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Bacterial Metabolism Shapes the Host–Pathogen Interface

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  • Authors: Karla D. Passalacqua1, Marie-Eve Charbonneau2, Mary X.D. O’Riordan3
  • Editors: Indira T. Kudva4, Nancy A. Cornick5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109; 2: Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109; 3: Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, MI 48109; 4: National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA; 5: Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA
    • Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0027-2015
  • Received 03 September 2015 Accepted 12 January 2016 Published 13 May 2016
  • Mary X.D. O’Riordan, [email protected]
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  • Abstract:

    Bacterial pathogens have evolved to exploit humans as a rich source of nutrients to support survival and replication. The pathways of bacterial metabolism that permit successful colonization are surprisingly varied and highlight remarkable metabolic flexibility. The constraints and immune pressures of distinct niches within the human body set the stage for understanding the mechanisms by which bacteria acquire critical nutrients. In this article we discuss how different bacterial pathogens carry out carbon and energy metabolism in the host and how they obtain or use key nutrients for replication and immune evasion.

  • Citation: Passalacqua K, Charbonneau M, O’Riordan M. 2016. Bacterial Metabolism Shapes the Host–Pathogen Interface. Microbiol Spectrum 4(3):VMBF-0027-2015. doi:10.1128/microbiolspec.VMBF-0027-2015.

References

1. Rohmer L, Hocquet D, Miller SI. 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19:341–348. [PubMed][CrossRef]
2. Lipmann F. 1941. Metabolic generation and utilization of phosphate bond energy. Adv Enzymol 1:99–162. [CrossRef]
3. de Duve C. 2013. The other revolution in the life sciences. Science 339:1148. [PubMed][CrossRef]
4. Adler CJ, Dobney K, Weyrich LS, Kaidonis J, Walker AW, Haak W, Bradshaw CJ, Townsend G, Soltysiak A, Alt KW, Parkhill J, Cooper A. 2013. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial Revolutions. Nat Genet 45:450–455. [PubMed][CrossRef]
5. Moye ZD, Zeng L, Burne RA. 2014. Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans. J Oral Microbiol 6. doi:10.3402/jom.v6.24878. [PubMed][CrossRef]
6. Abranches J, Nascimento MM, Zeng L, Browngardt CM, Wen ZT, Rivera MF, Burne RA. 2008. CcpA regulates central metabolism and virulence gene expression in Streptococcus mutans. J Bacteriol 190:2340–2349. [PubMed][CrossRef]
7. Kietzman CC, Caparon MG. 2011. Distinct time-resolved roles for two catabolite-sensing pathways during Streptococcus pyogenes infection. Infect Immun 79:812–821. [PubMed][CrossRef]
8. Iyer R, Baliga NS, Camilli A. 2005. Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J Bacteriol 187:8340–8349. [PubMed][CrossRef]
9. Carvalho SM, Kloosterman TG, Kuipers OP, Neves AR. 2011. CcpA ensures optimal metabolic fitness of Streptococcus pneumoniae. PLoS One 6:e26707. doi:10.1371/journal.pone.0026707. [PubMed][CrossRef]
10. Bidossi A, Mulas L, Decorosi F, Colomba L, Ricci S, Pozzi G, Deutscher J, Viti C, Oggioni MR. 2012. A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS One 7:e33320. doi:10.1371/journal.pone.0033320. [PubMed][CrossRef]
11. King SJ, Hippe KR, Weiser JN. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol 59:961–974. [PubMed][CrossRef]
12. Shelburne SA, Davenport MT, Keith DB, Musser JM. 2008. The role of complex carbohydrate catabolism in the pathogenesis of invasive streptococci. Trends Microbiol 16:318–325. [PubMed][CrossRef]
13. Burnaugh AM, Frantz LJ, King SJ. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190:221–230. [PubMed][CrossRef]
14. Bowden SD, Rowley G, Hinton JC, Thompson A. 2009. Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar Typhimurium. Infect Immun 77:3117–3126. [PubMed][CrossRef]
15. Tchawa Yimga M, Leatham MP, Allen JH, Laux DC, Conway T, Cohen PS. 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect Immun 74:1130–1140. [PubMed][CrossRef]
16. Dougan G, Baker S. 2014. Salmonella enterica serovar Typhi and the pathogenesis of typhoid fever. Annu Rev Microbiol 68:317–336. [PubMed][CrossRef]
17. Thiennimitr P, Winter SE, Baumler AJ. 2012. Salmonella, the host and its microbiota. Curr Opin Microbiol 15:108–114. [PubMed][CrossRef]
18. Salcedo SP, Noursadeghi M, Cohen J, Holden DW. 2001. Intracellular replication of Salmonella Typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol 3:587–597. [PubMed][CrossRef]
19. Mercado-Lubo R, Leatham MP, Conway T, Cohen PS. 2009. Salmonella enterica serovar Typhimurium mutants unable to convert malate to pyruvate and oxaloacetate are avirulent and immunogenic in BALB/c mice. Infect Immun 77:1397–1405. [PubMed][CrossRef]
20. Martinez FO, Gordon S. 2014. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000prime Rep 6:13. [PubMed][CrossRef]
21. Xavier MN, Winter MG, Spees AM, den Hartigh AB, Nguyen K, Roux CM, Silva TM, Atluri VL, Kerrinnes T, Keestra AM, Monack DM, Luciw PA, Eigenheer RA, Baumler AJ, Santos RL, Tsolis RM. 2013. PPARgamma-mediated increase in glucose availability sustains chronic Brucella abortus infection in alternatively activated macrophages. Cell Host Microbe 14:159–170. [PubMed][CrossRef]
22. Kang K, Reilly SM, Karabacak V, Gangl MR, Fitzgerald K, Hatano B, Lee CH. 2008. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell Metab 7:485–495. [PubMed][CrossRef]
23. Eisele NA, Ruby T, Jacobson A, Manzanillo PS, Cox JS, Lam L, Mukundan L, Chawla A, Monack DM. 2013. Salmonella require the fatty acid regulator PPARdelta for the establishment of a metabolic environment essential for long-term persistence. Cell Host Microbe 14:171–182. [PubMed][CrossRef]
24. Bloch H, Segal W. 1956. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72:132–141. [PubMed]
25. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544. [PubMed][CrossRef]
26. Sassetti CM, Rubin EJ. 2003. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100:12989–12994. [PubMed][CrossRef]
27. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, Bardou F, Daffe M, Emile JF, Marchou B, Cardona PJ, de Chastellier C, Altare F. 2008. Foamy macrophages from tuberculous patients’ granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4:e1000204. doi:10.1371/journal.ppat.1000204. [PubMed][CrossRef]
28. Daniel J, Maamar H, Deb C, Sirakova TD, Kolattukudy PE. 2011. Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 7:e1002093. doi:10.1371/journal.ppat.1002093. [PubMed][CrossRef]
29. Munoz-Elias EJ, McKinney JD. 2005. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11:638–644. [PubMed][CrossRef]
30. Gevers D, Knight R, Petrosino JF, Huang K, McGuire AL, Birren BW, Nelson KE, White O, Methe BA, Huttenhower C. 2012. The Human Microbiome Project: a community resource for the healthy human microbiome. PLoS Biol 10:e1001377. doi:10.1371/journal.pbio.1001377. [CrossRef]
31. Grice EA, Segre JA. 2012. The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170. [PubMed][CrossRef]
32. Vedantam G, Clark A, Chu M, McQuade R, Mallozzi M, Viswanathan VK. 2012. Clostridium difficile infection: toxins and non-toxin virulence factors, and their contributions to disease establishment and host response. Gut Microbes 3:121–134. [PubMed][CrossRef]
33. Ferreyra JA, Wu KJ, Hryckowian AJ, Bouley DM, Weimer BC, Sonnenburg JL. 2014. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16:770–777. [PubMed][CrossRef]
34. Njoroge JW, Gruber C, Sperandio V. 2013. The interacting Cra and KdpE regulators are involved in the expression of multiple virulence factors in enterohemorrhagic Escherichia coli. J Bacteriol 195:2499–2508. [PubMed][CrossRef]
35. Pacheco AR, Curtis MM, Ritchie JM, Munera D, Waldor MK, Moreira CG, Sperandio V. 2012. Fucose sensing regulates bacterial intestinal colonization. Nature 492:113–117. [PubMed][CrossRef]
36. Curtis MM, Hu Z, Klimko C, Narayanan S, Deberardinis R, Sperandio V. 2014. The Gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe 16:759–769. [PubMed][CrossRef]
37. Brown SA, Whiteley M. 2007. A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol 189:6407–6414. [PubMed][CrossRef]
38. Ramsey MM, Rumbaugh KP, Whiteley M. 2011. Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7:e1002012. doi:10.1371/journal.ppat.1002012. [PubMed][CrossRef]
39. Chico-Calero I, Suarez M, Gonzalez-Zorn B, Scortti M, Slaghuis J, Goebel W, Vazquez-Boland JA, European Listeria Genome Consortium. 2002. Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc Natl Acad Sci USA 99:431–436. [PubMed][CrossRef]
40. Keeney KM, Stuckey JA, O’Riordan MX. 2007. LplA1-dependent utilization of host lipoyl peptides enables Listeria cytosolic growth and virulence. Mol Microbiol 66:758–770. [PubMed][CrossRef]
41. O’Riordan M, Moors MA, Portnoy DA. 2003. Listeria intracellular growth and virulence require host-derived lipoic acid. Science 302:462–464. [PubMed][CrossRef]
42. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, Berche P, Bloecker H, Brandt P, Chakraborty T, Charbit A, Chetouani F, Couve E, de Daruvar A, Dehoux P, Domann E, Dominguez-Bernal G, Duchaud E, Durant L, Dussurget O, Entian KD, Fsihi H, Portillo FG, Garrido P, Gautier L, Goebel W, Gomez-Lopez N, Hain T, Hauf J, Jackson D, Jones LM, Kaerst U, Kreft J, Kuhn M, Kunst F, Kurapkat G, Madueno E, Maitournam A, Vicente JM, Ng E, Nedjari H, Nordsiek G, Novella S, de Pablos B, Perez-Diaz JC, Purcell R, Remmel B, Rose M, Schlueter T, Simoes N, Tierrez A, Vazquez-Boland JA, Voss H, Wehland J, Cossart P. 2001. Comparative genomics of Listeria species. Science 294:849–852. [PubMed]
43. Zhao X, Miller JR, Jiang Y, Marletta MA, Cronan JE. 2003. Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol 10:1293–1302. [PubMed][CrossRef]
44. Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C, Tsolis RM, Baumler AJ. 2009. Life in the inflamed intestine, Salmonella style. Trends Microbiol 17:498–506. [PubMed][CrossRef]
45. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, Kremer M, Chaffron S, Macpherson AJ, Buer J, Parkhill J, Dougan G, von Mering C, Hardt WD. 2007. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5:2177–2189. doi:10.1371/journal.pbio.0050244. [PubMed][CrossRef]
46. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Baumler AJ. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–429. [PubMed][CrossRef]
47. Lopez CA, Winter SE, Rivera-Chavez F, Xavier MN, Poon V, Nuccio SP, Tsolis RM, Baumler AJ. 2012. Phage-mediated acquisition of a type III secreted effector protein boosts growth of Salmonella by nitrate respiration. mBio 3:e00143-12. doi:10.1128/mBio.00143-12. [PubMed][CrossRef]
48. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM. 2008. Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13:1205–1218. [PubMed][CrossRef]
49. Klein JS, Lewinson O. 2011. Bacterial ATP-driven transporters of transition metals: physiological roles, mechanisms of action, and roles in bacterial virulence. Metallomics 3:1098–1108. [PubMed][CrossRef]
50. Hood MI, Skaar EP. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525–537. [PubMed][CrossRef]
51. Weinberg ED. 1975. Nutritional immunity. Host’s attempt to withold iron from microbial invaders. JAMA 231:39–41. [PubMed][CrossRef]
52. Johnson EE, Wessling-Resnick M. 2012. Iron metabolism and the innate immune response to infection. Microbes Infect 14:207–216. [PubMed][CrossRef]
53. Cellier MF, Courville P, Campion C. 2007. Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9:1662–1670. [PubMed][CrossRef]
54. Franza T, Expert D. 2013. Role of iron homeostasis in the virulence of phytopathogenic bacteria: an ‘a la carte’ menu. Mol Plant Pathol 14:429–438. [PubMed][CrossRef]
55. Geiser DL, Winzerling JJ. 2012. Insect transferrins: multifunctional proteins. Biochim Biophys Acta 1820:437–451. [PubMed][CrossRef]
56. Aranda J, Cortes P, Garrido ME, Fittipaldi N, Llagostera M, Gottschalk M, Barbe J. 2009. Contribution of the FeoB transporter to Streptococcus suis virulence. Int Microbiol 12:137–143. [PubMed]
57. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC. 2006. Feo-transport of ferrous iron into bacteria. Biometals 19:143–157. [PubMed][CrossRef]
58. Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A. 2006. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74:5433–5444. [PubMed][CrossRef]
59. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, Strong RK, Akira S, Aderem A. 2004. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432:917–921. [PubMed][CrossRef]
60. Hantke K, Nicholson G, Rabsch W, Winkelmann G. 2003. Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci USA 100:3677–3682. [PubMed][CrossRef]
61. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA, Butler BP, Chu H, Santos RL, Berger T, Mak TW, Tsolis RM, Bevins CL, Solnick JV, Dandekar S, Baumler AJ. 2009. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5:476–486. [PubMed][CrossRef]
62. Crouch ML, Castor M, Karlinsey JE, Kalhorn T, Fang FC. 2008. Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol Microbiol 67:971–983. [PubMed][CrossRef]
63. Drago-Serrano ME, Parra SG, Manjarrez-Hernandez HA. 2006. EspC, an autotransporter protein secreted by enteropathogenic Escherichia coli (EPEC), displays protease activity on human hemoglobin. FEMS Microbiol Lett 265:35–40. [PubMed][CrossRef]
64. Porcheron G, Garenaux A, Proulx J, Sabri M, Dozois CM. 2013. Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 3:90. [PubMed][CrossRef]
65. Coates R, Moran J, Horsburgh MJ. 2014. Staphylococci: colonizers and pathogens of human skin. Future Microbiol 9:75–91. [PubMed][CrossRef]
66. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339:520–532. [PubMed][CrossRef]
67. Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O. 2004. Iron-source preference of Staphylococcus aureus infections. Science 305:1626–1628. [PubMed][CrossRef]
68. Hammer ND, Skaar EP. 2011. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 65:129–147. [PubMed][CrossRef]
69. Pishchany G, Dickey SE, Skaar EP. 2009. Subcellular localization of the Staphylococcus aureus heme iron transport components IsdA and IsdB. Infect Immun 77:2624–2634. [PubMed][CrossRef]
70. Fabian M, Solomaha E, Olson JS, Maresso AW. 2009. Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis. J Biol Chem 284:32138–32146. [PubMed][CrossRef]
71. Honsa ES, Fabian M, Cardenas AM, Olson JS, Maresso AW. 2011. The five near-iron transporter (NEAT) domain anthrax hemophore, IsdX2, scavenges heme from hemoglobin and transfers heme to the surface protein IsdC. J Biol Chem 286:33652–33660. [PubMed][CrossRef]
72. Maresso AW, Garufi G, Schneewind O. 2008. Bacillus anthracis secretes proteins that mediate heme acquisition from hemoglobin. PLoS Pathog 4:e1000132. doi:10.1371/journal.ppat.1000132. [PubMed][CrossRef]
73. Andreini C, Banci L, Bertini I, Rosato A. 2006. Zinc through the three domains of life. J Proteome Res 5:3173–3178. [PubMed][CrossRef]
74. Cerasi M, Ammendola S, Battistoni A. 2013. Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3:108. [PubMed][CrossRef]
75. Kehres DG, Maguire ME. 2003. Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27:263–290. [PubMed][CrossRef]
76. Glaser R, Harder J, Lange H, Bartels J, Christophers E, Schroder JM. 2005. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 6:57–64. [PubMed][CrossRef]
77. Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR, Torres VJ, Anderson KL, Dattilo BM, Dunman PM, Gerads R, Caprioli RM, Nacken W, Chazin WJ, Skaar EP. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319:962–965. [PubMed][CrossRef]
78. Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G, Skaar EP, Chazin WJ. 2013. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci USA 110:3841–3846. [PubMed][CrossRef]
79. Jabado N, Jankowski A, Dougaparsad S, Picard V, Grinstein S, Gros P. 2000. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J Exp Med 192:1237–1248. [PubMed][CrossRef]
80. Begum NA, Kobayashi M, Moriwaki Y, Matsumoto M, Toyoshima K, Seya T. 2002. Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 80:630–645. [PubMed][CrossRef]
81. Kitamura H, Morikawa H, Kamon H, Iguchi M, Hojyo S, Fukada T, Yamashita S, Kaisho T, Akira S, Murakami M, Hirano T. 2006. Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat Immunol 7:971–977. [PubMed][CrossRef]
82. Kehl-Fie TE, Zhang Y, Moore JL, Farrand AJ, Hood MI, Rathi S, Chazin WJ, Caprioli RM, Skaar EP. 2013. MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect Immun 81:3395–3405. [PubMed][CrossRef]
83. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, Sugitani N, Chazin WJ, Caprioli RM, Skaar EP. 2012. Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8:e1003068. doi:10.1371/journal.ppat.1003068. [PubMed][CrossRef]
84. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227–239. [PubMed][CrossRef]
85. Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y, Brandli I, Wang C, Tailleux L, Tilleul S, Charriere GM, Waddell SJ, Foti M, Lugo-Villarino G, Gao Q, Maridonneau-Parini I, Butcher PD, Castagnoli PR, Gicquel B, de Chastellier C, Neyrolles O. 2011. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10:248–259. [PubMed][CrossRef]
86. Sabri M, Houle S, Dozois CM. 2009. Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infect Immun 77:1155–1164. [PubMed][CrossRef]
87. Dupont CL, Grass G, Rensing C. 2011. Copper toxicity and the origin of bacterial resistance: new insights and applications. Metallomics 3:1109–1118. [PubMed][CrossRef]
88. Hodgkinson V, Petris MJ. 2012. Copper homeostasis at the host-pathogen interface. J Biol Chem 287:13549–13555. [PubMed][CrossRef]
89. White C, Lee J, Kambe T, Fritsche K, Petris MJ. 2009. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J Biol Chem 284:33949–33956. [PubMed][CrossRef]
90. Macomber L, Imlay JA. 2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 106:8344–8349. [PubMed][CrossRef]
91. Djoko KY, Franiek JA, Edwards JL, Falsetta ML, Kidd SP, Potter AJ, Chen NH, Apicella MA, Jennings MP, McEwan AG. 2012. Phenotypic characterization of a copA mutant of Neisseria gonorrhoeae identifies a link between copper and nitrosative stress. Infect Immun 80:1065–1071. [PubMed][CrossRef]
92. Samanovic MI, Ding C, Thiele DJ, Darwin KH. 2012. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11:106–115. [PubMed][CrossRef]
93. Gold B, Deng H, Bryk R, Vargas D, Eliezer D, Roberts J, Jiang X, Nathan C. 2008. Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 4:609–616. [PubMed][CrossRef]
94. Schwan WR, Warrener P, Keunz E, Stover CK, Folger KR. 2005. Mutations in the cueA gene encoding a copper homeostasis P-type ATPase reduce the pathogenicity of Pseudomonas aeruginosa in mice. Int J Med Microbiol 295:237–242. [PubMed][CrossRef]
95. Wolschendorf F, Ackart D, Shrestha TB, Hascall-Dove L, Nolan S, Lamichhane G, Wang Y, Bossmann SH, Basaraba RJ, Niederweis M. 2011. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 108:1621–1626. [PubMed][CrossRef]
96. Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP. 2012. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol 8:731–736. [PubMed][CrossRef]
97. Abu Kwaik Y, Bumann D. 2013. Microbial quest for food in vivo: “nutritional virulence” as an emerging paradigm. Cell Microbiol 15:882–890. [PubMed][CrossRef]
98. Almagro-Moreno S, Boyd EF. 2009. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 77:3807–3816. [PubMed][CrossRef]
99. Jeong HG, Oh MH, Kim BS, Lee MY, Han HJ, Choi SH. 2009. The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun 77:3209–3217. [PubMed][CrossRef]
100. Almagro-Moreno S, Boyd EF. 2010. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes 1:45–50. [PubMed][CrossRef]
101. Soong G, Muir A, Gomez MI, Waks J, Reddy B, Planet P, Singh PK, Kaneko Y, Wolfgang MC, Hsiao YS, Tong L, Prince A. 2006. Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest 116:2297–2305. [PubMed][CrossRef]
102. Alkhuder K, Meibom KL, Dubail I, Dupuis M, Charbit A. 2009. Glutathione provides a source of cysteine essential for intracellular multiplication of F rancisella tularensis. PLoS Pathog 5:e1000284. doi:10.1371/journal.ppat.1000284. [PubMed][CrossRef]
103. Scidmore MA. 2011. Recent advances in Chlamydia subversion of host cytoskeletal and membrane trafficking pathways. Microbes Infect 13:527–535. [PubMed][CrossRef]
104. Derre I, Swiss R, Agaisse H. 2011. The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER- Chlamydia inclusion membrane contact sites. PLoS Pathog 7:e1002092. doi:10.1371/journal.ppat.1002092. [PubMed][CrossRef]
105. Elwell CA, Jiang S, Kim JH, Lee A, Wittmann T, Hanada K, Melancon P, Engel JN. 2011. Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog 7:e1002198. doi:10.1371/journal.ppat.1002198. [PubMed][CrossRef]
106. Ouellette SP, Dorsey FC, Moshiach S, Cleveland JL, Carabeo RA. 2011. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 6:e16783. doi:10.1371/journal.pone.0016783. [PubMed][CrossRef]
107. Ghigo E, Colombo MI, Heinzen RA. 2012. The Coxiella burnetii parasitophorous vacuole. Adv Exp Med Biol 984:141–169. [PubMed][CrossRef]
108. Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T. 1996. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun 64:796–809. [PubMed]
109. Isberg RR, O’Connor TJ, Heidtman M. 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7:13–24. [PubMed][CrossRef]
110. Price CT, Al-Quadan T, Santic M, Rosenshine I, Abu Kwaik Y. 2011. Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science 334:1553–1557. [PubMed][CrossRef]
111. Bruckert WM, Price CT, Abu Kwaik Y. 2014. Rapid nutritional remodeling of the host cell upon attachment of Legionella pneumophila. Infect Immun 82:72–82. [PubMed][CrossRef]
112. Sauer JD, Bachman MA, Swanson MS. 2005. The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc Natl Acad Sci USA 102:9924–9929. [PubMed][CrossRef]
113. Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N, Kawula T. 2013. Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog 9:e1003562. doi:10.1371/journal.ppat.1003562. [PubMed][CrossRef]
114. Niu H, Xiong Q, Yamamoto A, Hayashi-Nishino M, Rikihisa Y. 2012. Autophagosomes induced by a bacterial Beclin 1 binding protein facilitate obligatory intracellular infection. Proc Natl Acad Sci USA 109:20800–20807. [PubMed][CrossRef]
115. Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, Hardt WD. 2004. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72:4138–4150. [PubMed][CrossRef]
116. Rivera-Chavez F, Winter SE, Lopez CA, Xavier MN, Winter MG, Nuccio SP, Russell JM, Laughlin RC, Lawhon SD, Sterzenbach T, Bevins CL, Tsolis RM, Harshey R, Adams LG, Baumler AJ. 2013. Salmonella uses energy taxis to benefit from intestinal inflammation. PLoS Pathog 9:e1003267. doi:10.1371/journal.ppat.1003267. [PubMed][CrossRef]
117. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI. 2005. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955–1959. [PubMed][CrossRef]
118. Zhang YJ, Reddy MC, Ioerger TR, Rothchild AC, Dartois V, Schuster BM, Trauner A, Wallis D, Galaviz S, Huttenhower C, Sacchettini JC, Behar SM, Rubin EJ. 2013. Tryptophan biosynthesis protects mycobacteria from CD4 T-cell-mediated killing. Cell 155:1296–1308. [PubMed][CrossRef]
119. Schmidt SV, Schultze JL. 2014. New insights into IDO biology in bacterial and viral infections. Front Immunol 5:384. [PubMed][CrossRef]
120. MacKenzie CR, Gonzalez RG, Kniep E, Roch S, Daubener W. 1999. Cytokine mediated regulation of interferon-gamma-induced IDO activation. Adv Exp Med Biol 467:533–539. [PubMed][CrossRef]
121. Pearce EL, Pearce EJ. 2013. Metabolic pathways in immune cell activation and quiescence. Immunity 38:633–643. [PubMed][CrossRef]
122. Zarek PE, Powell JD. 2007. Adenosine and anergy. Autoimmunity 40:425–432. [PubMed][CrossRef]
123. Thiel M, Caldwell CC, Sitkovsky MV. 2003. The critical role of adenosine A2A receptors in downregulation of inflammation and immunity in the pathogenesis of infectious diseases. Microbes Infect 5:515–526. [PubMed][CrossRef]
124. Boucher HW, Corey GR. 2008. Epidemiology of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46(Suppl 5) :S344–S349. [PubMed][CrossRef]
125. Thammavongsa V, Kern JW, Missiakas DM, Schneewind O. 2009. Staphylococcus aureus synthesizes adenosine to escape host immune responses. J Exp Med 206:2417–2427. [PubMed][CrossRef]
126. Chubukov V, Gerosa L, Kochanowski K, Sauer U. 2014. Coordination of microbial metabolism. Nat Rev Microbiol 12:327–340. [PubMed][CrossRef]
127. Fetherston JD, Mier I, Jr, Truszczynska H, Perry RD. 2012. The Yfe and Feo transporters are involved in microaerobic growth and virulence of Yersinia pestis in bubonic plague. Infect Immun 80:3880–3891. [PubMed][CrossRef]
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/content/journal/microbiolspec/10.1128/microbiolspec.VMBF-0027-2015
2016-05-13
2020-07-14

Abstract:

Bacterial pathogens have evolved to exploit humans as a rich source of nutrients to support survival and replication. The pathways of bacterial metabolism that permit successful colonization are surprisingly varied and highlight remarkable metabolic flexibility. The constraints and immune pressures of distinct niches within the human body set the stage for understanding the mechanisms by which bacteria acquire critical nutrients. In this article we discuss how different bacterial pathogens carry out carbon and energy metabolism in the host and how they obtain or use key nutrients for replication and immune evasion.

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Bacterial Metabolism Shapes the Host–Pathogen Interface
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Citation: Passalacqua K, Charbonneau M, O’Riordan M. 2016. Bacterial metabolism shapes the host–pathogen interface. microbiolspec 4(3): doi:10.1128/microbiolspec.VMBF-0027-2015
/content/microbiolspec/10.1128/microbiolspec.VMBF-0027-2015.fig1
FIGURE 1

A simplified view of catabolic energy-yielding pathways in bacteria and points of relevance for the indicated bacterial pathogens. The figure shows a simplified outline of some of the different pathways for utilizing carbohydrates or fatty acids for the generation of ATP. These catabolic pathways and the anabolic pathways that they feed are under extremely complex levels of control, which have been studied mainly in noninfectious organisms ( 126 ). However, the unique metabolic strategies employed by infectious bacteria are becoming more appreciated as important aspects of bacterial pathogenesis ( 1 ). *ATP generated by substrate level phosphorylation; **ATP generated by oxidative phosphorylation; solid lines, metabolic pathway; dashed lines, substrates that feed into catabolic pathways and products generated by bacteria as a result of metabolism or required for metabolism; dotted lines, main energy-yielding metabolites generated from pathways. Blue letters indicate specific points of importance for the energy-yielding metabolism of select pathogens listed as follows (see Table 1 for summary): Pathogenic streptococci (, , ); serovar Typhimurium; ; ; ; Enterohemorrhagic ; ; .

microbiolspec/4/3/VMBF-0027-2015-fig1_thmb.gif
microbiolspec/4/3/VMBF-0027-2015-fig1.gif
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FIGURE 1

A simplified view of catabolic energy-yielding pathways in bacteria and points of relevance for the indicated bacterial pathogens. The figure shows a simplified outline of some of the different pathways for utilizing carbohydrates or fatty acids for the generation of ATP. These catabolic pathways and the anabolic pathways that they feed are under extremely complex levels of control, which have been studied mainly in noninfectious organisms ( 126 ). However, the unique metabolic strategies employed by infectious bacteria are becoming more appreciated as important aspects of bacterial pathogenesis ( 1 ). *ATP generated by substrate level phosphorylation; **ATP generated by oxidative phosphorylation; solid lines, metabolic pathway; dashed lines, substrates that feed into catabolic pathways and products generated by bacteria as a result of metabolism or required for metabolism; dotted lines, main energy-yielding metabolites generated from pathways. Blue letters indicate specific points of importance for the energy-yielding metabolism of select pathogens listed as follows (see Table 1 for summary): Pathogenic streptococci (, , ); serovar Typhimurium; ; ; ; Enterohemorrhagic ; ; .

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0027-2015
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FIGURE 2

Graphical summary of bacterial mechanisms used to release intracellular host nutrients. Pathogenic bacteria perturb host cell functions to provide resources for survival and replication. Abbreviations: GSH, glutathione; GGT, γ-glutamyl transpeptidase; LCV, -containing vacuole; ER, endoplasmic reticulum; AA, amino acids; CERT, ceramide transfer protein; SM, sphingomyelin.

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FIGURE 2

Graphical summary of bacterial mechanisms used to release intracellular host nutrients. Pathogenic bacteria perturb host cell functions to provide resources for survival and replication. Abbreviations: GSH, glutathione; GGT, γ-glutamyl transpeptidase; LCV, -containing vacuole; ER, endoplasmic reticulum; AA, amino acids; CERT, ceramide transfer protein; SM, sphingomyelin.

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0027-2015
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Tables

Bacterial Metabolism Shapes the Host–Pathogen Interface
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Citation: Passalacqua K, Charbonneau M, O’Riordan M. 2016. Bacterial metabolism shapes the host–pathogen interface. microbiolspec 4(3): doi:10.1128/microbiolspec.VMBF-0027-2015
/content/microbiolspec/10.1128/microbiolspec.VMBF-0027-2015.T1
TABLE 1

Summary points of energy-yielding metabolism for select pathogenic bacteria

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TABLE 1

Summary points of energy-yielding metabolism for select pathogenic bacteria

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0027-2015
/content/microbiolspec/10.1128/microbiolspec.VMBF-0027-2015.T2
TABLE 2

Summary of bacterial mechanisms for metal ion acquisition

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TABLE 2

Summary of bacterial mechanisms for metal ion acquisition

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0027-2015

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