Genomic insights into the iron uptake mechanisms of the biomining microorganism Acidithiobacillus ferrooxidans

Journal of Industrial Microbiology and Biotechnology

Volumn 32, Issue 11-12, 2005, Pages 606-614

  Quatrini, Raquel ^a   Jedlicki, Eugenia ^b   Holmes, David S ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

Acidithiobacillus ferrooxidans; Bioleaching; Iron uptake, storage and homeostasis; Leptospirillum; Siderophore

Indexed keywords

AMINO ACID; COPPER; FERRIC ION; FERROUS ION; GOLD; IRON; MEMBRANE PROTEIN; SIDEROPHORE;

ACIDITHIOBACILLUS FERROOXIDANS; AMINO ACID SEQUENCE; BACTERIUM; BIOINFORMATICS; BIOLEACHING; BIOSYNTHESIS; CONFERENCE PAPER; GENE SEQUENCE; GENETIC ORGANIZATION; GENOMICS; HOMEOSTASIS; IRON STORAGE; IRON TRANSPORT; METAL RECOVERY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OXIDATION; PH; PROTEIN PROTEIN INTERACTION;

ACIDITHIOBACILLUS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HOMEOSTASIS; INDUSTRIAL MICROBIOLOGY; IRON; METALLURGY; SIDEROPHORES;

ACIDITHIOBACILLUS FERROOXIDANS; BACTERIA (MICROORGANISMS); LEPTOSPIRILLUM;

EID: 28644432715     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-005-0233-2     Document Type: Conference Paper

References (69)

1. Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215-237
2. Barreto M, Quatrini R, Bueno S, Arraigada C, Valdés J, Silver S, Jedlicki E, Holmes DS (2003) Aspects of the predicted physiology of Acidithiobacillus ferrooxidans deduced from an analysis of its partial genome sequence. Hydrometallurgy 71:97-105
3. Braun M, Killmann H, Braun V (1990) The β-barrel domain of FhuA 5-160 is sufficient for TonB-dependent FhuA activities of Escherichia coli. Mol Microbiol 33:1037-1049
4. Braun V (1995) Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol Rev 16:295-307
5. Braun V, Killmann H (1999) Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24:104-109
6. + -binding protein reveals convergent evolution within a superfamily. Nat Struct Biol 4:919-924
7. Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, Chakraborty R, van der Helm D, Deisenhofer J (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6:56-63
8. Cao Z, Qi Z, Sprencel C, Newton SM, Klebba PE (2000) Aromatic components of two ferric enterobactin binding sites in Escherichia coli FepA. Mol Microbiol 37:1306-1317
9. Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J, Sayavedra-Soto L, Arciero D, Hommes N, Whittaker M, Arp D (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759-2773
10. 2+ homeostasis and avoidance of metal toxicity. Mol Microbiol 44:561-571
11. Chamnongpol S, Dodson W, Cromie MJ, Harris ZL, Groisman EA (2002) Fe(III)-mediated cellular toxicity. Mol Microbiol 45:711-719
12. Chang C, Mooser A, Plückthun A, Wlodawer A (2001) Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J Biol Chem 276:27535-27540
13. Clarke TE, Ku SY, Dougan DR, Vogel HJ, Tari LW (2000) The structure of the ferric siderophore binding protein FhuD complexed with gallichrome. Nat Struct Biol 7:287-291
14. Clarke TE, Braun V, Winkelmann G, Tari LW, Vogel HJ (2002) X-ray crystallographic structures of the Escherichia coli periplasmic protein FhuD bound to hydroxamate-type siderophores and the antibiotic albomycin. J Biol Chem 277:13966-13972
15. Cornelis P, Matthijs S (2002) Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 4:787-798
16. Cornelissen CN, Sparling PF (1994) Iron piracy: acquisition of transferring-bound iron by bacterial pathogens. Mol Microbiol 14:843-850
17. Crosa JH (1997) Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol Mol Biol Rev 61:319-336
18. Eitinger T, Mandrand-Berthelot MA (2000) Nickel transport systems in microorganisms. Arch Microbiol 173:1-9
19. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220
20. Ferguson AD, Chakraborty R, Smith BS, E sser L, van der Helm D, Deisenhofer J (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719
21. Fontecave M, Coves J, Pierre JL (1994) Ferric reductases or flavin reductases?. Biometals 7:3-8
22. Genco CA, Dixon DW (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39:1-11
23. González-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, Amils R (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853-4865
24. Gunn JS, Miller SI (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178:6857-6864
25. Hantke K (1997) Ferrous iron uptake by a magnesium transport system is toxic for Escherichia coli and Salmonella typhimurium. J Bacteriol 179:6201-6204
26. Hantke K (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172-177
27. Hantke K, Braun V (2000) The art of keeping low and high iron concentrations in balance. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM, New York, pp 275-288
28. Higgs PI, Myers PS, Postle K (1998) Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J Bacteriol 180:6031-6038
29. Higgs PI, Larsen RA, Postle K (2002) Quantification of known components of the Escherichia coli TonB energy transducing system: TonB, ExbB, ExbD and FepA. Mol Microbiol 44:271-281
30. Hyytiainen H, Sjoblom S, Palomaki T, Tuikkala A, Tapio Palva E (2003) The PmrA-PmrB two-component system responding to acidic pH and iron controls virulence in the plant pathogen Erwinia carotovora ssp. carotovora. Mol Microbiol 50:795-807
31. Jiang X, Payne MA, Cao Z, Foster SB, Feix JB, Newton SC, Klebba PE (1997) Ligand-specific opening of a gated porin channel in the outer membrane of living bacteria. Science 276:1261-1264
32. Kammler M, Schon C, Hantke K (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175:6212-6219
33. Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobaciltus gen. nov., and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511-516
34. Köster W (2001) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 152:291-301
35. Larsen RA, Wood GE, Postle K (1993) The conserved proline-rich motif is not essential for energy transduction by Escherichia coli TonB protein. Mol Microbiol 10:943-953
36. Larsen RA, Letain TE, Postle K (2003) In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol Microbiol 49:211-218
37. Liu Z, Guiliani N, Appia-Ayme C, Borne F, Ratouchniak J, Bonnefoy V (2000) Construction and characterization of a recA mutant of Thiobacillus ferrooxidans by marker exchange mutagenesis. J Bacteriol 182:2269-2276
38. Locher P, Rees B, Koepnik R, Mitschler A, Moulinier L, Rosenbusch J, Moras D (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771-778
39. Mey AR, Payne SM (2001) Haem utilization in Vibrio cholerae involves multiple TonB-dependent haem receptors. Mol Microbiol 42:835-849
40. Mey AR, Wyckoff EE, Oglesby AG, Rab E, Taylor RK, Payne SM (2002) Identification of the Vibrio cholerae enterobactin receptors VctA and IrgA: IrgA is not required for virulence. Infect Immun 70:3419-3426
41. Moeck GS, Coulton JW (1998) TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 28:675-681
42. Newton SM, Allen JS, Cao Z, Qi Z, Jiang X, Sprencel C et al (1997) Double mutagenesis of a positive charge cluster in the ligand-binding site of the ferric enterobactin receptor, FepA. Proc Natl Acad Sci USA 94:4560-4565
43. Niermann WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen J, Heidelberg JF, Alley MRK, Ohta N, Maddock JR et al (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98:4136-4141
44. Norris PR, Barr DW, Hinson D (1988) Iron and mineral oxidation by acidophilic bacteria: affinities for iron and attachment to pyrite. In: Norris PR, Kelly DP (eds) Proceedings of the International Symposium. Kew: biohydrometallurgy, Science and Technology Letters, Kew, London, pp 43-59
45. Olson GJ, Brierley JA, Brierley CL (2003) Bioleaching review part B: progress in bioleaching: applications of microbial processes by the minerals industries. Appl Microbiol Biotechnol 63:249-257
46. Postle K (1993) TonB protein and energy transduction between membranes. J Bioenerg Biomembr 25:591-601
47. Pressler U, Staudenmaier H, Zimmermann L, Braun V (1988) Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol 170:2716-2724
48. Pronk JT, Liem K, Bos P, Kuenen JG (1991) Energy transduction by anaerobic ferric iron respiration in Thiobacillus ferrooxidans. Appl Environ Microbiol 57:2063-2068
49. Quatrini R, Lefimil C, Holmes DS, Jedlicki E (2005) The ferric iron uptake regulator (Fur) from the extreme acidophile Acidithiobacillus ferrooxidans. Microbiology 151:2005-2015
50. Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65-91
51. Rawlings DE, Tributsch H, Hansford GS (1999) Reasons why "Leptospirillum"-like species rather than Thiobacillus ferrooxidans are the dominant iron-oxidizing bacteria in many commercial processes for the biooxidation of pyrite and related ores. Microbiology 145:5-13
52. Rodionov DA, Dubchak I, Arkin A, Alm E, Gelfand MS (2004) Reconstruction of regulatory and metabolic pathways in metal-reducing-δ-proteobacteria. Genome Biol 5:R90
53. Rogers MB, Sexton JA, DeCastro GJ, Calderwood SB (2000) Identification of an operon required for ferrichrome iron utilization in Vibrio cholerae. J Bacteriol 182:2350-2353
54. Rohwerder T, Gehrke K, Kinzler K, Sand W (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239-248
55. Saravolac EG, Taylor NF, Benz R, Hancock RE (1991) Purification of glucose-inducible outer membrane protein OprB of Pseudomonas putida and reconstitution of glucose-specific pores. J Bacteriol 173:4970-4976
56. Selkov E, Overbeek R, Kogan Y, Chu L, Vonstein V, Holmes D, Silver S, Haselkorn R, Fonstein M (2000) Functional analysis of gapped microbial genomes: amino acid metabolism of Thiobacillus ferrooxidans. Proc Natl Acad Sci USA 97:3509-3514
57. Shouldice SR, Dougan DR, Skene RJ, Tari LW, McRee DE, Yu RH, Schryvers AB (2003) High resolution structure of an alternate form of the ferric ion binding protein from Haemophilus influenzae. J Biol Chem 278:11513-11519
58. Shouldice SR, Dougan DR, Williams PA, Skene RJ, Snell G, Scheibe D, Kirby S, Hosfield DJ, McRee DE, Schryvers AB, Tari LW (2003) Crystal structure of Pasteurella haemolytica ferric ion-binding protein A reveals a novel class of bacterial iron-binding proteins. J Biol Chem 278:41093-41098
59. Stoebner JA, Butterton JR, Calderwood SB, Payne SM (1992) Identification of the vibriobactin receptor of Vibrio cholerae. J Bacteriol 174:3270-3274
60. Touati D (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1-6
61. Tsolis RM, Baumler AJ, Heffron F, Stojiljkovic I (1996) Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse. Infect Immun 64:4549-4556
62. Valdés J, Jedlicki E, Holmes D (2003) Metabolic reconstruction of sulfur assimilation in the extremophile Acidithiobacillus ferrooxidans based on genome analysis. Biomed Cent Genomics 4:51-67
63. Velayudhan J, Hughes NJ, McColm AA, Bagshaw J, Clayton CL, Andrews SC, Kelly DJ (2000) Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol 37:274-286
64. Vian M, Creo C, Dalmastri C, Gionni A, Palazzolo P, Levi G (1986) Thiobacillus ferrooxidans selection in continuous culture. In: Lawrence RW, Branion RMR, Ebner RMR (eds) Fundamental and applied biohydrometallurgy. Elsevier, Amsterdam, pp 395-406
65. Winkelmann G (2002) Microbial siderophore-mediated transport. Biochem Soc Trans 30:691-696
66. Wosten MM, Groisman EA (1990) Molecular characterization of the PmrA regulon. J Biol Chem 274:27185-27190
67. Wylie JL, Worobec EA (1995) The OprB porin plays a central role in carbohydrate uptake in Pseudomonas aeruginosa. J Bacteriol 177:3021-3026
68. Wylie JL, Bernegger-Egli C, O'Neil JD, Worobec EA (1993) Biophysical characterization of OprB, a glucose-inducible porin of Pseudomonas aeruginosa. J Bioenerg Biomembr 25:547-556
69. Yue WW, Grizot S, Buchanan SK (2003) Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA. J Mol Biol 332:353-368