The Regulatory Role of Ferric Uptake Regulator (Fur) during Anaerobic Respiration of Shewanella piezotolerans WP3

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Yang, Xin Wei ^a   He, Ying ^a   Xu, Jun ^a   Xiao, Xiang ^a   Wang, Feng Ping ^a,b  

^a Shanghai Jiao Tong University   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; FERRIC UPTAKE REGULATOR; HEME;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM MUTANT; COMPARATIVE STUDY; CONTROLLED STUDY; DELETION MUTANT; ELECTRON TRANSPORT; FUR1 GENE; GEL MOBILITY SHIFT ASSAY; GENE REGULATORY NETWORK; GROWTH RATE; GROWTH REGULATION; HEME SYNTHESIS; IRON METABOLISM; MICROBIAL RESPIRATION; NONHUMAN; PLEIOTROPY; PROTEIN FUNCTION; REGULATORY MECHANISM; SHEWANELLA; SHEWANELLA PIEZOTOLERANS; TRANSCRIPTOMICS; WILD TYPE;

AEROBIOSIS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; REPRESSOR PROTEINS; SHEWANELLA;

EID: 84885063651     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075588     Document Type: Article

References (70)

1. Andrews SC, Robinson AK, Rodriguez-Quinones F, (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
2. Touati D, (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373: 1-6.
3. Wandersman C, Delepelaire P, (2004) Bacterial iron sources: from siderophores to hemophores. Annual Review of Microbiology 58: 611-647.
4. Schroder I, Johnson E, de Vries S, (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27: 427-447.
5. Cornelis P, Wei Q, Andrews SC, Vinckx T, (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3: 540-549.
6. Delany I, Rappuoli R, Scarlato V, (2004) Fur functions as an activator and as a repressor of putative virulence genes in Neisseria meningitidis. Mol Microbiol 52: 1081-1090.
7. Nandal A, Huggins CC, Woodhall MR, McHugh J, Rodriguez-Quinones F, et al. (2010) Induction of the ferritin gene (ftnA) of Escherichia coli by Fe(2+)-Fur is mediated by reversal of H-NS silencing and is RyhB independent. Mol Microbiol 75: 637-657.
8. Craig SA, Carpenter CD, Mey AR, Wyckoff EE, Payne SM, (2011) Positive Regulation of the Vibrio cholerae Porin OmpT by Iron and Fur. J Bacteriol 193: 6505-6511.
9. Miles S, Carpenter BM, Gancz H, Merrell DS, (2010) Helicobacter pylori apo-Fur regulation appears unconserved across species. J Microbiol 48: 378-386.
10. Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB, et al. (2008) 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 105: 11927-11932.
11. Masse E, Salvail H, Desnoyers G, Arguin M, (2007) Small RNAs controlling iron metabolism. Curr Opin Microbiol 10: 140-145.
12. Masse E, Vanderpool CK, Gottesman S, (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187: 6962-6971.
13. Escolar L, Perez-Martin J, de Lorenzo V, (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
14. Ratledge C, Dover LG, (2000) Iron metabolism in pathogenic bacteria. Annual Review of Microbiology 54: 881-941.
15. Yang Y, Harris DP, Luo F, Wu L, Parsons AB, et al. (2008) Characterization of the Shewanella oneidensis Fur gene: roles in iron and acid tolerance response. BMC Genomics 9Suppl 1: S11.
16. Ellermeier JR, Slauch JM, (2008) Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J Bacteriol 190: 476-486.
17. Teixido L, Cortes P, Bigas A, Alvarez G, Barbe J, et al. (2010) Control by Fur of the nitrate respiration regulators NarP and NarL in Salmonella enterica. Int Microbiol 13: 33-39.
18. Wan XF, Verberkmoes NC, McCue LA, Stanek D, Connelly H, et al. (2004) Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J Bacteriol 186: 8385-8400.
19. Baichoo N, Wang T, Ye R, Helmann JD, (2002) Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol Microbiol 45: 1613-1629.
20. Paustian ML, May BJ, Kapur V, (2001) Pasteurella multocida gene expression in response to iron limitation. Infect Immun 69: 4109-4115.
21. Pellicer S, Gonzalez A, Peleato ML, Martinez JI, Fillat MF, et al. (2012) Site-directed mutagenesis and spectral studies suggest a putative role of FurA from Anabaena sp. PCC 7120 as a heme sensor protein. FEBS J 279: 2231-2246.
22. Gonzalez A, Bes MT, Valladares A, Peleato ML, Fillat MF, (2012) FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environ Microbiol 14: 3175-3187.
23. Wang F, Wang J, Jian H, Zhang B, Li S, et al. (2008) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS One 3: e1937.
24. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, et al. (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49 Pt 2: 705-724.
25. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, et al. (2008) Towards environmental systems biology of Shewanella. Nature Reviews Microbiology 6: 592-603.
26. Meyer TE, Tsapin AI, Vandenberghe I, de Smet L, Frishman D, et al. (2004) Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8: 57-77.
27. Rodionov DA, Novichkov PS, Stavrovskaya ED, Rodionova IA, Li X, et al. (2011) Comparative genomic reconstruction of transcriptional networks controlling central metabolism in the Shewanella genus. BMC Genomics 12Suppl 1: S3.
28. Myers CR, Nealson KH, (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240: 1319-1321.
29. Thompson DK, Beliaev AS, Giometti CS, Tollaksen SL, Khare T, et al. (2002) Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl Environ Microbiol 68: 881-892.
30. Wang F, Wang P, Chen M, Xiao X, (2004) Isolation of extremophiles with the detection and retrieval of Shewanella strains in deep-sea sediments from the west Pacific. Extremophiles 8: 165-168.
31. Chen S-Y, Ambe S, Takematsu N, Ambe F, (1996) The Chemical States of Iron in Marine Sediments by Means of Mössbauer Spectroscopy in Combination with Chemical Leachings. J Oceanography 52: 705-715.
32. Xiao X, Wang P, Zeng X, Bartlett DH, Wang F, (2007) Shewanella psychrophila sp. nov. and Shewanella piezotolerans sp. nov., isolated from west Pacific deep-sea sediment. Int J Syst Evol Microbiol 57: 60-65.
33. Wu W, Li B, Hu J, Li J, Wang F, et al. (2011) Iron reduction and magnetite biomineralization mediated by a deep-sea iron reducing bacterium Shewanella piezotolerans WP3. J Geophys Res 116: G04034.
34. Chen Y, Wang F, Xu J, Mehmood MA, Xiao X, (2010) Physiological and evolutionary studies of NAP systems in Shewanella piezotolerans WP3. ISME J 5: 843-855.
35. Schwyn B, Neilands JB, (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
36. Fennessey CM, Jones ME, Taillefert M, DiChristina TJ, (2010) Siderophores are not involved in Fe(III) solubilization during anaerobic Fe(III) respiration by Shewanella oneidensis MR-1. Appl Environ Microbiol 76: 2425-2432.
37. Lovley DR, Holmes DE, Nevin KP, (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49: 219-286.
38. Edwards RA, Keller LH, Schifferli DM, (1998) Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207: 149-157.
39. Li R, Li Y, Kristiansen K, Wang J, (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714.
40. Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG, (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
41. Novichkov PS, Rodionov DA, Stavrovskaya ED, Novichkova ES, Kazakov AE, et al. (2010) RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res 38: W299-307.
42. Bender KS, Yen HC, Hemme CL, Yang Z, He Z, et al. (2007) Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 73: 5389-5400.
43. Troxell B, Fink RC, Porwollik S, McClelland M, Hassan HM, (2011) The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets. BMC Microbiol 11: 236.
44. Parker D, Kennan RM, Myers GS, Paulsen IT, Rood JI, (2005) Identification of a Dichelobacter nodosus ferric uptake regulator and determination of its regulatory targets. J Bacteriol 187: 366-375.
45. Gao H, Barua S, Liang Y, Wu L, Dong Y, et al. (2010) Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration. Microb Biotechnol 3: 455-466.
46. Shi L, Squier TC, Zachara JM, Fredrickson JK, (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65: 12-20.
47. Postle K, Kadner RJ, (2003) Touch and go: tying TonB to transport. Mol Microbiol 49: 869-882.
48. Kuehl CJ, Crosa JH, (2010) The TonB energy transduction systems in Vibrio species. Future Microbiol 5: 1403-1412.
49. Beliaev AS, Klingeman DM, Klappenbach JA, Wu L, Romine MF, et al. (2005) Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J Bacteriol 187: 7138-7145.
50. Masse E, Gottesman S, (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99: 4620-4625.
51. Iuchi S, Lin EC, (1988) arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci U S A 85: 1888-1892.
52. Evans MR, Fink RC, Vazquez-Torres A, Porwollik S, Jones-Carson J, et al. (2011) Analysis of the ArcA regulon in anaerobically grown Salmonella enterica sv. Typhimurium. BMC Microbiol 11: 58.
53. Gao H, Wang X, Yang ZK, Palzkill T, Zhou J, (2008) Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses. BMC Genomics 9: 42.
54. Yuan J, Wei B, Lipton MS, Gao H, (2012) Impact of ArcA loss in Shewanella oneidensis revealed by comparative proteomics under aerobic and anaerobic conditions. Proteomics 12: 1957-1969.
55. Gralnick JA, Brown CT, Newman DK, (2005) Anaerobic regulation by an atypical Arc system in Shewanella oneidensis. Mol Microbiol 56: 1347-1357.
56. Gao H, Wang X, Yang ZK, Chen J, Liang Y, et al. (2010) Physiological roles of ArcA, Crp, and EtrA and their interactive control on aerobic and anaerobic respiration in Shewanella oneidensis. PLoS One 5: e15295.
57. Saffarini DA, Schultz R, Beliaev A, (2003) Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J Bacteriol 185: 3668-3671.
58. Yang Y, Harris DP, Luo F, Xiong W, Joachimiak M, et al. (2009) Snapshot of iron response in Shewanella oneidensis by gene network reconstruction. BMC Genomics 10: 131.
59. Troxell B, Sikes ML, Fink RC, Vazquez-Torres A, Jones-Carson J, et al. (2011) Fur negatively regulates hns and is required for the expression of HilA and virulence in Salmonella enterica sv. Typhimurium. J Bacteriol 193: 497-505.
60. Myers JM, Myers CR, (2000) Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J Bacteriol 182: 67-75.
61. Murphy JN, Saltikov CW, (2007) The cymA gene, encoding a tetraheme c-type cytochrome, is required for arsenate respiration in Shewanella species. J Bacteriol 189: 2283-2290.
62. Maier TM, Myers JM, Myers CR, (2003) Identification of the gene encoding the sole physiological fumarate reductase in Shewanella oneidensis MR-1. J Basic Microbiol 43: 312-327.
63. Cavallaro G, Decaria L, Rosato A, (2008) Genome-based analysis of heme biosynthesis and uptake in prokaryotic systems. J Proteome Res 7: 4946-4954.
64. Wang LY, Brown L, Elliott M, Elliott T, (1997) Regulation of heme biosynthesis in Salmonella typhimurium: activity of glutamyl-tRNA reductase (HemA) is greatly elevated during heme limitation by a mechanism which increases abundance of the protein. J Bacteriol 179: 2907-2914.
65. Sanders C, Turkarslan S, Lee DW, Daldal F, (2010) Cytochrome c biogenesis: the Ccm system. Trends Microbiol 18: 266-274.
66. Sanders C, Turkarslan S, Lee DW, Onder O, Kranz RG, et al. (2008) The cytochrome c maturation components CcmF, CcmH, and CcmI form a membrane-integral multisubunit heme ligation complex. J Biol Chem 283: 29715-29722.
67. Shroff NP, Charania MA, Saffarini DA, (2010) ArcB1, a Homolog of Escherichia coli ArcB, Regulates Dimethyl Sulfoxide Reduction in Shewanella oneidensis MR-1. J Bacteriol 192: 3227-3230.
68. Orcutt BN, Sylvan JB, Knab NJ, Edwards KJ, (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75: 361-422.
69. Spiro S, Guest JR, (1990) FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev 6: 399-428.
70. Unden G, Bongaerts J, (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320: 217-234.