Regulation of high-affinity iron acquisition homologues in the tsetse fly symbiont Sodalis glossinidius

Journal of Bacteriology

Volumn 192, Issue 14, 2010, Pages 3780-3787

  Runyen Janecky, Laura J ^a   Brown, Alexandria N ^a   Ott, Brittany ^b   Tujuba, Haddis G ^a   Rio, Rita V M ^b  

^a UNIVERSITY OF RICHMOND   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC UPTAKE REGULATOR; FERROPORTIN; HEME; IRON; MANGANESE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE FUSION; HEMT BACTERIAL GENE; INTRACELLULAR BACTERIUM; INTRON; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SHIGELLA FLEXNERI; SITA BACTERIAL GENE; SODALIS GLOSSINIDIUS; SYMBIONT; TRANSCRIPTION REGULATION; TSETSE FLY;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; DNA, BACTERIAL; ENTEROBACTERIACEAE; GENE EXPRESSION REGULATION, BACTERIAL; IRON; MUTAGENESIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SYMBIOSIS; TSETSE FLIES;

BACTERIA (MICROORGANISMS); DIPTERA; ESCHERICHIA COLI; GLOSSINA (GENUS); GLOSSINIDAE; SHIGELLA FLEXNERI; SODALIS; SODALIS GLOSSINIDIUS;

EID: 77954407501     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00161-10     Document Type: Article

References (56)

1. Aksoy, S., X. Chen, and V. Hypsa. 1997. Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera:Glossinidae). Insect Mol. Biol. 6:183-190. (Pubitemid 27153125)
2. Attardo, G. M., C. Lohs, A. Heddi, U. H. Alam, S. Yildirim, and S. Aksoy. 2008. Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 54:1236-1242.
3. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006-2008.
4. Bearden, S. W., and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
5. Bearden, S. W., T. M. Staggs, and R. D. Perry. 1998. An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J. Bacteriol. 180:1135-1147.
6. Chao, T. C., A. Becker, J. Buhrmester, A. Puhler, and S. Weidner. 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.
7. Chen, Z., K. A. Lewis, R. K. Shultzaberger, I. G. Lyakhov, M. Zheng, B. Doan, G. Storz, and T. D. Schneider. 2007. Discovery of Fur binding site clusters in Escherichia coli by information theory models. Nucleic Acids Res. 35:6762-6777.
8. Cheng, Q., and S. Aksoy. 1999. Tissue trophism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol. Biol. 8:125-132.
9. Clarke, T. E., L. W. Tari, and H. J. Vogel. 2001. Structural biology of bacterial iron uptake systems. Curr. Top. Med. Chem. 1:7-30.
10. Crosa, J. H., A. R. Mey, and S. M. Payne (ed.). 2004. Iron transport in bacteria. ASM Press, Washington, DC.
11. Dale, C., G. R. Plague, B. Wang, H. Ochman, and N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 99:12397-12402.
12. Dale, C., and S. C. Welburn. 2001. The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol. 31:628-631.
13. Dale, C., S. A. Young, D. T. Haydon, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. U. S. A. 98:1883-1888.
14. Darby, A. C., J. Lagnel, C. Z. Matthew, K. Bourtzis, I. Maudlin, and S. C. Welburn. 2005. Extrachromosomal DNA of the symbiont Sodalis glossinidius. J. Bacteriol. 187:5003-5007.
15. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
16. Davanloo, P., A. H. Rosenberg, J. J. Dunn, and F. W. Studier. 1984. Cloning and expression of the gene for bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 81:2035-2039.
17. Denlinger, D. L., and W. C. Ma. 1974. Dynamics of the pregnancy cycle in the tsetse Glossina morsitans. J. Insect Physiol. 20:1015-1026.
18. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229. (Pubitemid 29512928)
19. Forman, S., J. T. Paulley, J. D. Fetherston, Y. Q. Cheng, and R. D. Perry. 2010. Yersinia ironomics: comparison of iron transporters among Yersinia pestis biotypes and its nearest neighbor, Yersinia pseudotuberculosis. Biometals 23:275-294.
20. Hantke, K. 1987. Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol. Gen. Genet. 210:135-139.
21. Janakiraman, A., and J. M. Slauch. 2000. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146-1155.
22. Kabayo, J. P., M. E. Ruhm, H. F. Barnor, and E. Zeiller. 1988. Studies on the absorption of ingested haemoglobin-iron in Glossina. Int. J. Rad. Appl. Instrum. A 39:207-211.
23. Kitphati, W., P. Ngok-Ngam, S. Suwanmaneerat, R. Sukchawalit, and S. Mongkolsuk. 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.
24. Locke, M., and H. Nichol. 1992. Iron economy in insects: transport, metabolism, and storage. Annu. Rev. Entomol. 37:195-215.
25. Matthew, C. Z., A. C. Darby, S. A. Young, L. H. Hume, and S. C. Welburn. 2005. The rapid isolation and growth dynamics of the tsetse symbiont Sodalis glossinidius. FEMS Microbiol. Lett. 248:69-74.
26. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Milligan, P. J., I. Maudlin, and S. C. Welburn. 1995. Trypanozoon: infectivity to humans is linked to reduced transmissibility in tsetse. II. Genetic mechanisms. Exp. Parasitol. 81:409-415.
28. Moloo, S. K. 1971. An artificial feeding technique for Glossina. Parasitology 63:507-512.
29. Moran, N. A., and G. R. Plague. 2004. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14:627-633.
30. Munch, R., K. Hiller, A. Grote, M. Scheer, J. Klein, M. Schobert, and D. Jahn. 2005. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187-4189.
31. Payne, S. M., E. E. Wyckoff, E. R. Murphy, A. G. Oglesby, M. L. Boulette, and N. M. Davies. 2006. Iron and pathogenesis of Shigella: iron acquisition in the intracellular environment. Biometals 19:173-180.
32. Pinnock, D. E., and R. T. Hess. 1974. The occurrence of intracellular rickettsia-like organisms in the tsetse flies, Glossina morsitans, G. fuscipes, G. brevipalpis and G. pallidipes. Acta Trop. 31:70-79.
33. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
34. Reigstad, C. S., S. J. Hultgren, and J. I. Gordon. 2007. Functional genomic studies of uropathogenic Escherichia coli and host urothelial cells when intracellular bacterial communities are assembled. J. Biol. Chem. 282:21259-21267.
35. Rio, R. V., Y. N. Wu, G. Filardo, and S. Aksoy. 2006. Dynamics of multiple symbiont density regulation during host development: tsetse fly and its microbial flora. Proc. Biol. Sci. 273:805-814.
36. Rogers, H. J. 1973. Iron-binding catechols and virulence in Escherichia coli. Infect. Immun. 7:438-444.
37. Runyen-Janecky, L. J., E. Dazenski, S. Hawkins, and L. Warner. 2006. Role and regulation of the Shigella flexneri Sit and MntH systems. Infect. Immun. 74:4666-4672.
38. Runyen-Janecky, L. J., and S. M. Payne. 2002. Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect. Immun. 70:4379-4388.
39. Runyen-Janecky, L. J., S. A. Reeves, E. G. Gonzales, and S. M. Payne. 2003. Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect. Immun. 71:1919-1928.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Shaw, M. K., and S. K. Moloo. 1991. Comparative study on Rickettsia-like organisms in the midgut epithelial cells of different Glossina species. Parasitology 102:193-199.
42. Stojiljkovic, I., A. J. Baumler, and K. Hantke. 1994. Fur regulon in gramnegative bacteria: identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay. J. Mol. Biol. 236:531-545.
43. Stojiljkovic, I., and K. Hantke. 1994. Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding- proteindependent transport system in Yersinia enterocolitica. Mol. Microbiol. 13:719-732.
44. Thompson, J. M., H. A. Jones, and R. D. Perry. 1999. Molecular characterization of the hemin uptake locus (hmu) from Yersinia pestis and analysis of hmu mutants for hemin and hemoprotein utilization. Infect. Immun. 67:3879-3892.
45. Toh, H., B. L. Weiss, S. A. Perkin, A. Yamashita, K. Oshima, M. Hattori, and S. Aksoy. 2006. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 16:149-156.
46. Torres, A. G., and S. M. Payne. 1997. Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol. Microbiol. 23:825-833.
47. Torres, A. G., P. Redford, R. A. Welch, and S. M. Payne. 2001. TonBdependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect. Immun. 69:6179-6185.
48. Touati, D. 2000. Iron and oxidative stress in bacteria. Arch. Biochem. Biophys. 373:1-6.
49. Weiss, B. L., R. Mouchotte, R. V. Rio, Y. N. Wu, Z. Wu, A. Heddi, and S. Aksoy. 2006. Interspecific transfer of bacterial endosymbionts between tsetse fly species: infection establishment and effect on host fitness. Appl. Environ. Microbiol. 72:7013-7021.
50. Weiss, B. L., Y. Wu, J. J. Schwank, N. S. Tolwinski, and S. Aksoy. 2008. An insect symbiosis is influenced by bacterium-specific polymorphisms in outermembrane protein A. Proc. Natl. Acad. Sci. U. S. A. 105:15088-15093.
51. Welburn, S. C., and I. Maudlin. 1987. A simple in vitro method for infecting tsetse with trypanosomes. Ann. Trop. Med. Parasitol. 81:453-455.
52. Weyda, F., T. Soldan, and V. Matha. 1995. Rickettsia-like organisms in the tsetse fly Glossina palpalis palpalis. Cytobios 81:223-228.
53. Wyckoff, E. E., D. Duncan, A. G. Torres, M. Mills, K. Maase, and S. M. Payne. 1998. Structure of the Shigella dysenteriae haem transport locus and its phylogenetic distribution in enteric bacteria. Mol. Microbiol. 28:1139-1152.
54. Zhou, D., W. D. Hardt, and J. E. Galan. 1999. Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect. Immun. 67:1974-1981.
55. Zhou, D., L. Qin, Y. Han, J. Qiu, Z. Chen, B. Li, Y. Song, J. Wang, Z. Guo, J. Zhai, Z. Du, X. Wang, and R. Yang. 2006. Global analysis of iron assimilation and fur regulation in Yersinia pestis. FEMS Microbiol. Lett. 258:9-17.
56. Zhou, G., P. Kohlhepp, D. Geiser, C. Frasquillo Mdel, L. Vazquez-Moreno, and J. J. Winzerling. 2007. Fate of blood meal iron in mosquitoes. J. Insect Physiol. 53:1169-1178.