The LysR-type transcription factor HbrL is a global regulator of iron homeostasis and porphyrin synthesis in Rhodobacter capsulatus

Molecular Microbiology

Volumn 90, Issue 6, 2013, Pages 1277-1292

  Zappa, Sébastien ^a   Bauer, Carl E ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; HEME; IRON; PORPHYRIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HBRL; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; CULTURE MEDIUM; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; HBRL GENE; HEME SYNTHESIS; IRON HOMEOSTASIS; IRON METABOLISM; IRON TRANSPORT; NONHUMAN; PHOTOSYNTHESIS; PORPHYRIN SYNTHESIS; PRIORITY JOURNAL; RHODOBACTER CAPSULATUS; SYNTHESIS;

BACTERIA (MICROORGANISMS); RHODOBACTER CAPSULATUS;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HEME; HOMEOSTASIS; ION TRANSPORT; IRON; RHODOBACTER CAPSULATUS; TETRAPYRROLES; TRANSCRIPTION FACTORS;

EID: 84890114982     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12431     Document Type: Article

References (68)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Andrews, S.C., Robinson, A.K., and Rodríguez-Quiñones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
3. Anzaldi, L.L., and Skaar, E.P. (2010) Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect Immun 78: 4977-4989.
4. Butcher, J., Sarvan, S., Brunzelle, J.S., Couture, J.-F., and Stintzi, A.P. (2012) Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation. Proc Natl Acad Sci USA 109: 10047-10052.
5. Cao, J., Woodhall, M.R., Alvarez, J., Cartron, M.L., and Andrews, S.C. (2007) EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65: 857-875.
6. Carpenter, B.M., Whitmire, J.M., and Merrell, D.S. (2009) This is not your mother's repressor: the complex role of Fur in pathogenesis. Infect Immun 77: 2590-2601.
7. Cartron, M.L., Maddocks, S.E., Gillingham, P., Craven, C.J., and Andrews, S.C. (2006) Feo - transport of ferrous iron into bacteria. Biometals 19: 143-157.
8. Chao, T.-C., Becker, A., Buhrmester, J., Pühler, A., and Weidner, S. (2004) The Sinorhizobium meliloti fur gene regulates, with dependence on Mn(II), transcription of the sitABCD operon, encoding a metal-type transporter. J Bacteriol 186: 3609-3620.
9. Chiancone, E., Ceci, P., Ilari, A., Ribacchi, F., and Stefanini, S. (2004) Iron and proteins for iron storage and detoxification. Biometals 17: 197-202.
10. Clark-Walker, G.D., Rittenberg, B., and Lascelles, J. (1967) Cytochrome synthesis and its regulation in Spirillum itersonii. J Bacteriol 94: 1648-1655.
11. Cornelis, P., and Andrews, S.C. (2012) Regulation of iron homeostasis in bacteria. In Bacterial Regulatory Networks. Filloux, A. (ed.). Norfolk, UK: Caister Academic Press, pp. 261-272.
12. Cornelis, P., Wei, Q., Andrews, S.C., and Vinckx, T. (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3: 540-549.
13. Dailey, H.A., Septer, A.N., Daugherty, L., Thames, D., Gerdes, S., Stabb, E.V., etal. (2011) The Escherichia coli protein YfeX functions as a porphyrinogen oxidase, not a heme dechelatase. MBio 2: e00248-11.
14. Dangel, A.W., and Tabita, F.R. (2009) Protein-protein interactions between CbbR and RegA (PrrA), transcriptional regulators of the cbb operons of Rhodobacter sphaeroides. Mol Microbiol 71: 717-729.
15. Dashper, S.G., Butler, C.A., Lissel, J.P., Paolini, R.A., Hoffmann, B., Veith, P.D., etal. (2005) A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280: 28095-28102.
16. Davies, B.W., Bogard, R.W., and Mekalanos, J.J. (2011) Mapping the regulon of Vibrio cholerae ferric uptake regulator expands its known network of gene regulation. Proc Natl Acad Sci USA 108: 12467-12472.
17. Díaz-Mireles, E., Wexler, M., Sawers, G., Bellini, D., Todd, J.D., and Johnston, A.W.B. (2004) The Fur-like protein Mur of Rhizobium leguminosarum is a Mn(2+)-responsive transcriptional regulator. Microbiology 150: 1447-1456.
18. Ghrist, A.C., Heil, G., and Stauffer, G.V. (2001) GcvR interacts with GcvA to inhibit activation of the Escherichia coli glycine cleavage operon. Microbiology 147: 2215-2221.
19. Graça-Souza, A.V., Maya-Monteiro, C., Paiva-Silva, G.O., Braz, G.R.C., Paes, M.C., Sorgine, M.H.F., etal. (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem Mol Biol 36: 322-335.
20. Grosse, C., Scherer, J., Koch, D., Otto, M., Taudte, N., and Grass, G. (2006) A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62: 120-131.
21. Hamza, I., Chauhan, S., Hassett, R., and O'Brian, M.R. (1998) The bacterial irr protein is required for coordination of heme biosynthesis with iron availability. J Biol Chem 273: 21669-21674.
22. Hohle, T.H., and O'Brian, M.R. (2009) The mntH gene encodes the major Mn(2+) transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein. Mol Microbiol 72: 399-409.
23. Hohle, T.H., and O'Brian, M.R. (2010) Transcriptional control of the Bradyrhizobium japonicum irr gene requires repression by Fur and antirepression by Irr. J Biol Chem 285: 26074-26080.
24. Johnston, A.W.B., Todd, J.D., Curson, A.R., Lei, S., Nikolaidou-Katsaridou, N., Gelfand, M.S., and Rodionov, D.A. (2007) Living without Fur: the subtlety and complexity of iron-responsive gene regulation in the symbiotic bacterium Rhizobium and other alpha-proteobacteria. Biometals 20: 501-511.
25. Kitphati, W., Ngok-Ngam, P., Suwanmaneerat, S., Sukchawalit, R., and Mongkolsuk, S. (2007) Agrobacterium tumefaciens Fur has important physiological roles in iron and manganese homeostasis, the oxidative stress response, and full virulence. Appl Environ Microbiol 73: 4760-4768.
26. Kovacikova, G., Lin, W., and Skorupski, K. (2004) Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Mol Microbiol 53: 129-142.
27. Lascelles, J. (1956) The synthesis of porphyrins and bacteriochlorophyll by cell suspensions of Rhodopseudomonas spheroides. Biochem J 62: 78-93.
28. Lascelles, J., and Hatch, T.P. (1969) Bacteriochlorophyll and heme synthesis in Rhodopseudomonas spheroides: possible role of heme in regulation of the branched biosynthetic pathway. J Bacteriol 98: 712-720.
29. Lascelles, J., Rittenberg, B., and Clark-Walker, G.D. (1969) Growth and cytochrome synthesis in a hemin-requiring mutant of Spirillum itersonii. J Bacteriol 97: 455-456.
30. Lee, J.-W., and Helmann, J.D. (2007) Functional specialization within the Fur family of metalloregulators. Biometals 20: 485-499.
31. Létoffé, S., Heuck, G., Delepelaire, P., Lange, N., and Wandersman, C. (2009) Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact. Proc Natl Acad Sci USA 106: 11719-11724.
32. Martínez, M., Ugalde, R.A., and Almirón, M. (2006) Irr regulates brucebactin and 2, 3-dihydroxybenzoic acid biosynthesis, and is implicated in the oxidative stress resistance and intracellular survival of Brucella abortus. Microbiology 152: 2591-2598.
33. Massé, E., and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99: 4620-4625.
34. Massé, E., Salvail, H., Desnoyers, G., and Arguin, M. (2007) Small RNAs controlling iron metabolism. Curr Opin Microbiol 10: 140-145.
35. Menscher, E.A., Caswell, C.C., Anderson, E.S., and Roop, R.M. (2012) Mur regulates the gene encoding the manganese transporter MntH in Brucella abortus 2308. J Bacteriol 194: 561-566.
36. Nakahigashi, K., Nishimura, K., Miyamoto, K., and Inokuchi, H. (1991) Photosensitivity of a protoporphyrin-accumulating, light-sensitive mutant (visA) of Escherichia coli K-12. Proc Natl Acad Sci USA 88: 10520-10524.
37. Pappenheimer, A.M. (1947) Diphtheria toxin; a reinvestigation of the effect of iron on toxin and porphyrin production. J Biol Chem 167: 251-259.
38. Pappenheimer, A.M., and Hendee, E.D. (1947) Diphtheria toxin; the iron enzymes of Corynebacterium diphtheriae and their possible relation to diphtheria toxin. J Biol Chem 171: 701-713.
39. Perry, R.D., Craig, S.K., Abney, J., Bobrov, A.G., Kirillina, O., Mier, I., etal. (2012) Manganese transporters Yfe and MntH are Fur-regulated and important for the virulence of Yersinia pestis. Microbiology 158: 804-815.
40. Peuser, V., Metz, S., and Klug, G. (2011) Response of the photosynthetic bacterium Rhodobacter sphaeroides to iron limitation and the role of a Fur orthologue in this response. Environ Microbiol Rep 3: 397-404.
41. Peuser, V., Remes, B., and Klug, G. (2012) Role of the Irr protein in the regulation of iron metabolism in Rhodobacter sphaeroides. PLoS ONE 7: e42231.
42. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
43. Pfaffl, M.W., Horgan, G.W., and Dempfle, L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36.
44. Qi, Z., and O'Brian, M.R. (2002) Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol Cell 9: 155-162.
45. Rajasekaran, M.B., Nilapwar, S., Andrews, S.C., and Watson, K.A. (2010) EfeO-cupredoxins: major new members of the cupredoxin superfamily with roles in bacterial iron transport. Biometals 23: 1-17.
46. Rawlinson, W.A., and Hale, J.H. (1948) The prosthetic groups of the intracellular haems of Corynebacterium diphtheriae and their relationship to the cytochromes. Biochem J 42: 247-255.
47. Rodionov, D.A., Gelfand, M.S., Todd, J.D., Curson, A.R.J., and Johnston, A.W.B. (2006) Computational reconstruction of iron- and manganese-responsive transcriptional networks in alpha-proteobacteria. PLoS Comput Biol 2: e163.
48. Roe, K.L., Hogle, S.L., and Barbeau, K.A. (2013) Utilization of heme as an iron source by marine Alphaproteobacteria in the Roseobacter clade. Appl Environ Microbiol 79: 5753-5762.
49. Rong, C., Zhang, C., Zhang, Y., Qi, L., Yang, J., Guan, G., etal. (2012) FeoB2 functions in magnetosome formation and oxidative stress protection in Magnetospirillum gryphiswaldense strain MSR-1. J Bacteriol 194: 3972-3976.
50. Rudolph, G., Hennecke, H., and Fischer, H.-M.M. (2006) Beyond the Fur paradigm: iron-controlled gene expression in rhizobia. FEMS Microbiol Rev 30: 631-648.
51. Sarma, R., Barney, B.M., Hamilton, T.L., Jones, A., Seefeldt, L.C., and Peters, J.W. (2008) Crystal structure of the L protein of Rhodobacter sphaeroides light-independent protochlorophyllide reductase with MgADP bound: a homologue of the nitrogenase Fe protein. Biochemistry 47: 13004-13015.
52. Schobert, M., and Jahn, D. (2002) Regulation of heme biosynthesis in non-phototrophic bacteria. J Mol Microbiol Biotechnol 4: 287-294.
53. Senanayake, S.D., and Brian, D.A. (1995) Precise large deletions by the PCR-based overlap extension method. Mol Biotechnol 4: 13-15.
54. Sirijovski, N., Mamedov, F., Olsson, U., Styring, S., and Hansson, M. (2007) Rhodobacter capsulatus magnesium chelatase subunit BchH contains an oxygen sensitive iron-sulfur cluster. Arch Microbiol 188: 599-608.
55. Smaldone, G.T., Revelles, O., Gaballa, A., Sauer, U., Antelmann, H., and Helmann, J.D. (2012) A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism. J Bacteriol 194: 2594-2605.
56. Small, S.K., and O'Brian, M.R. (2011) The Bradyrhizobium japonicum frcB gene encodes a diheme ferric reductase. J Bacteriol 193: 4088-4094.
57. Small, S.K., Puri, S., Sangwan, I., and O'Brian, M.R. (2009) Positive control of ferric siderophore receptor gene expression by the Irr protein in Bradyrhizobium japonicum. J Bacteriol 191: 1361-1368.
58. Smart, J.L., and Bauer, C.E. (2006) Tetrapyrrole biosynthesis in Rhodobacter capsulatus is transcriptionally regulated by the heme-binding regulatory protein, HbrL. J Bacteriol 188: 1567-1576.
59. Smart, J.L., Willett, J.W., and Bauer, C.E. (2004) Regulation of hem gene expression in Rhodobacter capsulatus by redox and photosystem regulators RegA, CrtJ, FnrL, and AerR. J Mol Biol 342: 1171-1186.
60. Swem, D.L., Swem, L.R., Setterdahl, A., and Bauer, C.E. (2005) Involvement of SenC in assembly of cytochrome c oxidase in Rhodobacter capsulatus. J Bacteriol 187: 8081-8087.
61. Touati, D. (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373: 1-6.
62. Vermeglio, A., and Joliot, P. (1999) The photosynthetic apparatus of Rhodobacter sphaeroides. Trends Microbiol 7: 435-440.
63. Weaver, P.F., Wall, J.D., and Gest, H. (1975) Characterization of Rhodopseudomonas capsulata. Arch Microbiol 105: 207-216.
64. Wexler, M., Todd, J.D., Kolade, O., Bellini, D., Hemmings, A.M., Sawers, G., and Johnston, A. (2003) Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149: 1357-1365.
65. Yang, H., Inokuchi, H., and Adler, J. (1995) Phototaxis away from blue light by an Escherichia coli mutant accumulating protoporphyrin IX. Proc Natl Acad Sci USA 92: 7332-7336.
66. Yoon, J.-H., Kang, S.-J., Park, S., Lee, S.-Y., and Oh, T.-K. (2007) Reclassification of Aquaspirillum itersonii and Aquaspirillum peregrinum as Novispirillum itersonii gen. nov., comb. nov. and Insolitispirillum peregrinum gen. nov., comb. nov. Int J Syst Evol Microbiol 57: 2830-2835.
67. Zappa, S., and Bauer, C.E. (2013) Iron homeostasis in the Rhodobacter genus. Adv Bot Res 66: 289-326.
68. Zappa, S., Li, K., and Bauer, C.E. (2010) The tetrapyrrole biosynthetic pathway and its regulation in Rhodobacter capsulatus. Adv Exp Med Biol 675: 229-250.