1887

Abstract

Bacterial nutrition is a fundamental aspect of pathogenesis. While the host environment is in principle nutrient-rich, hosts have evolved strategies to interfere with nutrient acquisition by pathogens. In turn, pathogens have developed mechanisms to circumvent these restrictions. Changing the availability of bioavailable metal ions is a common strategy used by hosts to limit bacterial replication. Macrophages and neutrophils withhold iron, manganese, and zinc ions to starve bacteria. Alternatively, they can release manganese, zinc, and copper ions to intoxicate microorganisms. Metals are essential micronutrients and participate in catalysis, macromolecular structure, and signalling. This review summarises our current understanding of how central carbon metabolism in pathogens adapts to local fluctuations in free metal ion concentrations. We focus on the transcriptomics and proteomics data produced in studies of the iron-sparing response in , the etiological agent of tuberculosis, and consequently generate a hypothetical model linking trehalose accumulation, succinate secretion and substrate-level phosphorylation in iron-starved . This review also aims to highlight a large gap in our knowledge of pathogen physiology: the interplay between metal homeostasis and central carbon metabolism, two cellular processes which are usually studied separately. Integrating metabolism and metal biology would allow the discovery of new weaknesses in bacterial physiology, leading to the development of novel and improved antibacterial therapies.

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2021-06-03
2024-04-25
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References

  1. Kramer J, Ö Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol 2020; 18:152–163 [View Article]
    [Google Scholar]
  2. O’Halloran TV. Transition metals in control of gene expression. Science 1993; 261:715–725 [View Article][PubMed]
    [Google Scholar]
  3. Maciag A, Dainese E, Rodriguez GM, Milano A, Provvedi R et al. Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J Bacteriol 2007; 189:730–740 [View Article][PubMed]
    [Google Scholar]
  4. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, ideR SI. An essential gene in mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 2002; 70:3371–3381
    [Google Scholar]
  5. Lisher JP, Higgins KA, Maroney MJ, Giedroc DP. Physical characterization of the manganese-sensing pneumococcal surface antigen repressor from Streptococcus pneumoniae . Biochemistry 2013; 52:7689–7701 [View Article][PubMed]
    [Google Scholar]
  6. Stapleton B, Walker LR, Logan TM. Zn(II) stimulation of Fe(II)-activated repression in the iron-dependent repressor from Mycobacterium tuberculosis . Biochemistry 2013; 52:1927–1938 [View Article][PubMed]
    [Google Scholar]
  7. Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 2012; 10:525–537 [View Article][PubMed]
    [Google Scholar]
  8. Neyrolles O, Wolschendorf F, Mitra A, Niederweis M. Mycobacteria, metals, and the macrophage. Immunol Rev 2015; 264:249–263 [View Article][PubMed]
    [Google Scholar]
  9. Sheldon JR, Skaar EP. Metals as phagocyte antimicrobial effectors. Curr Opin Immunol 2019; 60:1–9 [View Article][PubMed]
    [Google Scholar]
  10. Soldati T, Neyrolles O. Mycobacteria and the intraphagosomal environment: take it with a pinch of salt(s)!. Traffic 2012; 13:1042–1052 [View Article][PubMed]
    [Google Scholar]
  11. Kehl-Fie TE, Chitayat S, Hood MI, Damo S, Restrepo N et al. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus . Cell Host Microbe 2011; 10:158–164 [View Article][PubMed]
    [Google Scholar]
  12. Nairz M, Weiss G. Iron in infection and immunity. Mol Aspects Med 2020; 75:100864 [View Article][PubMed]
    [Google Scholar]
  13. Wessling-Resnick M. Nramp1 and other transporters involved in metal withholding during infection. J Biol Chem 2015; 290:18984–18990 [View Article][PubMed]
    [Google Scholar]
  14. Cellier MF. Nramp: from sequence to structure and mechanism of divalent metal import. Curr Top Membr 2012; 69:249–293 [View Article][PubMed]
    [Google Scholar]
  15. Cellier MF. Nutritional immunity: homology modeling of Nramp metal import. Adv Exp Med Biol 2012; 946:335–351 [View Article][PubMed]
    [Google Scholar]
  16. Stafford SL, Bokil NJ, Achard ME, Kapetanovic R, Schembri MA et al. Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci Rep 2013; 33: [View Article][PubMed]
    [Google Scholar]
  17. Arnold FM, Weber MS, Gonda I, Gallenito MJ, Adenau S et al. The ABC exporter IrtAB imports and reduces mycobacterial siderophores. Nature 2020; 580:413–417 [View Article][PubMed]
    [Google Scholar]
  18. Tanaka KJ, Song S, Mason K, Pinkett HW. Selective substrate uptake: The role of ATP-binding cassette (ABC) importers in pathogenesis. Biochim Biophys Acta Biomembr 2018; 1860:868–877 [View Article][PubMed]
    [Google Scholar]
  19. Neyrolles O, Mintz E, Catty P. Zinc and copper toxicity in host defense against pathogens: Mycobacterium tuberculosis as a model example of an emerging paradigm. Front Cell Infect Microbiol 2013; 3:89 [View Article][PubMed]
    [Google Scholar]
  20. Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 2011; 10:248–259 [View Article][PubMed]
    [Google Scholar]
  21. Argüello JM, González-Guerrero M, Raimunda D. Bacterial transition metal P(1B)-ATPases: transport mechanism and roles in virulence. Biochemistry 2011; 50:9940–9949 [View Article][PubMed]
    [Google Scholar]
  22. León-Torres A, Arango E, Castillo E, Soto CY. CtpB is a plasma membrane copper (I) transporting P-type ATPase of Mycobacterium tuberculosis . . Biol Res 2020; 53:66 [View Article][PubMed]
    [Google Scholar]
  23. Troxell B, Hassan HM. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 2013; 3:59 [View Article][PubMed]
    [Google Scholar]
  24. Volz K: The functional duality of iron regulatory protein 1. Curr Opin Struct Biol 2008 18 106–111 [View Article][PubMed]
    [Google Scholar]
  25. Lushchak OV, Piroddi M, Galli F, Lushchak VI. Aconitase post-translational modification as a key in linkage between Krebs cycle, iron homeostasis, redox signaling, and metabolism of reactive oxygen species. Redox Rep 2014; 19:8–15 [View Article][PubMed]
    [Google Scholar]
  26. Serafini A, Pisu D, Palù G, Rodriguez GM, Manganelli R. The ESX-3 secretion system is necessary for iron and zinc homeostasis in mycobacterium tuberculosis. PLoS One 2013; 8:e78351 [View Article]
    [Google Scholar]
  27. Kurthkoti K, Amin H, Marakalala MJ, Ghanny S, Subbian S et al. The capacity of Mycobacterium tuberculosis to survive iron starvation might enable it to persist in iron-deprived microenvironments of human granulomas. mBio 2017; 8: [View Article][PubMed]
    [Google Scholar]
  28. Wong DK, Lee BY, Horwitz MA, Gibson BW. Identification of fur, aconitase, and other proteins expressed by Mycobacterium tuberculosis under conditions of low and high concentrations of iron by combined two-dimensional gel electrophoresis and mass spectrometry. Infect Immun 1999; 67:327–336 [View Article][PubMed]
    [Google Scholar]
  29. Zhang L, Hendrickson RC, Meikle V, Lefkowitz EJ, Ioerger TR et al. Comprehensive analysis of iron utilization by mycobacterium tuberculosis. PLoS Pathog 2020; 16:e1008337 [View Article][PubMed]
    [Google Scholar]
  30. Janagama HK, Senthilkumar BJ, Kugadas A, Jagtap P, Higgins L. Iron-sparing response of Mycobacterium avium subsp. paratuberculosis is strain dependent. BMC Microbiol 2010; 10:268 [View Article][PubMed]
    [Google Scholar]
  31. Yellaboina S, Ranjan S, Vindal V, Ranjan A. Comparative analysis of iron regulated genes in mycobacteria. FEBS Lett 2006; 580:2567–2576 [View Article][PubMed]
    [Google Scholar]
  32. Stokas H, Rhodes HL, Purdy GE. Modulation of the M. tuberculosis cell envelope between replicating and non-replicating persistent bacteria. Tuberculosis (Edinb) 2020; 125:102007 [View Article][PubMed]
    [Google Scholar]
  33. Lapp D, Elbein AD. Purification and properties of the adenosine diphosphate-glucose and uridine diphosphate-glucose pyrophosphorylases of Mycobacterium smegmatis: inhibition and activation of the adenosine diphosphate-glucose pyrophosphorylase. J Bacteriol 1972; 112:327–336 [View Article][PubMed]
    [Google Scholar]
  34. Mikkola S. Nucleotide sugars in chemistry and biology. Molecules 2020; 25:23 [View Article]
    [Google Scholar]
  35. Singh P, Rameshwaram NR, Ghosh S, Mukhopadhyay S. Cell envelope lipids in the pathophysiology of Mycobacterium tuberculosis . Future Microbiol 2018; 13:689–710 [View Article][PubMed]
    [Google Scholar]
  36. Huber A, Killy B, Grummel N, Bodendorfer B, Paul S et al. Mycobacterial cord factor reprograms the macrophage response to IFN-γ towards enhanced inflammation yet impaired antigen presentation and expression of GBP1. J Immunol 2020; 205:1580–1592 [View Article][PubMed]
    [Google Scholar]
  37. Chandra G, Chater KF, Bornemann S. Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology (Reading) 2011; 157:1565–1572 [View Article][PubMed]
    [Google Scholar]
  38. Pan YT, Drake RR, Elbein AD. Trehalose-P synthase of mycobacteria: its substrate specificity is affected by polyanions. Glycobiology 1996; 6:453–461 [View Article][PubMed]
    [Google Scholar]
  39. Pan YT, Carroll JD, Elbein AD. Trehalose-phosphate synthase of Mycobacterium tuberculosis. Cloning, expression and properties of the recombinant enzyme. Eur J Biochem 2002; 269:6091–6100 [View Article][PubMed]
    [Google Scholar]
  40. Kalscheuer R, Koliwer-Brandl H. Genetics of mycobacterial trehalose metabolism. Microbiol Spectr 2014; 2: [View Article][PubMed]
    [Google Scholar]
  41. Shleeva MO, Trutneva KA, Demina GR, Zinin AI, Sorokoumova GM et al. Free Trehalose Accumulation in Dormant Mycobacterium smegmatis Cells and Its Breakdown in Early Resuscitation Phase. Front Microbiol 2017; 8:524
    [Google Scholar]
  42. Miah F, Koliwer-Brandl H, Rejzek M, Field RA, Kalscheuer R et al. Flux through trehalose synthase flows from trehalose to the alpha anomer of maltose in mycobacteria. Chem Biol 2013; 20:487–493 [View Article][PubMed]
    [Google Scholar]
  43. Eoh H, Wang Z, Layre E, Rath P, Morris R et al. Metabolic anticipation in Mycobacterium tuberculosis . Nat Microbiol 2017; 2:17084 [View Article][PubMed]
    [Google Scholar]
  44. Lee JJ, Lee SK, Song N, Nathan TO, Swarts BM et al. Transient drug-tolerance and permanent drug-resistance rely on the trehalose-catalytic shift in Mycobacterium tuberculosis . Nat Commun 2019; 10:2928
    [Google Scholar]
  45. Pohane AA, Carr CR, Garhyan J, Swarts BM, Siegrist MS. Trehalose recycling promotes energy-efficient biosynthesis of the mycobacterial cell envelope. mBio 2021; 12: [View Article][PubMed]
    [Google Scholar]
  46. Vanaporn M, Titball RW. Trehalose and bacterial virulence. Virulence 2020; 11:1192–1202 [View Article][PubMed]
    [Google Scholar]
  47. Harland CW, Rabuka D, Bertozzi CR, Parthasarathy R. The Mycobacterium tuberculosis virulence factor trehalose dimycolate imparts desiccation resistance to model mycobacterial membranes. Biophys J 2008; 94:4718–4724 [View Article][PubMed]
    [Google Scholar]
  48. Woodruff PJ, Carlson BL, Siridechadilok B, Pratt MR, Senaratne RH et al. Trehalose is required for growth of Mycobacterium smegmatis . J Biol Chem 2004; 279:28835–28843 [View Article][PubMed]
    [Google Scholar]
  49. Allison SD, Chang B, Randolph TW, Carpenter JF. Hydrogen bonding between sugar and protein is responsible for inhibition of dehydration-induced protein unfolding. Arch Biochem Biophys 1999; 365:289–298 [View Article][PubMed]
    [Google Scholar]
  50. Banerjee S, Nandyala AK, Raviprasad P, Ahmed N, Hasnain SE. Iron-dependent RNA-binding activity of Mycobacterium tuberculosis aconitase. J Bacteriol 2007; 189:4046–4052 [View Article][PubMed]
    [Google Scholar]
  51. Balakrishnan K, Mohareer K, Banerjee S. Mycobacterium tuberculosis Rv1474c is a TetR-like transcriptional repressor that regulates aconitase, an essential enzyme and RNA-binding protein, in an iron-responsive manner. Tuberculosis (Edinb) 2017; 103:71–82 [View Article][PubMed]
    [Google Scholar]
  52. Machová I, Snašel J, Zimmermann M, Laubitz D, Plocinski P et al. Mycobacterium tuberculosis phosphoenolpyruvate carboxykinase is regulated by redox mechanisms and interaction with thioredoxin. J Biol Chem 2014; 289:13066–13078 [View Article][PubMed]
    [Google Scholar]
  53. Marrero J, Rhee KY, Schnappinger D, Pethe K, Ehrt S. Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc Natl Acad Sci U S A 2010; 107:9819–9824 [View Article][PubMed]
    [Google Scholar]
  54. Basu P, Sandhu N, Bhatt A, Singh A, Balhana R et al. The anaplerotic node is essential for the intracellular survival of Mycobacterium tuberculosis. J Biol Chem 2018; 293:5695–5704 [View Article][PubMed]
    [Google Scholar]
  55. Bancroft PJ, Turapov O, Jagatia H, Arnvig KB, Mukamolova GV et al. Coupling of peptidoglycan synthesis to central metabolism in mycobacteria: Post-transcriptional control of CWLM by aconitase. Cell Rep 2020; 32:108209 [View Article][PubMed]
    [Google Scholar]
  56. Cortes T, Schubert OT, Rose G, Arnvig KB, Comas I et al. Genome-wide mapping of transcriptional start sites defines an extensive leaderless transcriptome in Mycobacterium tuberculosis . Cell Rep 2013; 5:1121–1131 [View Article][PubMed]
    [Google Scholar]
  57. Arnvig KB, Pennell S, Gopal B, Colston MJ. A high-affinity interaction between NusA and the rrn nut site in Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 2004; 101:8325–8330 [View Article][PubMed]
    [Google Scholar]
  58. Beste DJV, Bonde B, Hawkins N, Ward JL, Beale MH et al. 1 3 C metabolic flux analysis identifies an unusual route for pyruvate dissimilation in mycobacteria which requires isocitrate lyase and carbon dioxide fixation. PLoS Pathog 2011; 7:e1002091 [View Article][PubMed]
    [Google Scholar]
  59. Folsom JP, Parker AE, Carlson RP. Physiological and proteomic analysis of Escherichia coli iron-limited chemostat growth. J Bacteriol 2014; 196:2748–2761 [View Article][PubMed]
    [Google Scholar]
  60. Machová I, Snášel J, Dostál J, Brynda J, Fanfrlík J et al. Structural and functional studies of phosphoenolpyruvate carboxykinase from mycobacterium tuberculosis. PLoS One 2015; 10:e0120682 [View Article][PubMed]
    [Google Scholar]
  61. Höner Zu Bentrup K, Miczak A, Swenson DL, Russell DG. Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis . J Bacteriol 1999; 181:7161–7167 [View Article][PubMed]
    [Google Scholar]
  62. Rao SP, Alonso S, Rand L, Dick T, Pethe K. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 2008; 105:11945–11950 [View Article][PubMed]
    [Google Scholar]
  63. Eoh H, Rhee KY. Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis . Proc Natl Acad Sci U S A 2013; 110:6554–6559 [View Article][PubMed]
    [Google Scholar]
  64. Baughn AD, Garforth SJ, Vilchèze C, Jacobs WR. An anaerobic-type alpha-ketoglutarate ferredoxin oxidoreductase completes the oxidative tricarboxylic acid cycle of mycobacterium tuberculosis. PLoS Pathog 2009; 5:11–e1000662
    [Google Scholar]
  65. Agapova A, Serafini A, Petridis M, Hunt DM, Garza-Garcia A et al. Flexible nitrogen utilisation by the metabolic generalist pathogen. Elife 2019; 8: [View Article][PubMed]
    [Google Scholar]
  66. Serafini A, Tan L, Horswell S, Howell S, Greenwood DJ et al. Mycobacterium tuberculosis requires glyoxylate shunt and reverse methylcitrate cycle for lactate and pyruvate metabolism. Mol Microbiol 2019; 112:1284–1307 [View Article][PubMed]
    [Google Scholar]
  67. de Carvalho LP, Fischer SM, Marrero J, Nathan C, Ehrt S et al. Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 2010; 17:1122–1131 [View Article][PubMed]
    [Google Scholar]
  68. Gutka HJ, Wang Y, Franzblau SG, Movahedzadeh F. Glpx gene in mycobacterium tuberculosis is required for in vitro gluconeogenic growth and in vivo survival. PLoS One 2015; 10:e0138436 [View Article]
    [Google Scholar]
  69. Ganapathy U, Marrero J, Calhoun S, Eoh H, de Carvalho LPS et al. Two enzymes with redundant fructose bisphosphatase activity sustain gluconeogenesis and virulence in Mycobacterium tuberculosis . Nat Commun 2015; 6:7912 [View Article][PubMed]
    [Google Scholar]
  70. Phong WY, Lin W, Rao SPS, Dick T, Alonso S et al. Characterization of phosphofructokinase activity in mycobacterium tuberculosis reveals that a functional glycolytic carbon flow is necessary to limit the accumulation of toxic metabolic intermediates under hypoxia. PLoS One 2013; 8:e56037 [View Article][PubMed]
    [Google Scholar]
  71. Alén C, Sonenshein AL. Bacillus subtilis aconitase is an RNA-binding protein. Proc Natl Acad Sci U S A 1999; 96:10412–10417 [View Article][PubMed]
    [Google Scholar]
  72. Pechter KB, Meyer FM, Serio AW, Stülke J, Sonenshein AL. Two roles for aconitase in the regulation of tricarboxylic acid branch gene expression in Bacillus subtilis . J Bacteriol 2013; 195:1525–1537 [View Article][PubMed]
    [Google Scholar]
  73. Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB et al. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 2008; 105:11927–11932 [View Article][PubMed]
    [Google Scholar]
  74. Smaldone GT, Revelles O, Gaballa A, Sauer U, Antelmann H et al. A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism. J Bacteriol 2012; 194:2594–2605 [View Article][PubMed]
    [Google Scholar]
  75. Fischer E, Sauer U. Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat Genet 2005; 37:636–640 [View Article][PubMed]
    [Google Scholar]
  76. Jordan PA, Tang Y, Bradbury AJ, Thomson AJ, Guest JR. Biochemical and spectroscopic characterization of Escherichia coli aconitases (AcnA and AcnB. Biochem J 1999; 344:739–746 [View Article]
    [Google Scholar]
  77. Tang Y, Guest JR. Direct evidence for mRNA binding and post-transcriptional regulation by Escherichia coli aconitases. Microbiology (Reading 1999; 145:3069–3079 [View Article]
    [Google Scholar]
  78. Benjamin JA, Massé E. The iron-sensing aconitase B binds its own mRNA to prevent sRNA-induced mRNA cleavage. Nucleic Acids Res 2014; 42:10023–10036 [View Article][PubMed]
    [Google Scholar]
  79. Tang Y, Guest JR, Artymiuk PJ, Green J. Switching aconitase B between catalytic and regulatory modes involves iron-dependent dimer formation. Mol Microbiol 2005; 56:1149–1158 [View Article][PubMed]
    [Google Scholar]
  80. Seo SW, Kim D, Latif H, O’Brien EJ, Szubin R et al. Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli. Nat Commun 2014; 5:4910 [View Article][PubMed]
    [Google Scholar]
  81. Himpsl SD, Shea AE, Zora J, Stocki JA, Foreman D et al. The oxidative fumarase Fumc is a key contributor for E. coli fitness under iron-limitation and during UTI. PLoS Pathog 2020; 16:e1008382 [View Article][PubMed]
    [Google Scholar]
  82. McHugh JP, Rodríguez-Quinoñes F, Abdul-Tehrani H, Svistunenko DA, Poole RK et al. Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 2003; 278:29478–29486 [View Article][PubMed]
    [Google Scholar]
  83. Gruer MJ, Guest JR. Two genetically-distinct and differentially-regulated aconitases (AcnA and AcnB) in Escherichia coli . Microbiology 1994; 140:2531–2541 [View Article]
    [Google Scholar]
  84. Cunningham L, Gruer MJ, Guest JR. Transcriptional regulation of the aconitase genes (acnA and acnB) of Escherichia coli . Microbiology 1997; 143:3795–3805 [View Article]
    [Google Scholar]
  85. Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ et al. Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2006; 2:e87 [View Article][PubMed]
    [Google Scholar]
  86. Ha S, Shin B, Park W. Lack of glyoxylate shunt dysregulates iron homeostasis in pseudomonas aeruginosa. Microbiology (Reading) 2018; 164:587–599 [View Article][PubMed]
    [Google Scholar]
  87. Middaugh J, Hamel R, Jean-Baptiste G, Beriault R, Chenier D et al. Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase: a metabolic network mediating cellular survival. J Biol Chem 2005; 280:3159–3165 [View Article][PubMed]
    [Google Scholar]
  88. Sazanov LA, Jackson JB. Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett 1994; 344:109–116 [View Article][PubMed]
    [Google Scholar]
  89. Taymaz-Nikerel H, De Mey M, Baart GJ, Maertens J, Foulquié-Moreno MR et al. Comparative fluxome and metabolome analysis for overproduction of succinate in Escherichia coli . Biotechnol Bioeng 2016; 113:817–829 [View Article][PubMed]
    [Google Scholar]
  90. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE et al. Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis . PLoS Pathog 2011; 7:e1002287 [View Article][PubMed]
    [Google Scholar]
  91. Babor M, Gerzon S, Raveh B, Sobolev V, Edelman M. Prediction of transition metal-binding sites from apo protein structures. Proteins 2008; 70:208–217 [View Article][PubMed]
    [Google Scholar]
  92. Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S et al. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci U S A 2013; 110:3841–3846 [View Article][PubMed]
    [Google Scholar]
  93. Zygiel EM, Nolan EM. Transition metal Sequestration by the host-defense protein calprotectin. Annu Rev Biochem 2018; 87:621–643 [View Article][PubMed]
    [Google Scholar]
  94. Libardo MDJ, de la Fuente-Nuñez C, Anand K, Krishnamoorthy G, Kaiser P et al. Phagosomal copper-promoted oxidative attack on intracellular Mycobacterium tuberculosis . ACS Infect Dis 2018; 4:1623–1634 [View Article][PubMed]
    [Google Scholar]
  95. Barwinska-Sendra A, Waldron KJ. The role of intermetal competition and mis-metalation in metal toxicity. Adv Microb Physiol 2017; 70:315–379 [View Article][PubMed]
    [Google Scholar]
  96. Volentini SI, Farías RN, Rodríguez-Montelongo L, Rapisarda VA. Cu(II)-reduction by Escherichia coli cells is dependent on respiratory chain components. Biometals 2011; 24:827–835 [View Article][PubMed]
    [Google Scholar]
  97. Abicht HK, Gonskikh Y, Gerber SD, Solioz M. Non-enzymic copper reduction by menaquinone enhances copper toxicity in Lactococcus lactis il1403. Microbiology (Reading) 2013; 159:1190–1197 [View Article][PubMed]
    [Google Scholar]
  98. Andrei A, Öztürk Y, Khalfaoui-Hassani B, Rauch J, Marckmann D et al. Cu homeostasis in bacteria: The ins and outs. Membranes (Basel) 2020; 10: [View Article][PubMed]
    [Google Scholar]
  99. Pandey R, Russo R, Ghanny S, Huang X, Helmann J et al. MntR(Rv2788): a transcriptional regulator that controls manganese homeostasis in Mycobacterium tuberculosis . . Mol Microbiol 2015; 98:1168–1183 [View Article][PubMed]
    [Google Scholar]
  100. Halsey CR, Lei S, Wax JK, Lehman MK, Nuxoll AS et al. Amino acid catabolism in Staphylococcus aureus and the function of carbon catabolite repression. mBio 2017; 8: [View Article][PubMed]
    [Google Scholar]
  101. Radin JN, Kelliher JL, Solórzano PKP, Grim KP, Ramezanifard R et al. Metal-independent variants of phosphoglycerate mutase promote resistance to nutritional immunity and retention of glycolysis during infection. PLoS Pathog 2019; 15:e1007971 [View Article][PubMed]
    [Google Scholar]
  102. Radin JN, Kelliher JL, Párraga Solórzano PK, Kehl-Fie TE. The two-component system arlrs and alterations in metabolism enable Staphylococcus aureus to resist calprotectin-induced manganese starvation. PLoS Pathog 2016; 12:e1006040 [View Article]
    [Google Scholar]
  103. Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY et al. RegPrecise 3.0--a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genomics 2013; 14:745 [View Article][PubMed]
    [Google Scholar]
  104. Tarrant E, Riboldi G P, McIlvin MR, Stevenson J, Barwinska-Sendra A et al. Copper stress in Staphylococcus aureus leads to adaptive changes in central carbon metabolism. Metallomics 2019; 11:183–200 [View Article]
    [Google Scholar]
  105. Purves J, Cockayne A, Moody PC, Morrissey JA. Comparison of the regulation, metabolic functions, and roles in virulence of the glyceraldehyde-3-phosphate dehydrogenase homologues gapA and gapB in Staphylococcus aureus . Infect Immun 2010; 78:5223–5232 [View Article][PubMed]
    [Google Scholar]
  106. Liu Y, Zhang Q, Hu M, Yu K, Fu J et al. Proteomic analyses of intracellular Salmonella enterica serovar typhimurium reveal extensive bacterial adaptations to infected host epithelial cells. Infect Immun 2015; 83:2897–2906 [View Article][PubMed]
    [Google Scholar]
  107. Zalewski PD, Truong-Tran AQ, Grosser D, Jayaram L, Murgia C et al. Zinc metabolism in airway epithelium and airway inflammation: basic mechanisms and clinical targets. Pharmacol Ther 2005; 105:127–149 [View Article][PubMed]
    [Google Scholar]
  108. Ong CL, Walker MJ, McEwan AG. Zinc disrupts central carbon metabolism and capsule biosynthesis in Streptococcus pyogenes . Sci Rep 2015; 5:10799 [View Article][PubMed]
    [Google Scholar]
  109. Blanchette KA, Shenoy AT, Milner J, Gilley RP, McClure E et al. Neuraminidase A-Exposed galactose promotes Streptococcus pneumoniae biofilm formation during colonization. Infect Immun 2016; 84:2922–2932 [View Article][PubMed]
    [Google Scholar]
  110. Toulouse C, Metesch K, Pfannstiel J, Steuber J. Metabolic reprogramming of vibrio cholerae impaired in respiratory NADH Oxidation is accompanied by increased copper sensitivity. J Bacteriol 2018; 200:15
    [Google Scholar]
  111. Agarwal S, Bernt M, Toulouse C, Kurz H, Pfannstiel J et al. Impact of Na +-Translocating NADH:Quinone Oxidoreductase on Iron Uptake and nqrM Expression in Vibrio cholerae. J Bacteriol 2020; 202:
    [Google Scholar]
  112. Steuber J, Halang P, Vorburger T, Steffen W, Vohl G et al. Central role of the Na(+)-translocating NADH:quinone oxidoreductase (Na(+)-NQR) in sodium bioenergetics of Vibrio cholerae . Biol Chem 2014; 395:1389–1399 [View Article][PubMed]
    [Google Scholar]
  113. Peng ED, Payne SM. Vibrio cholerae VciB Mediates Iron Reduction. J Bacteriol 2017; 199:12
    [Google Scholar]
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