Metabolic defence against oxidative stress: the road less travelled so far

Journal of Applied Microbiology

Volumn 123, Issue 4, 2017, Pages 798-809

  Lemire, J ^a   Alhasawi, A ^b   Appanna, V P ^b   Tharmalingam, S ^b   Appanna, V D ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b LAURENTIAN UNIVERSITY   (Canada)

Author keywords

ketoacids; metabolism; oxidative stress; reactive oxygen species; signalling

Indexed keywords

BACTERIA; CARBOXYLATION; DETOXIFICATION; METABOLITES; OXIDATIVE STRESS; OXYGEN; PHYSIOLOGY; REDOX REACTIONS; SUPEROXIDE DISMUTASE;

ALKYL HYDROPEROXIDE; CHALCOGENS; CYCLING SYSTEMS; GLUCOSE-6-PHOSPHATE DEHYDROGENASE; GLUTHATHIONE; KETOACIDS; METABOLIC ENZYMES; REACTIVE OXYGEN SPECIES; SUPER OXIDE DISMUTASE; SUPEROXIDE DISMUTASES;

METABOLISM;

ANTIOXIDANT; CARBOXYLIC ACID; ENZYME; OXIDIZING AGENT; OXOACID; REACTIVE OXYGEN METABOLITE; SCAVENGER; BACTERIAL PROTEIN; CATALASE; GLUTATHIONE; SUPEROXIDE DISMUTASE;

BACTERIUM; DECARBOXYLATION; DETOXIFICATION; ENZYME ACTIVITY; METABOLISM; METABOLITE; ORGANIC COMPOUND; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

BACTERIAL CELL; BACTERIAL METABOLISM; CELL METABOLISM; DECARBOXYLATION; DEFENSE MECHANISM; DETOXIFICATION; HUMAN; METABOLIC REGULATION; METABOLISM; METABOLITE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; BACTERIUM; ENZYMOLOGY; GENETICS;

ANTIOXIDANTS; BACTERIA; BACTERIAL PROTEINS; CATALASE; GLUTATHIONE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 85029591389     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13509     Document Type: Review

References (88)

1. Aertsen, A., De Spiegeleer, P., Vanoirbeek, K., Lavilla, M. and Michiels, C.W. (2005) Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl Environ Microbiol 71, 2226–2231.
2. Aldarini, N., Alhasawi, A.A., Thomas, S.C. and Appanna, V.D. (2017) The role of glutamine synthetase in energy production and glutamine metabolism during oxidative stress. Antonie Van Leeuwenhoek 110, 629–639.
3. Alhasawi, A., Castonguay, Z., Appanna, N.D., Auger, C. and Appanna, V.D. (2015a) Glycine metabolism and anti-oxidative defence mechanisms in Pseudomonas fluorescens. Microbiol Res 171, 26–31.
4. Alhasawi, A., Leblanc, M., Appanna, N.D., Auger, C. and Appanna, V.D. (2015b) Aspartate metabolism and pyruvate homeostasis triggered by oxidative stress in Pseudomonas fluorescens: a functional metabolomic study. Metabolomics 11, 1792–1801.
5. Alhasawi, A., Thomas, S.C. and Appanna, V.D. (2016) Metabolic networks to generate pyruvate, PEP and ATP from glycerol in Pseudomonas fluorescens. Enzyme Microb Technol 85, 51–56.
6. Ambrus, A., Nemeria, N.S., Torocsik, B., Tretter, L., Nilsson, M., Jordan, F. and Adam-Vizi, V. (2015) Formation of reactive oxygen species by human and bacterial pyruvate and 2-oxoglutarate dehydrogenase multienzyme complexes reconstituted from recombinant components. Free Radic Biol Med 89, 642–650.
7. Appanna, V.P., Auger, C., Thomas, S.C. and Omri, A. (2014) Fumarate metabolism and ATP production in Pseudomonas fluorescens exposed to nitrosative stress. Antonie Van Leeuwenhoek 106, 431–438.
8. Appanna, V.P., Alhasawi, A.A., Auger, C., Thomas, S.C. and Appanna, V.D. (2016) Phospho-transfer networks and ATP homeostasis in response to an ineffective electron transport chain in Pseudomonas fluorescens. Arch Biochem Biophys 606, 26–33.
9. Arenas, F.A., Covarrubias, P.C., Sandoval, J.M., Perez-Donoso, J.M., Imlay, J.A. and Vasquez, C.C. (2011) The Escherichia coli BtuE protein functions as a resistance determinant against reactive oxygen species. PLoS ONE 6, e15979.
10. Auger, C., Lemire, L., Appanna, V.P. and Appanna, V.D. (2013) Gallium in bacteria: metabolic and medical implications. In Encyclopedia of Metalloproteins eds. Kretsinger, R.H., Uversky, V.N. and Permyakov, E.A. pp. 800–807. New York: Springer.
11. Auger, C., Appanna, N.D. and Appanna, V.D. (2016) Metabolic networks to counter aluminum toxicity in Pseudomonas fluorescens: A holistic View in Stress and Environmental Regulation of Gene expression and Adaptation in Bacteria, ed. de Bruijn, F.J., Chapter 20, pp. 1–38. Hoboken, New Jersey: Wiley-Blackwell Publishers.
12. Baumler, A.J. and Sperandio, V. (2016) Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535, 85–93.
13. Bielski, B.H., Arudi, R.L. and Sutherland, M.W. (1983) A study of the reactivity of HO2/O2- with unsaturated fatty acids. J Biol Chem 258, 4759–4761.
14. Bignucolo, A., Appanna, V.P., Thomas, S.C., Auger, C., Han, S., Omri, A. and Appanna, V.D. (2013) Hydrogen peroxide stress provokes a metabolic reprogramming in Pseudomonas fluorescens: enhanced production of pyruvate. J Biotechnol 167, 309–315.
15. Bloes, D.A., Kretschmer, D. and Peschel, A. (2015) Enemy attraction: bacterial agonists for leukocyte chemotaxis receptors. Nat Rev Microbiol 13, 95–104.
16. Bunton, C.A. (1949) Oxidation of α-diketones and α-keto-acids by hydrogen peroxide. Nature 163, 444–444.
17. Cabiscol, E., Tamarit, J. and Ros, J. (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microb 3, 3–8.
18. Carlioz, A. and Touati, D. (1986) Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5, 623–630.
19. Carmel-Harel, O. and Storz, G. (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54, 439–461.
20. Chavez, F.P., Lunsdorf, H. and Jerez, C.A. (2004) Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chlorobiphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. Appl Environ Microbiol 70, 3064–3072.
21. Chen, Y., Gozzi, K., Yan, F. and Chai, Y. (2015) Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation. mBio 6, e00392–15.
22. Chenier, D., Beriault, R., Mailloux, R., Baquie, M., Abramia, G., Lemire, J. and Appanna, V. (2008) Involvement of fumarase C and NADH oxidase in metabolic adaptation of Pseudomonas fluorescens cells evoked by aluminum and gallium toxicity. Appl Environ Microbiol 74, 3977–3984.
23. Demple, B. (1991) Regulation of bacterial oxidative stress genes. Annu Rev Genet 25, 315–337.
24. Ferreyra, J.A., Wu, K.J., Hryckowian, A.J., Bouley, D.M., Weimer, B.C. and Sonnenburg, J.L. (2014) Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe 16, 770–777.
25. Flint, D.H., Tuminello, J.F. and Emptage, M.H. (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268, 22369–22376.
26. Frey, H.E. and Pollard, E.C. (1966) Ionizing radiation and bacteria: nature of the effect of irradiated medium. Radiat Res 28, 668–676.
27. Fukuzaki, S. (2006) Mechanisms of actions of sodium hypochlorite in cleaning and disinfection processes. Biocontrol Sci 11, 147–157.
28. Gonzalez-Flecha, B. and Demple, B. (1995) Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270, 13681–13687.
29. Gonzalez-Flecha, B. and Demple, B. (1997) Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J Bacteriol 179, 382–388.
30. Görke, B. and Stülke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6, 613–624.
31. Gort, A.S., Ferber, D.M. and Imlay, J.A. (1999) The regulation and role of the periplasmic copper, zinc superoxide dismutase of Escherichia coli. Mol Microbiol 32, 179–191.
32. Haritos, V.S. and Dojchinov, G. (2003) Cytochrome c oxidase inhibition in the rice weevil Sitophilus oryzae (L.) by formate, the toxic metabolite of volatile alkyl formates. Comp Biochem Physiol C Toxicol Pharmacol 136, 135–143.
33. Hawkins, C.L. and Davies, M.J. (2001) Generation and propagation of radical reactions on proteins. Biochim Biophys Acta 1504, 196–219.
34. Helmann, J.D., Wu, M.F., Gaballa, A., Kobel, P.A., Morshedi, M.M., Fawcett, P. and Paddon, C. (2003) The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J Bacteriol 185, 243–253.
35. Hirst, J., King, M.S. and Pryde, K.R. (2008) The production of reactive oxygen species by complex I. Biochem Soc Trans 36, 976–980.
36. Hogg, S. (2005) Essential Microbiology. West Sussex; Hoboken, NJ: John Wiley and Sons.
37. Hondorp, E.R. and Matthews, R.G. (2004) Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol 2, e336.
38. Imlay, J.A. (2003) Pathways of oxidative damage. Annu Rev Microbiol 57, 395–418.
39. Imlay, J.A. (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11, 443–454.
40. Imlay, J.A. (2015) Diagnosing oxidative stress in bacteria: not as easy as you might think. Curr Opin Microbiol 24, 124–131.
41. Imlay, J.A. and Fridovich, I. (1991) Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266, 6957–6965.
42. Jenney, F.E., Verhagen, M.F.J.M., Cui, X. and Adams, M.W.W. (1999) Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306–309.
43. Jin, W. and Wu, F. (2016) Proteome-wide identification of lysine succinylation in the proteins of tomato (Solanum lycopersicum). PLoS ONE 11, e0147586.
44. Korshunov, S. and Imlay, J.A. (2010) Two sources of endogenous hydrogen peroxide in Escherichia coli. Mol Microbiol 75, 1389–1401.
45. Krumova, K. and Cosa, G. (2016) Overview of reactive oxygen speciesIn Singlet Oxygen: Applications in Biosciences and Nanosciences pp. 1–21. The Royal Society of Chemistry 1.
46. LeBlanc, J.G., Milani, C., de Giori, G.S., Sesma, F., van Sinderen, D. and Ventura, M. (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24, 160–168.
47. 2 by metal-catalysed histidine oxidation. Nature 440, 363–367.
48. Leichert, L.I., Gehrke, F., Gudiseva, H.V., Blackwell, T., Ilbert, M., Walker, A.K., Strahler, J.R., Andrews, P.C. et al. (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A 105, 8197–8202.
49. Lemire, J., Mailloux, R. and Appanna, V.D. (2008) Zinc toxicity alters mitochondrial metabolism and leads to decreased ATP production in hepatocytes. J Appl Toxicol 28, 175–182.
50. Lemire, J., Mailloux, R., Auger, C., Whalen, D. and Appanna, V.D. (2010a) Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminium toxicity. Environ Microbiol 12, 1384–1390.
51. Lemire, J., Milandu, Y., Auger, C., Bignucolo, A., Appanna, V.P. and Appanna, V.D. (2010b) Histidine is a source of the antioxidant, alpha-ketoglutarate, in Pseudomonas fluorescens challenged by oxidative stress. FEMS Microbiol Lett 309, 170–177.
52. Lemire, J., Mailloux, R., Darwich, R., Auger, C. and Appanna, V.D. (2011) The disruption of L-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells. Toxicol Lett 203, 219–226.
53. Lemire, J.A., Harrison, J.J. and Turner, R.J. (2013) Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol 11, 371–384.
54. Lemire, J., Auger, C., Mailloux, R. and Appanna, V.D. (2014) Mitochondrial lactate metabolism is involved in antioxidative defense in human astrocytoma cells. J Neurosci Res 92, 464–475.
55. Liu, Y. and Imlay, J.A. (2013) Cell death from antibiotics without the involvement of reactive oxygen species. Science 339, 1210–1213.
56. Lu, Z. and Imlay, J.A. (2017) The Fumarate reductase of bacteroides thetaiotaomicron, unlike that of Escherichia coli, is configured so that it does not generate reactive oxygen species. mBio 8, e01873–16.
57. Mailloux, R.J., Beriault, R., Lemire, J., Singh, R., Chenier, D.R., Hamel, R.D. and Appanna, V.D. (2007) The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS ONE 2, e690.
58. Mailloux, R.J., Singh, R., Brewer, G., Auger, C., Lemire, J. and Appanna, V.D. (2009a) Alpha-ketoglutarate dehydrogenase and glutamate dehydrogenase work in tandem to modulate the antioxidant alpha-ketoglutarate during oxidative stress in Pseudomonas fluorescens. J Bacteriol 191, 3804–3810.
59. Mailloux, R., Puiseux-Dao, S. and Appanna, V.D. (2009b) α -Ketoglutarate abrogates the nuclear localization of HIF-α in aluminum-exposed hepatocytes. Biochimie 91, 408–415.
60. Mailloux, R.J., Lemire, J. and Appanna, V.D. (2011) Metabolic networks to combat oxidative stress in Pseudomonas fluorescens. Antonie Van Leeuwenhoek 99, 433–442.
61. Mallet, R.T. and Sun, J. (2003) Antioxidant properties of myocardial fuels. Mol Cell Biochem 253, 103–111.
62. Messner, K.R. and Imlay, J.A. (1999) The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J Biol Chem 274, 10119–10128.
63. Middaugh, J., Hamel, R., Jean-Baptiste, G., Beriault, R., Chenier, D. and Appanna, V.D. (2005) 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 280, 3159–3165.
64. Mills, E. and O'Neill, L.A. (2014) Succinate: a metabolic signal in inflammation. Trends Cell Biol 24, 313–320.
65. 2-degrading compounds. Arch Microbiol 172, 63–67.
66. Moore, L.J. and Kiley, P.J. (2001) Characterization of the dimerization domain in the FNR transcription factor. J Biol Chem 276, 45744–45750.
67. Morgan, R.W., Christman, M.F., Jacobson, F.S., Storz, G. and Ames, B.N. (1986) Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci U S A 83, 8059–8063.
68. Nichols, D.S. and McMeekin, T.A. (2002) Biomarker techniques to screen for bacteria that produce polyunsaturated fatty acids. J Microbiol Methods 48, 161–170.
69. Patrauchan, M.A., Florizone, C., Eapen, S., Gomez-Gil, L., Sethuraman, B., Fukuda, M., Davies, J., Mohn, W.W. et al. (2008) Roles of ring-hydroxylating dioxygenases in styrene and benzene catabolism in Rhodococcus jostii RHA1. J Bacteriol 190, 37–47.
70. Py, B. and Barras, F. (2010) Building Fe–S proteins: bacterial strategies. Nat Rev Microbiol 8, 436–446.
71. Reinoso, C.A., Auger, C., Appanna, V.D. and Vasquez, C.C. (2012) Tellurite-exposed Escherichia coli exhibits increased intracellular alpha-ketoglutarate. Biochem Biophys Res Commun 421, 721–726.
72. Salmon, K., Hung, S.-P., Mekjian, K., Baldi, P., Hatfield, G.W. and Gunsalus, R.P. (2003) Global gene expression profiling in Escherichia coli K12: the effects of oxygen availability and FNR. J Biol Chem 278, 29837–29855.
73. Seaver, L.C. and Imlay, J.A. (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183, 7173–7181.
74. Semchyshyn, H., Bagnyukova, T., Storey, K. and Lushchak, V. (2005) Hydrogen peroxide increases the activities of soxRS regulon enzymes and the levels of oxidized proteins and lipids in Escherichia coli. Cell Biol Int 29, 898–902.
75. Sies, H., Stahl, W. and Sundquist, A.R. (1992) Antioxidant functions of vitamins. Vitamins E and C, beta-carotene, and other carotenoids. Ann N Y Acad Sci 669, 7–20.
76. Singh, R., Mailloux, R.J., Puiseux-Dao, S. and Appanna, V.D. (2007) Oxidative stress evokes a metabolic adaptation that favors increased NADPH synthesis and decreased NADH production in Pseudomonas fluorescens. J Bacteriol 189, 6665–6675.
77. Singh, R., Lemire, J., Mailloux, R.J. and Appanna, V.D. (2008) A novel strategy involved in anti-oxidative defense: the conversion of NADH into NADPH by a metabolic network. PLoS ONE 3, e2682.
78. Singh, S., Brocker, C., Koppaka, V., Chen, Y., Jackson, B.C., Matsumoto, A. and Vasiliou, V. (2013) Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress. Free Radic Biol Med 56, 89–101.
79. Somerville, G.A. and Proctor, R.A. (2009) At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiol Mol Biol Rev 73, 233–248.
80. Somerville, G.A., Chaussee, M.S., Morgan, C.I., Fitzgerald, J.R., Dorward, D.W., Reitzer, L.J. and Musser, J.M. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect Immun 70, 6373–6382.
81. Somerville, G.A., Saïd-Salim, B., Wickman, J.M., Raffel, S.J., Kreiswirth, B.N. and Musser, J.M. (2003) Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun 71, 4724–4732.
82. Storz, G., Tartaglia, L.A., Farr, S.B. and Ames, B.N. (1990) Bacterial defenses against oxidative stress. Trends Genet 6, 363–368.
83. Thao, S. and Escalante-Semerena, J.C. (2011) Biochemical and thermodynamic analyses of Salmonella enterica Pat, a multidomain, multimeric Nε-lysine acetyltransferase involved in carbon and energy metabolism. MBio 2, e00216–11.
84. Thomas, S.C., Alhasawi, A., Auger, C., Omri, A. and Appanna, V.D. (2016) The role of formate in combatting oxidative stress. Antonie Van Leeuwenhoek 109, 263–271.
85. Tremaroli, V., Fedi, S. and Zannoni, D. (2007) Evidence for a tellurite-dependent generation of reactive oxygen species and absence of a tellurite-mediated adaptive response to oxidative stress in cells of Pseudomonas pseudoalcaligenes KF707. Arch Microbiol 187, 127–135.
86. Van Acker, H., Sass, A., Bazzini, S., De Roy, K., Udine, C., Messiaen, T., Riccardi, G., Boon, N. et al. (2013) Biofilm-grown Burkholderia cepacia complex cells survive antibiotic treatment by avoiding production of reactive oxygen species. PLoS ONE 8, e58943.
87. Walling, C. (1975) Fenton's reagent revisited. Acc Chem Res 8, 125–131.
88. Wolfe, A.J. (2005) The acetate switch. Microbiol Mol Biol Rev 69, 12–50.