Metabolism of long-chain fatty acids affects disulfide bond formation in Escherichia coli and activates envelope stress response pathways as a combat strategy
Autoři:
Kanchan Jaswal aff001; Megha Shrivastava aff001; Deeptodeep Roy aff001; Shashank Agrawal aff001; Rachna Chaba aff001
Působiště autorů:
Department of Biological Sciences, Indian Institute of Science Education and Research (IISER) Mohali, SAS Nagar, Punjab, India
aff001
Vyšlo v časopise:
Metabolism of long-chain fatty acids affects disulfide bond formation in Escherichia coli and activates envelope stress response pathways as a combat strategy. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009081
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009081
Souhrn
The envelope of gram-negative bacteria serves as the first line of defense against environmental insults. Therefore, its integrity is continuously monitored and maintained by several envelope stress response (ESR) systems. Due to its oxidizing environment, the envelope represents an important site for disulfide bond formation. In Escherichia coli, the periplasmic oxidoreductase, DsbA introduces disulfide bonds in substrate proteins and transfers electrons to the inner membrane oxidoreductase, DsbB. Under aerobic conditions, the reduced form of DsbB is re-oxidized by ubiquinone, an electron carrier in the electron transport chain (ETC). Given the critical role of ubiquinone in transferring electrons derived from the oxidation of reduced cofactors, we were intrigued whether metabolic conditions that generate a large number of reduced cofactors render ubiquinone unavailable for disulfide bond formation. To test this, here we investigated the influence of metabolism of long-chain fatty acid (LCFA), an energy-rich carbon source, on the redox state of the envelope. We show that LCFA degradation increases electron flow in the ETC. Further, whereas cells metabolizing LCFAs exhibit characteristics of insufficient disulfide bond formation, these hallmarks are averted in cells exogenously provided with ubiquinone. Importantly, the ESR pathways, Cpx and σE, are activated by envelope signals generated during LCFA metabolism. Our results argue that Cpx is the primary ESR that senses and maintains envelope redox homeostasis. Amongst the two ESRs, Cpx is induced to a greater extent by LCFAs and senses redox-dependent signal. Further, ubiquinone accumulation during LCFA metabolism is prevented in cells lacking Cpx response, suggesting that Cpx activation helps maintain redox homeostasis by increasing the oxidizing power for disulfide bond formation. Taken together, our results demonstrate an intricate relationship between cellular metabolism and disulfide bond formation dictated by ETC and ESR, and provide the basis for examining whether similar mechanisms control envelope redox status in other gram-negative bacteria.
Zdroje
1. Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harbor perspectives in biology. 2010;2(5):a000414. Epub 2010/05/11. doi: 10.1101/cshperspect.a000414 20452953
2. Macritchie DM, Raivio TL. Envelope Stress Responses. EcoSal Plus. 2009;3(2). Epub 2009/08/01.
3. Mitchell AM, Silhavy TJ. Envelope stress responses: balancing damage repair and toxicity. Nature reviews Microbiology. 2019;17(7):417–28. Epub 2019/06/01. doi: 10.1038/s41579-019-0199-0 31150012
4. Raivio TL. Everything old is new again: an update on current research on the Cpx envelope stress response. Biochimica et biophysica acta. 2014;1843(8):1529–41. Epub 2013/11/05. doi: 10.1016/j.bbamcr.2013.10.018 24184210
5. Kim DY. Two stress sensor proteins for the expression of σE regulon: DegS and RseB. Journal of Microbiology. 2015;53(5):306–10. Epub 2015/05/04.
6. Grabowicz M, Silhavy TJ. Envelope Stress Responses: An Interconnected Safety Net. Trends in biochemical sciences. 2017;42(3):232–42. Epub 2016/11/15. doi: 10.1016/j.tibs.2016.10.002 27839654
7. Dutton RJ, Boyd D, Berkmen M, Beckwith J. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(33):11933–8. Epub 2008/08/13. doi: 10.1073/pnas.0804621105 18695247
8. Manta B, Boyd D, Berkmen M. Disulfide Bond Formation in the Periplasm of Escherichia coli. EcoSal Plus. 2019;8(2). Epub 2019/02/15.
9. Denoncin K, Collet JF. Disulfide bond formation in the bacterial periplasm: major achievements and challenges ahead. Antioxidants & redox signaling. 2013;19(1):63–71. Epub 2012/08/21.
10. Bardwell JC, Lee JO, Jander G, Martin N, Belin D, Beckwith J. A pathway for disulfide bond formation in vivo. Proceedings of the National Academy of Sciences of the United States of America. 1993;90(3):1038–42. Epub 1993/02/01. doi: 10.1073/pnas.90.3.1038 8430071
11. Missiakas D, Georgopoulos C, Raina S. Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo. Proceedings of the National Academy of Sciences of the United States of America. 1993;90(15):7084–8. Epub 1993/08/01. doi: 10.1073/pnas.90.15.7084 7688471
12. Bardwell JC, McGovern K, Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell. 1991;67(3):581–9. Epub 1991/11/01. doi: 10.1016/0092-8674(91)90532-4 1934062
13. Stafford SJ, Humphreys DP, Lund PA. Mutations in dsbA and dsbB, but not dsbC, lead to an enhanced sensitivity of Escherichia coli to Hg2+ and Cd2+. FEMS microbiology letters. 1999;174(1):179–84. Epub 1999/05/11. doi: 10.1111/j.1574-6968.1999.tb13566.x 10234837
14. Rensing C, Mitra B, Rosen BP. Insertional inactivation of dsbA produces sensitivity to cadmium and zinc in Escherichia coli. Journal of bacteriology. 1997;179(8):2769–71. Epub 1997/04/01. doi: 10.1128/jb.179.8.2769-2771.1997 9098080
15. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, Fukui K. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. Journal of bacteriology. 2007;189(3):950–7. Epub 2006/11/24. doi: 10.1128/JB.01294-06 17122336
16. Landeta C, Boyd D, Beckwith J. Disulfide bond formation in prokaryotes. Nature microbiology. 2018;3(3):270–80. Epub 2018/02/22. doi: 10.1038/s41564-017-0106-2 29463925
17. Bader M, Muse W, Ballou DP, Gassner C, Bardwell JC. Oxidative protein folding is driven by the electron transport system. Cell. 1999;98(2):217–27. Epub 1999/07/31. doi: 10.1016/s0092-8674(00)81016-8 10428033
18. Kobayashi T, Kishigami S, Sone M, Inokuchi H, Mogi T, Ito K. Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(22):11857–62. Epub 1997/10/29. doi: 10.1073/pnas.94.22.11857 9342327
19. Unden G, Steinmetz PA, Degreif-Dunnwald P. The Aerobic and Anaerobic Respiratory Chain of Escherichia coli and Salmonella enterica: Enzymes and Energetics. EcoSal Plus. 2014;6(1). Epub 2014/05/01.
20. Son MS, Matthews WJ Jr., Kang Y, Nguyen DT, Hoang TT. In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infection and immunity. 2007;75(11):5313–24. Epub 2007/08/29. doi: 10.1128/IAI.01807-06 17724070
21. Fang FC, Libby SJ, Castor ME, Fung AM. Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infection and immunity. 2005;73(4):2547–9. Epub 2005/03/24. doi: 10.1128/IAI.73.4.2547-2549.2005 15784602
22. Rivera-Chavez F, Mekalanos JJ. Cholera toxin promotes pathogen acquisition of host-derived nutrients. Nature. 2019;572(7768):244–8. Epub 2019/08/02. doi: 10.1038/s41586-019-1453-3 31367037
23. Clark DP, Cronan JE. Two-Carbon Compounds and Fatty Acids as Carbon Sources. EcoSal Plus. 2005;1(2). Epub 2005/11/01.
24. Agrawal S, Jaswal K, Shiver AL, Balecha H, Patra T, Chaba R. A genome-wide screen in Escherichia coli reveals that ubiquinone is a key antioxidant for metabolism of long-chain fatty acids. The Journal of biological chemistry. 2017;292(49):20086–99. Epub 2017/10/19. doi: 10.1074/jbc.M117.806240 29042439
25. Petit-Koskas E, Contesse G. Stimulation in trans of synthesis of E. coli gal operon enzymes by lambdoid phages during low catabolite repression. Molecular & general genetics: MGG. 1976;143(2):203–9. Epub 1976/01/16.
26. Campbell JW, Cronan JE Jr., The enigmatic Escherichia coli fadE gene is yafH. Journal of bacteriology. 2002;184(13):3759–64. Epub 2002/06/12. doi: 10.1128/jb.184.13.3759-3764.2002 12057976
27. Sone M, Kishigami S, Yoshihisa T, Ito K. Roles of disulfide bonds in bacterial alkaline phosphatase. The Journal of biological chemistry. 1997;272(10):6174–8. Epub 1997/03/07. doi: 10.1074/jbc.272.10.6174 9045630
28. Rietsch A, Belin D, Martin N, Beckwith J. An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America. 1996;93(23):13048–53. Epub 1996/11/12. doi: 10.1073/pnas.93.23.13048 8917542
29. Aussel L, Pierrel F, Loiseau L, Lombard M, Fontecave M, Barras F. Biosynthesis and physiology of coenzyme Q in bacteria. Biochimica et biophysica acta. 2014;1837(7):1004–11. Epub 2014/02/01. doi: 10.1016/j.bbabio.2014.01.015 24480387
30. Skorko-Glonek J, Sobiecka-Szkatula A, Narkiewicz J, Lipinska B. The proteolytic activity of the HtrA (DegP) protein from Escherichia coli at low temperatures. Microbiology. 2008;154(Pt 12):3649–58. Epub 2008/12/03. doi: 10.1099/mic.0.2008/020487-0 19047732
31. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(36):13318–23. Epub 2004/08/25. doi: 10.1073/pnas.0403064101 15326287
32. Sardesai AA, Genevaux P, Schwager F, Ang D, Georgopoulos C. The OmpL porin does not modulate redox potential in the periplasmic space of Escherichia coli. The EMBO journal. 2003;22(7):1461–6. Epub 2003/03/28. doi: 10.1093/emboj/cdg152 12660153
33. Zeng H, Snavely I, Zamorano P, Javor GT. Low ubiquinone content in Escherichia coli causes thiol hypersensitivity. Journal of bacteriology. 1998;180(14):3681–5. Epub 1998/07/11. doi: 10.1128/JB.180.14.3681-3685.1998 9658014
34. Raivio TL, Silhavy TJ. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. Journal of bacteriology. 1997;179(24):7724–33. Epub 1997/12/24. doi: 10.1128/jb.179.24.7724-7733.1997 9401031
35. Snyder WB, Davis LJ, Danese PN, Cosma CL, Silhavy TJ. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. Journal of bacteriology. 1995;177(15):4216–23. Epub 1995/08/01. doi: 10.1128/jb.177.15.4216-4223.1995 7635808
36. Buelow DR, Raivio TL. Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. Journal of bacteriology. 2005;187(19):6622–30. Epub 2005/09/17. doi: 10.1128/JB.187.19.6622-6630.2005 16166523
37. Isaac DD, Pinkner JS, Hultgren SJ, Silhavy TJ. The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(49):17775–9. Epub 2005/11/24. doi: 10.1073/pnas.0508936102 16303867
38. Wolfe AJ, Parikh N, Lima BP, Zemaitaitis B. Signal integration by the two-component signal transduction response regulator CpxR. Journal of bacteriology. 2008;190(7):2314–22. Epub 2008/01/29. doi: 10.1128/JB.01906-07 18223085
39. Vogt SL, Evans AD, Guest RL, Raivio TL. The Cpx envelope stress response regulates and is regulated by small noncoding RNAs. Journal of bacteriology. 2014;196(24):4229–38. Epub 2014/09/24. doi: 10.1128/JB.02138-14 25246476
40. Walsh NP, Alba BM, Bose B, Gross CA, Sauer RT. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell. 2003;113(1):61–71. Epub 2003/04/08. doi: 10.1016/s0092-8674(03)00203-4 12679035
41. Lima S, Guo MS, Chaba R, Gross CA, Sauer RT. Dual molecular signals mediate the bacterial response to outer-membrane stress. Science. 2013;340(6134):837–41. Epub 2013/05/21. doi: 10.1126/science.1235358 23687042
42. Costanzo A, Ades SE. Growth phase-dependent regulation of the extracytoplasmic stress factor, σE, by guanosine 3',5'-bispyrophosphate (ppGpp). Journal of bacteriology. 2006;188(13):4627–34. Epub 2006/06/22. doi: 10.1128/JB.01981-05 16788171
43. Pittman MS, Robinson HC, Poole RK. A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. The Journal of biological chemistry. 2005;280(37):32254–61. Epub 2005/07/26. doi: 10.1074/jbc.M503075200 16040611
44. Pittman MS, Corker H, Wu G, Binet MB, Moir AJ, Poole RK. Cysteine is exported from the Escherichia coli cytoplasm by CydDC, an ATP-binding cassette-type transporter required for cytochrome assembly. The Journal of biological chemistry. 2002;277(51):49841–9. Epub 2002/10/24. doi: 10.1074/jbc.M205615200 12393891
45. Raivio TL, Leblanc SK, Price NL. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. Journal of bacteriology. 2013;195(12):2755–67. Epub 2013/04/09. doi: 10.1128/JB.00105-13 23564175
46. Cox GB, Newton NA, Gibson F, Snoswell AM, Hamilton JA. The function of ubiquinone in Escherichia coli. The Biochemical journal. 1970;117(3):551–62. Epub 1970/04/01. doi: 10.1042/bj1170551 4192611
47. Sharma P, Stagge S, Bekker M, Bettenbrock K, Hellingwerf KJ. Kinase activity of ArcB from Escherichia coli is subject to regulation by both ubiquinone and demethylmenaquinone. PloS one. 2013;8(10):e75412. Epub 2013/10/12. doi: 10.1371/journal.pone.0075412 24116043
48. Guest RL, Wang J, Wong JL, Raivio TL. A Bacterial Stress Response Regulates Respiratory Protein Complexes To Control Envelope Stress Adaptation. Journal of bacteriology. 2017;199(20):e00153–17. Epub 2017/08/02. doi: 10.1128/JB.00153-17 28760851
49. Miyadai H, Tanaka-Masuda K, Matsuyama S, Tokuda H. Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. The Journal of biological chemistry. 2004;279(38):39807–13. Epub 2004/07/15. doi: 10.1074/jbc.M406390200 15252048
50. Delhaye A, Laloux G, Collet JF. The Lipoprotein NlpE Is a Cpx Sensor That Serves as a Sentinel for Protein Sorting and Folding Defects in the Escherichia coli Envelope. Journal of bacteriology. 2019;201(10):e00611–18. Epub 2019/03/06. doi: 10.1128/JB.00611-18 30833359
51. May KL, Lehman KM, Mitchell AM, Grabowicz M. A Stress Response Monitoring Lipoprotein Trafficking to the Outer Membrane. mBio. 2019;10(3):e00618–19. Epub 2019/05/30. doi: 10.1128/mBio.00618-19 31138744
52. DiGiuseppe PA, Silhavy TJ. Signal detection and target gene induction by the CpxRA two-component system. Journal of bacteriology. 2003;185(8):2432–40. Epub 2003/04/03. doi: 10.1128/jb.185.8.2432-2440.2003 12670966
53. Chaba R, Alba BM, Guo MS, Sohn J, Ahuja N, Sauer RT, et al. Signal integration by DegS and RseB governs the σE-mediated envelope stress response in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(5):2106–11. Epub 2011/01/20. doi: 10.1073/pnas.1019277108 21245315
54. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. Conserved and variable functions of the σE stress response in related genomes. PLoS biology. 2006;4(1):e2. Epub 2005/12/13. doi: 10.1371/journal.pbio.0040002 16336047
55. Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes & development. 1997;11(9):1169–82. Epub 1997/05/01.
56. Holyoake LV, Hunt S, Sanguinetti G, Cook GM, Howard MJ, Rowe ML, et al. CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress. The Biochemical journal. 2016;473(6):693–701. Epub 2015/12/25. doi: 10.1042/BJ20150536 26699904
57. Ha UH, Wang Y, Jin S. DsbA of Pseudomonas aeruginosa is essential for multiple virulence factors. Infection and immunity. 2003;71(3):1590–5. Epub 2003/02/22. doi: 10.1128/iai.71.3.1590-1595.2003 12595484
58. Peek JA, Taylor RK. Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America. 1992;89(13):6210–4. Epub 1992/07/01. doi: 10.1073/pnas.89.13.6210 1631111
59. Wu W, Badrane H, Arora S, Baker HV, Jin S. MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. Journal of bacteriology. 2004;186(22):7575–85. Epub 2004/11/02. doi: 10.1128/JB.186.22.7575-7585.2004 15516570
60. Kovacikova G, Skorupski K. The alternative sigma factor σE plays an important role in intestinal survival and virulence in Vibrio cholerae. Infection and immunity. 2002;70(10):5355–62. Epub 2002/09/14. doi: 10.1128/iai.70.10.5355-5362.2002 12228259
61. Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M. The alternative sigma factor, σE, is critically important for the virulence of Salmonella typhimurium. Infection and immunity. 1999;67(4):1560–8. Epub 1999/03/20. 10084987
62. Humphreys S, Rowley G, Stevenson A, Anjum MF, Woodward MJ, Gilbert S, et al. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infection and immunity. 2004;72(8):4654–61. Epub 2004/07/24. doi: 10.1128/IAI.72.8.4654-4661.2004 15271926
63. Acosta N, Pukatzki S, Raivio TL. The Cpx system regulates virulence gene expression in Vibrio cholerae. Infection and immunity. 2015;83(6):2396–408. Epub 2015/04/01. doi: 10.1128/IAI.03056-14 25824837
64. Miki T, Okada N, Danbara H. Two periplasmic disulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island 2 type III secretion system. The Journal of biological chemistry. 2004;279(33):34631–42. Epub 2004/06/01. doi: 10.1074/jbc.M402760200 15169785
65. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular systems biology. 2006;2:2006.0008. Epub 2006/06/02. doi: 10.1038/msb4100050 16738554
66. Haldimann A, Wanner BL. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. Journal of bacteriology. 2001;183(21):6384–93. Epub 2001/10/10. doi: 10.1128/JB.183.21.6384-6393.2001 11591683
67. San KY, Bennett GN, Berrios-Rivera SJ, Vadali RV, Yang YT, Horton E, et al. Metabolic engineering through cofactor manipulation and its effects on metabolic flux redistribution in Escherichia coli. Metabolic engineering. 2002;4(2):182–92. Epub 2002/05/16. doi: 10.1006/mben.2001.0220 12009797
68. Wang G, Maier RJ. An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infection and immunity. 2004;72(3):1391–6. Epub 2004/02/24. doi: 10.1128/iai.72.3.1391-1396.2004 14977943
69. McNeil MB, Clulow JS, Wilf NM, Salmond GP, Fineran PC. SdhE is a conserved protein required for flavinylation of succinate dehydrogenase in bacteria. The Journal of biological chemistry. 2012;287(22):18418–28. Epub 2012/04/05. doi: 10.1074/jbc.M111.293803 22474332
70. Miller JH. Experiments in molecular genetics Cold Spring Harbor Laboratory, NY; 1972.
71. Pathania A, Gupta AK, Dubey S, Gopal B, Sardesai AA. The Topology of the l-Arginine Exporter ArgO Conforms to an Nin-Cout Configuration in Escherichia coli: Requirement for the Cytoplasmic N-Terminal Domain, Functional Helical Interactions, and an Aspartate Pair for ArgO Function. Journal of bacteriology. 2016;198(23):3186–99. Epub 2016/09/21. doi: 10.1128/JB.00423-16 27645388
72. Brickman E, Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. Journal of molecular biology. 1975;96(2):307–16. Epub 1975/08/05. doi: 10.1016/0022-2836(75)90350-2 1100846
73. Kumar C, Igbaria A, D'Autreaux B, Planson AG, Junot C, Godat E, et al. Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. The EMBO journal. 2011;30(10):2044–56. Epub 2011/04/12. doi: 10.1038/emboj.2011.105 21478822
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 10
- Zvoní budík? Přispěte si ještě chvilku, bude vám to myslet rychleji!
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
- Umíme správně řešit osteporotické zlomeniny?
- Vědci vytvořili první funkční mozkovou tkáň pomocí 3D tisku
Nejčtenější v tomto čísle
- Evaluation of both exonic and intronic variants for effects on RNA splicing allows for accurate assessment of the effectiveness of precision therapies
- RNA-directed DNA Methylation
- The DNA methylome of human sperm is distinct from blood with little evidence for tissue-consistent obesity associations
- Correction: Molecular predictors of brain metastasis-related microRNAs in lung adenocarcinoma