The iron stimulon and fur regulon of Geobacter sulfurreducens and their role in energy metabolism

Applied and Environmental Microbiology

Volumn 80, Issue 9, 2014, Pages 2918-2927

  Embree, Mallory ^a   Qiu, Yu ^a   Shieu, Wendy ^a   Nagarajan, Harish ^a   O'Neil, Regina ^b   Lovley, Derek ^b   Zengler, Karsten ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOLISM; PHYSIOLOGY; PROTEINS; TRANSCRIPTION;

ANAEROBIC RESPIRATION; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION STUDIES; GEOBACTER SULFURREDUCENS; TRANSCRIPTIONAL ANALYSIS; TRANSCRIPTIONAL LEVELS; TRANSCRIPTIONAL REGULATOR; TRANSCRIPTIONAL REGULATORY NETWORKS;

IRON;

BACTERIAL PROTEIN; IRON;

ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; GEOBACTER; METABOLISM; REGULON;

BACTERIAL PROTEINS; ENERGY METABOLISM; GENE EXPRESSION REGULATION, BACTERIAL; GEOBACTER; IRON; REGULON;

EID: 84898620711     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03916-13     Document Type: Article

References (50)

1. Escolar L, Perez-Martin J, de Lorenzo V. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181: 6223-6229.
2. Caccavo F, Jr, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ. 1994. Geobacter sulfurreducens sp. nov., a hydrogen-and acetateoxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60:3752-3759.
3. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S. 1993. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159:336-344. http://dx.doi.org/10.1007/BF00290916.
4. Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim B-C, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR. 2011. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6:573-579. http://dx.doi.org/10.1038/nnano.2011.119.
5. Lovley DR. 1991. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55:259-287.
6. Bell PE, Mills AL, Herman JS. 1987. Biogeochemical conditions favoring magnetite formation during anaerobic iron reduction. Appl. Environ. Microbiol. 53:2610-2616.
7. De Lorenzo V, Herrero M, Giovannini F, Neilands JB. 1988. Fur (ferric uptake regulation) protein and CAP (catabolite-activator protein) modulate transcription of Fur gene in Escherichia coli. Eur. J. Biochem. 173: 537-546. http://dx.doi.org/10.1111/j.1432-1033.1988.tb14032.x.
8. Danielli A, Roncarati D, Delany I, Chiarini V, Rappuoli R, Scarlato V.2006. In vivo dissection of the Helicobacter pylori Fur regulatory circuit by genome-wide location analysis. J. Bacteriol. 188:4654-4662. http://dx.doi.org/10.1128/JB.00120-06.
9. Jackson LA, Ducey TF, Day MW, Zaitshik JB, Orvis J, Dyer DW. 2010. Transcriptional and functional analysis of the Neisseria gonorrhoeae Fur regulon. J. Bacteriol. 192:77-85. http://dx.doi.org/10.1128/JB.00741-09.
10. Ollinger J, Song K-B, Antelmann H, Hecker M, Helmann JD. 2006. Role of the fur regulon in iron transport in Bacillus subtilis. J. Bacteriol. 188: 3664-3673. http://dx.doi.org/10.1128/JB.188.10.3664-3673.2006.
11. Stojiljkovic I, Bäumler AJ, Hantke K. 1994. Fur regulon in gram-negative bacteria: identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay. J. Mol. Biol. 236:531-545. http://dx.doi.org/10.1006/jmbi.1994.1163.
12. Lavrrar JL, McIntosh MA. 2003. Architecture of a Fur binding site: a comparative analysis. J. Bacteriol. 185:2194-2202. http://dx.doi.org/10.1128/JB.185.7.2194-2202.2003.
13. Coppi MV, Leang C, Sandler SJ, Lovley DR. 2001. Development of a genetic system for Geobacter sulfurreducens. Appl. Environ. Microbiol. 67:3180-3187. http://dx.doi.org/10.1128/AEM.67.7.3180-3187.2001.
14. Lloyd JR, Leang C, Hodges Myerson AL, Coppi MV, Cuifo S, Methe B, Sandler SJ, Lovley DR. 2003. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369:153-161. http://dx.doi.org/10.1042/BJ20020597.
15. Lovley DR, Phillips EJP. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
16. Cho B-K, Knight EM, Barrett CL, Palsson BØ. 2008. Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res. 18:900-910. http://dx.doi.org/10.1101/gr.070276.107.
17. Cho B-K, Knight EM, Palsson BØ. 2008. Genomewide identification of protein binding locations using chromatin immunoprecipitation coupled with microarray. Methods Mol. Biol. 439:131-145. http://dx.doi.org/10.1007/978-1-59745-188-8_9.
18. Cho B-K, Zengler K, Qiu Y, Park YS, Knight EM, Barrett CL, Gao Y, Palsson BO. 2009. The transcription unit architecture of the Escherichia coli genome. Nat. Biotechnol. 27:1043-1049. http://dx.doi.org/10.1038/nbt.1582.
19. Mao F, Dam P, Chou J, Olman V, Xu Y. 2009. DOOR: a database for prokaryotic operons. Nucleic Acids Res. 37:D459-D463. http://dx.doi.org/10.1093/nar/gkn757.
20. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 37:W202-W208. http://dx.doi.org/10.1093/nar/gkp335.
21. Grant CE, Bailey TL, Noble WS. 16 February 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btr064.
22. Gupta S, Stamatoyannopoulos J, Bailey T, Noble W. 2007. Quantifying similarity between motifs. Genome Biol. 8:R24. http://dx.doi.org/10.1186/gb-2007-8-2-r24.
23. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264. http://dx.doi.org/10.1093/biostatistics/4.2.249.
24. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A. 2009. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res. 37:e123. http://dx.doi.org/10.1093/nar/gkp596.
25. Zhong S, Joung J-G, Zheng Y, Chen Y-r, Liu B, Shao Y, Xiang JZ, Fei Z, Giovannoni JJ. 2011. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011:940-949. http://dx.doi.org/10.1101/pdb.prot5652.
26. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A. 2010. Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Methods 7:709-715. http://dx.doi.org/10.1038/nmeth.1491.
27. Langmead B, Trapnell C, Pop M, Salzberg S. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
28. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28:511-515. http://dx.doi.org/10.1038/nbt.1621.
29. Qiu Y, Cho BK, Park YS, Lovley D, Palsson BØ, Zengler K. 2010. Structural and operational complexity of the Geobacter sulfurreducens genome. Genome Res. 20:1304-1311. http://dx.doi.org/10.1101/gr.107540.110.
30. Inoue K, Qian X, Morgado L, Kim B-C, Mester T, Izallalen M, Salgueiro CA, Lovley DR. 2010. Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 76:3999-4007. http://dx.doi.org/10.1128/AEM.00027-10.
31. Yang Y, Harris D, Luo F, Wu L, Parsons A, Palumbo A, Zhou J. 2008. Characterization of the Shewanella oneidensis Fur gene: roles in iron and acid tolerance response. BMCGenomics 9(Suppl 1):S11. http://dx.doi.org/10.1186/1471-2164-9-S1-S11.
32. Butcher BG, Bronstein PA, Myers CR, Stodghill PV, Bolton JJ, Markel EJ, Filiatrault MJ, Swingle B, Gaballa A, Helmann JD, Schneider DJ, Cartinhour SW. 2011. Characterization of the Fur regulon in Pseudomonas syringae pv. tomato DC3000. J. Bacteriol. 193:4598-4611. http://dx.doi.org/10.1128/JB.00340-11.
33. Cartron M, Maddocks S, Gillingham P, Craven C, Andrews S. 2006. Feo-transport of ferrous iron into bacteria. Biometals 19:143-157. http://dx.doi.org/10.1007/s10534-006-0003-2.
34. Hantke K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4:172-177. http://dx.doi.org/10.1016/S1369-5274(00)00184-3.
35. Bender KS, Yen H-CB, Hemme CL, Yang Z, He Z, He Q, Zhou J, Huang KH, Alm EJ, Hazen TC, Arkin AP, Wall JD. 2007. Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl. Environ. Microbiol. 73:5389-5400. http://dx.doi.org/10.1128/AEM.00276-07.
36. Ledala N, Sengupta M, Muthaiyan A, Wilkinson BJ, Jayaswal RK. 2010. Transcriptomic response of Listeria monocytogenes to iron limitation and fur mutation. Appl. Environ. Microbiol. 76:406-416. http://dx.doi.org/10.1128/AEM.01389-09.
37. Wan X-F, VerBerkmoes NC, McCue LA, Stanek D, Connelly H, Hauser LJ, Wu L, Liu X, Yan T, Leaphart A, Hettich RL, Zhou J, Thompson DK. 2004. Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J. Bacteriol. 186:8385-8400. http://dx.doi.org/10.1128/JB.186.24.8385-8400.2004.
38. Nandal A, Huggins CCO, Woodhall MR, McHugh J, Rodríguez-Quiñones F, Quail MA, Guest JR, Andrews SC. 2010. Induction of the ferritin gene (ftnA) of Escherichia coli by Fe2+-Fur is mediated by reversal of H-NS silencing and is RyhB independent. Mol. Microbiol. 75:637-657. http://dx.doi.org/10.1111/j.1365-2958.2009.06977.x.
39. 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. http://dx.doi.org/10.1111/j.1365-2958.2004.04030.x.
40. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I. 2002. IdeR, an essential gene in Mycobacterium tuberculosis: role of IdeR in irondependent gene expression, iron metabolism, and oxidative stress response. Infect. Immun. 70:3371-3381. http://dx.doi.org/10.1128/IAI.70.7.3371-3381.2002.
41. Andrews SC, Robinson AK, Rodríguez-Quiñones F. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237. http://dx.doi.org/10.1016/S0168-6445(03)00055-X.
42. Touati D. 2000. Iron and oxidative stress in bacteria. Arch. Biochem. Biophys. 373:1-6. http://dx.doi.org/10.1006/abbi.1999.1518.
43. Dubrac S, Touati D. 2000. Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter. J. Bacteriol. 182:3802-3808. http://dx.doi.org/10.1128/JB.182.13.3802-3808.2000.
44. Mey AR, Wyckoff EE, Kanukurthy V, Fisher CR, Payne SM. 2005. Iron and Fur regulation in Vibrio cholerae and the role of Fur in virulence. Infect. Immun. 73:8167-8178. http://dx.doi.org/10.1128/IAI.73.12.8167-8178.2005.
45. Lee H-J, Bang SH, Lee K-H, Park S-J. 2007. Positive regulation of Fur gene expression via direct interaction of Fur in a pathogenic bacterium, Vibrio vulnificus. J. Bacteriol. 189:2629-2636. http://dx.doi.org/10.1128/JB.01791-06.
46. Massé E, Salvail H, Desnoyers G, Arguin M. 2007. Small RNAs controlling iron metabolism. Curr. Opin. Microbiol. 10:140-145. http://dx.doi.org/10.1016/j.mib.2007.03.013.
47. Africa LAA, Murphy ER, Egan NR, Wigley AF, Wing HJ. 2011. The Iron-responsive Fur/RyhB regulatory cascade modulates the Shigella outer membrane protease IcsP. Infect. Immun. 79:4543-4549. http://dx.doi.org/10.1128/IAI.05340-11.
48. Massé E, Vanderpool CK, Gottesman S. 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 187:6962-6971. http://dx.doi.org/10.1128/JB.187.20.6962-6971.2005.
49. Methé BA, Webster J, Nevin K, Butler J, Lovley DR. 2005. DNA microarray analysis of nitrogen fixation and Fe(III) reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71:2530-2538. http://dx.doi.org/10.1128/AEM.71.5.2530-2538.2005.
50. Delany I, Ieva R, Soragni A, Hilleringmann M, Rappuoli R, Scarlato V. 2005. In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J. Bacteriol. 187:7703-7715. http://dx.doi.org/10.1128/JB.187.22.7703-7715.2005.