors N., Badía J., Baldomà L., Aguilar J. ( 1988). Anaerobic metabolism of the l-rhamnose fermentation product 1,2-propanediol in Salmonella typhimurium . J Bacteriol 170:2159–2162[PubMed]
    [Google Scholar]
  116. Pacheco A. R., Curtis M. M., Ritchie J. M., Munera D., Waldor M. K., Moreira C. G., Sperandio V. ( 2012). Fucose sensing regulates bacterial intestinal colonization. Nature 492:113–117 [View Article][PubMed]
    [Google Scholar]
  117. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T. & other authors ( 2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [View Article][PubMed]
    [Google Scholar]
  118. Penrod J. T., Roth J. R. ( 2006). Conserving a volatile metabolite: a role for carboxysome-like organelles in Salmonella enterica . J Bacteriol 188:2865–2874 [View Article][PubMed]
    [Google Scholar]
  119. Pham T. A., Lawley T. D. ( 2014). Emerging insights on intestinal dysbiosis during bacterial infections. Curr Opin Microbiol 17:67–74 [View Article][PubMed]
    [Google Scholar]
  120. Poncet S., Milohanic E., Mazé A., Nait Abdallah J., Aké F., Larribe M., Deghmane A.-E., Taha M.-K., Dozot M. & other authors ( 2009). Correlations between carbon metabolism and virulence in bacteria. Contrib Microbiol 16:88–102 [View Article][PubMed]
    [Google Scholar]
  121. Power J. ( 1967). The l-rhamnose genetic system in Escherichia coli K-12. Genetics 55:557–568[PubMed]
    [Google Scholar]
  122. Price-Carter M., Tingey J., Bobik T. A., Roth J. R. ( 2001). The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar typhimurium on ethanolamine or 1,2-propanediol. J Bacteriol 183:2463–2475 [View Article][PubMed]
    [Google Scholar]
  123. Qin J., Li R., Raes J., Arumugam M., Burgdorf K. S., Manichanh C., Nielsen T., Pons N., Levenez F. & other authors ( 2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65 [View Article][PubMed]
    [Google Scholar]
  124. Reddy N. ( 2001). Occurrence, distribution, content, and dietary intake of phytate. Food Phytates25–51 Reddy N. R., Sathe S. K. Boca Raton, FL: CRC Press; [View Article]
    [Google Scholar]
  125. Robbe C., Capon C., Coddeville B., Michalski J. C. ( 2004). Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem J 384:307–316 [View Article][PubMed]
    [Google Scholar]
  126. Rohmer L., Hocquet D., Miller S. I. ( 2011). Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19:341–348 [View Article][PubMed]
    [Google Scholar]
  127. Rollenhagen C., Bumann D. ( 2006). Salmonella enterica highly expressed genes are disease specific. Infect Immun 74:1649–1660 [View Article][PubMed]
    [Google Scholar]
  128. Rondon M. R., Escalante-Semerena J. C. ( 1992). The poc locus is required for 1,2-propanediol-dependent transcription of the cobalamin biosynthetic (cob) and propanediol utilization (pdu) genes of Salmonella typhimurium . J Bacteriol 174:2267–2272[PubMed]
    [Google Scholar]
  129. Rondon M. R., Escalante-Semerena J. C. ( 1996). In vitro analysis of the interactions between the PocR regulatory protein and the promoter region of the cobalamin biosynthetic (cob) operon of Salmonella typhimurium LT2. J Bacteriol 178:2196–2203[PubMed]
    [Google Scholar]
  130. Rondon M. R., Kazmierczak R., Escalante-Semerena J. C. ( 1995). Glutathione is required for maximal transcription of the cobalamin biosynthetic and 1,2-propanediol utilization (cob/pdu) regulon and for the catabolism of ethanolamine, 1,2-propanediol, and propionate in Salmonella typhimurium LT2. J Bacteriol 177:5434–5439[PubMed]
    [Google Scholar]
  131. Roth J. R., Lawrence J. G., Bobik T. A. ( 1996). Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol 50:137–181 [View Article][PubMed]
    [Google Scholar]
  132. Ruiz-Albert J., Yu X. J., Beuzón C. R., Blakey A. N., Galyov E. E., Holden D. W. ( 2002). Complementary activities of SseJ and SifA regulate dynamics of the Salmonella typhimurium vacuolar membrane. Mol Microbiol 44:645–661 [View Article][PubMed]
    [Google Scholar]
  133. Ruiz-Palacios G. M., Cervantes L. E., Ramos P., Chavez-Munguia B., Newburg D. S. ( 2003). Campylobacter jejuni binds intestinal H(O) antigen (Fucα1, 2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278:14112–14120 [View Article][PubMed]
    [Google Scholar]
  134. Salazar J. K., Wu Z., McMullen P. D., Luo Q., Freitag N. E., Tortorello M. L., Hu S., Zhang W. ( 2013). PrfA-like transcription factor gene lmo0753 contributes to l-rhamnose utilization in Listeria monocytogenes strains associated with human food-borne infections. Appl Environ Microbiol 79:5584–5592 [View Article][PubMed]
    [Google Scholar]
  135. Salyers A. A., Pajeau M. ( 1989). Competitiveness of different polysaccharide utilization mutants of Bacteroides thetaiotaomicron in the intestinal tracts of germfree mice. Appl Environ Microbiol 55:2572–2578[PubMed]
    [Google Scholar]
  136. Sampson E. M., Bobik T. A. ( 2008). Microcompartments for B12-dependent 1,2-propanediol degradation provide protection from DNA and cellular damage by a reactive metabolic intermediate. J Bacteriol 190:2966–2971 [View Article][PubMed]
    [Google Scholar]
  137. Savage D. C. ( 1977). Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133 [View Article][PubMed]
    [Google Scholar]
  138. Schär J., Stoll R., Schauer K., Loeffler D. I., Eylert E., Joseph B., Eisenreich W., Fuchs T. M., Goebel W. ( 2010). Pyruvate carboxylase plays a crucial role in carbon metabolism of extra- and intracellularly replicating Listeria monocytogenes . J Bacteriol 192:1774–1784 [View Article][PubMed]
    [Google Scholar]
  139. Schauer K., Geginat G., Liang C., Goebel W., Dandekar T., Fuchs T. M. ( 2010). Deciphering the intracellular metabolism of Listeria monocytogenes by mutant screening and modelling. BMC Genomics 11:573 [View Article][PubMed]
    [Google Scholar]
  140. Scott K. P., Martin J. C., Campbell G., Mayer C. D., Flint H. J. ( 2006). Whole-genome transcription profiling reveals genes up-regulated by growth on fucose in the human gut bacterium “Roseburia inulinivorans”. J Bacteriol 188:4340–4349 [View Article][PubMed]
    [Google Scholar]
  141. Sela D. A., Chapman J., Adeuya A., Kim J. H., Chen F., Whitehead T. R., Lapidus A., Rokhsar D. S., Lebrilla C. B. & other authors ( 2008). The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105:18964–18969 [View Article][PubMed]
    [Google Scholar]
  142. Severi E., Hood D. W., Thomas G. H. ( 2007). Sialic acid utilization by bacterial pathogens. Microbiology 153:2817–2822 [View Article][PubMed]
    [Google Scholar]
  143. Sheppard D. E., Roth J. R. ( 1994). A rationale for autoinduction of a transcriptional activator: ethanolamine ammonia-lyase (EutBC) and the operon activator (EutR) compete for adenosyl-cobalamin in Salmonella typhimurium . J Bacteriol 176:1287–1296[PubMed]
    [Google Scholar]
  144. Snider T. A., Fabich A. J., Conway T., Clinkenbeard K. D. ( 2009). E. coli O157 : H7 catabolism of intestinal mucin-derived carbohydrates and colonization. Vet Microbiol 136:150–154 [View Article][PubMed]
    [Google Scholar]
  145. Sonnenburg J. L., Xu J., Leip D. D., Chen C. H., Westover B. P., Weatherford J., Buhler J. D., Gordon J. I. ( 2005). Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955–1959 [View Article][PubMed]
    [Google Scholar]
  146. Spees A. M., Wangdi T., Lopez C. A., Kingsbury D. D., Xavier M. N., Winter S. E., Tsolis R. M., Bäumler A. J. ( 2013). Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. MBio 4:e00430-13 [View Article][PubMed]
    [Google Scholar]
  147. Srikumar S., Fuchs T. M. ( 2011). Ethanolamine utilization contributes to proliferation of Salmonella enterica serovar Typhimurium in food and in nematodes. Appl Environ Microbiol 77:281–290 [View Article][PubMed]
    [Google Scholar]
  148. Stahl M., Friis L. M., Nothaft H., Liu X., Li J., Szymanski C. M., Stintzi A. ( 2011). l-Fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A 108:7194–7199 [View Article][PubMed]
    [Google Scholar]
  149. Stahl M., Butcher J., Stintzi A. ( 2012). Nutrient acquisition and metabolism by Campylobacter jejuni . Front Cell Infect Microbiol 2:5 [View Article][PubMed]
    [Google Scholar]
  150. Stams A. J. ( 1994). Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie van Leeuwenhoek 66:271–294 [View Article][PubMed]
    [Google Scholar]
  151. Stecher B., Hardt W. D. ( 2008). The role of microbiota in infectious disease. Trends Microbiol 16:107–114 [View Article][PubMed]
    [Google Scholar]
  152. Stecher B., Robbiani R., Walker A. W., Westendorf A. M., Barthel M., Kremer M., Chaffron S., Macpherson A. J., Buer J. & other authors ( 2007). Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5:e244 [View Article][PubMed]
    [Google Scholar]
  153. Stecher B., Barthel M., Schlumberger M. C., Haberli L., Rabsch W., Kremer M., Hardt W. D. ( 2008). Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 10:1166–1180 [View Article][PubMed]
    [Google Scholar]
  154. Steeb B., Claudi B., Burton N. A., Tienz P., Schmidt A., Farhan H., Mazé A., Bumann D. ( 2013). Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog 9:e1003301 [View Article][PubMed]
    [Google Scholar]
  155. Steyert S. R., Kaper J. B. ( 2012). Contribution of urease to colonization by Shiga toxin-producing Escherichia coli . Infect Immun 80:2589–2600 [View Article][PubMed]
    [Google Scholar]
  156. Stojiljkovic I., Bäumler A. J., Heffron F. ( 1995). Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177:1357–1366[PubMed]
    [Google Scholar]
  157. Thiennimitr P., Winter S. E., Winter M. G., Xavier M. N., Tolstikov V., Huseby D. L., Sterzenbach T., Tsolis R. M., Roth J. R., Bäumler A. J. ( 2011). Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108:17480–17485 [View Article][PubMed]
    [Google Scholar]
  158. Thomson N. R., Howard S., Wren B. W., Holden M. T. G., Crossman L., Challis G. L., Churcher C., Mungall K., Brooks K. & other authors ( 2006). The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2:e206 [View Article][PubMed]
    [Google Scholar]
  159. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T. & other authors ( 2009). The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956 [View Article][PubMed]
    [Google Scholar]
  160. Tsoy O., Ravcheev D., Mushegian A. ( 2009). Comparative genomics of ethanolamine utilization. J Bacteriol 191:7157–7164 [View Article][PubMed]
    [Google Scholar]
  161. Turnbaugh P. J., Hamady M., Yatsunenko T., Cantarel B. L., Duncan A., Ley R. E., Sogin M. L., Jones W. J., Roe B. A. & other authors ( 2009). A core gut microbiome in obese and lean twins. Nature 457:480–484 [View Article][PubMed]
    [Google Scholar]
  162. Varki A. ( 1993). Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130 [View Article][PubMed]
    [Google Scholar]
  163. Velayudhan J., Jones M. A., Barrow P. A., Kelly D. J. ( 2004). l-Serine catabolism via an oxygen-labile l-serine dehydratase is essential for colonization of the avian gut by Campylobacter jejuni . Infect Immun 72:260–268 [View Article][PubMed]
    [Google Scholar]
  164. Wang Y., Holmes E., Comelli E. M., Fotopoulos G., Dorta G., Tang H., Rantalainen M. J., Lindon J. C., Corthésy-Theulaz I. E. & other authors ( 2007). Topographical variation in metabolic signatures of human gastrointestinal biopsies revealed by high-resolution magic-angle spinning 1H NMR spectroscopy. J Proteome Res 6:3944–3951 [View Article][PubMed]
    [Google Scholar]
  165. Wexler H. M. ( 2007). Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621 [View Article][PubMed]
    [Google Scholar]
  166. Winter S. E., Bäumler A. J. ( 2014). Dysbiosis in the inflamed intestine: chance favors the prepared microbe. Gut Microbes 5:1–3 [View Article][PubMed]
    [Google Scholar]
  167. Winter S. E., Thiennimitr P., Winter M. G., Butler B. P., Huseby D. L., Crawford R. W., Russell J. M., Bevins C. L., Adams L. G. & other authors ( 2010). Gut inflammation provides a respiratory electron acceptor for Salmonella. . Nature 467:426–429 [View Article][PubMed]
    [Google Scholar]
  168. Winter S. E., Winter M. G., Xavier M. N., Thiennimitr P., Poon V., Keestra A. M., Laughlin R. C., Gomez G., Wu J. & other authors ( 2013). Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339:708–711 [View Article][PubMed]
    [Google Scholar]
  169. Worley M. J., Ching K. H., Heffron F. ( 2000). Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol 36:749–761 [View Article][PubMed]
    [Google Scholar]
  170. Zhang Y., Rodionov D. A., Gelfand M. S., Gladyshev V. N. ( 2009). Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10:78 [View Article][PubMed]
    [Google Scholar]
  171. Zheng X., Xie G., Zhao A., Zhao L., Yao C., Chiu N. H. L., Zhou Z., Bao Y., Jia W. & other authors ( 2011). The footprints of gut microbial–mammalian co-metabolism. J Proteome Res 10:5512–5522 [View Article][PubMed]
    [Google Scholar]
  172. Zúñiga M., Comas I., Linaje R., Monedero V., Yebra M. J., Esteban C. D., Deutscher J., Pérez-Martínez G., González-Candelas F. ( 2005). Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol Biol Evol 22:1673–1685 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.078105-0
Loading
/content/journal/micro/10.1099/mic.0.078105-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error