Characterization of the achromobactin iron acquisition operon in Sodalis glossinidius

Applied and Environmental Microbiology

Volumn 79, Issue 9, 2013, Pages 2872-2881

  Smith, Caitlin L ^a   Weiss, Brian L ^b   Aksoy, Serap ^b   Runyen Janecky, Laura J ^a  

^a UNIVERSITY OF RICHMOND   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS GENES; IRON ACQUISITION; REVERSE TRANSCRIPTION; SIDEROPHORE PRODUCTION; SIDEROPHORE SYNTHESIS; SIDEROPHORE TRANSPORT; TITRATION ASSAYS; TRANSCRIPTIONAL REPRESSORS;

BIOCHEMISTRY; ESCHERICHIA COLI; HISTOLOGY; MERGERS AND ACQUISITIONS; PROTEINS; TISSUE; TRANSCRIPTION;

IRON;

FECAL COLIFORM; FLY; GENE EXPRESSION; GROWTH RATE; INOCULATION; IRON; MUTATION; PROTEIN; SIDEROPHORE; SYMBIONT;

ESCHERICHIA COLI; GLOSSINA (GENUS); GLOSSINIDAE; HEXAPODA; SODALIS; SODALIS GLOSSINIDIUS;

2 OXOGLUTARIC ACID; ACHROMOBACTIN; BACTERIAL PROTEIN; CITRIC ACID; HYBRID PROTEIN; IRON; PROTEIN BINDING; SIDEROPHORE;

ANIMAL; BINDING SITE; ENTEROBACTERIACEAE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLOSSINIDAE; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; OPERON; PHYSIOLOGY; PROMOTER REGION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; BIOLOGICAL TRANSPORT; CITRATES; ENTEROBACTERIACEAE; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; IRON; KETOGLUTARIC ACIDS; MALE; MOLECULAR SEQUENCE DATA; MUTATION; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SIDEROPHORES; TSETSE FLIES;

EID: 84876323451     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03959-12     Document Type: Article

References (44)

1. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42:165-190
2. Aksoy S. 2000. Tsetse-a haven for microorganisms. Parasitol. Today 16:114-118
3. Attardo GM, Lohs C, Heddi A, Alam UH, Yildirim S, Aksoy S. 2008. Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 54:1236-1242
4. Denlinger D, Ma W. 1974. Dynamics of the pregnancy cycle in the tsetse Glossina morsitans. J. Insect Physiol. 20:1015-1026
5. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402-407
6. Cheng Q, Aksoy S. 1999. Tissue trophism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol. Biol. 8:125-132
7. Pinnock DE, Hess RT. 1974. The occurrence of intracellular rickettsialike organisms in the tsetse flies, Glossina morsitans, G. fuscipes, G. brevipalpis and G. pallidipes. Acta Trop. 31:70-79
8. Shaw MK, Moloo SK. 1991. Comparative study on Rickettsia-like organisms in the midgut epithelial cells of different Glossina species. Parasitology 102:193-199
9. Weyda F, Soldan T, Matha V. 1995. Rickettsia-like organisms in the tsetse fly Glossina palpalis palpalis. Cytobios 81:223-228
10. Dale C, Welburn SC. 2001. The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol. 31:628-631
11. Kabayo JP, Ruhm ME, Barnor HF, Zeiller E. 1988. Studies on the absorption of ingested haemoglobin-iron in Glossina. Int. J. Rad. Appl. Instrum. A39:207-211
12. Locke M, Nichol H. 1992. Iron economy in insects: transport, metabolism, and storage. Annu. Rev. Entomol. 37:195-215
13. Zhou G, Kohlhepp P, Geiser D, del Carmen Frasquillo M, Vazquez-Moreno L, Winzerling JJ. 2007. Fate of blood meal iron in mosquitoes. J. Insect Physiol. 53:1169-1178
14. Runyen-Janecky LJ, Brown AN, Ott B, Tujuba HG, Rio RV. 2010. Regulation of high-affinity iron acquisition homologues in the tsetse fly symbiont, Sodalis glossinidius. J. Bacteriol. 192:3780-3787
15. Darby AC, Lagnel J, Matthew CZ, Bourtzis K, Maudlin I, Welburn SC. 2005. ExtrachromosomalDNAof the symbiont Sodalis glossinidius. J. Bacteriol. 187:5003-5007
16. Miethke M, Marahiel MA. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71:413-451
17. Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, Hattori M, Aksoy S. 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
18. Escolar L, Perez-Martin J, de Lorenzo V. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229
19. Rogers HJ. 1973. Iron-binding catechols and virulence in Escherichia coli. Infect. Immun. 7:438-444
20. Moloo SK. 1971. An artificial feeding technique for Glossina. Parasitology 63:507-512
21. Weiss BL, Maltz M, Aksoy S. 2012. Obligate symbionts activate immune system development in the tsetse fly. J. Immunol. 188:3395-3403
22. Munch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D. 2005. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187-4189
23. Weiss BL, Wu Y, Schwank JJ, Tolwinski NS, Aksoy S. 2008. An insect symbiosis is influenced by bacterium-specific polymorphisms in outermembrane protein A. Proc. Natl. Acad. Sci. U. S. A. 105:15088-15093
24. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156
25. Runyen-Janecky LJ, Payne SM. 2002. Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect. Immun. 70:4379-4388
26. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Dale C, Young SA, Haydon DT, Welburn SC. 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
28. Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56
29. Maltz MA, Weiss BL, O'Neill M, Wu Y, Aksoy S. 2012. OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Appl. Environ. Microbiol. 78:7760-7768
30. Stojiljkovic I, Baumler 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
31. Berti AD, Thomas MG. 2009. Analysis of achromobactin biosynthesis by Pseudomonas syringae pv. Syringae B728a. J. Bacteriol. 191:4594-4604
32. Schmelz S, Kadi N, McMahon SA, Song L, Oves-Costales D, Oke M, Liu H, Johnson KA, Carter LG, Botting CH, White MF, Challis GL, Naismith JH. 2009. AcsD catalyses enantioselective citrate desymmetryzation in siderophore biosynthesis. Nat. Chem. Biol. 5:174-182
33. Franza T, Mahe B, Expert D. 2005. Erwinia chrysanthemi requires a second iron transport route dependent on the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55:261-275
34. Dellagi A, Segond D, Rigault M, Fargard M, Simon C, Saindrenan P, Expert D. 2009. Microbial siderophores exert a subtle role in Arabidopsis during infection by manipulating the immune response and the iron status. Plant Physiol. 150:1687-1696
35. Ciche TA, Bintrim SB, Horswill AR, Ensign JC. 2001. A phosphopantetheinyl transferase homolog is essential for Photorhabdus luminescens to support growth and reproduction of the entomopathogenic nematode Heterorhabditis bacteriophora. J. Bacteriol. 183:3117-3126
36. Brickman TJ, Armstrong SK. 1995. Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants. J. Bacteriol. 177:268-270
37. Hassett DJ, Sokol PA, Howell ML, Ma JF, Schweizer HT, Ochsner U, Vasil ML. 1996. Ferric uptake regulator (Fur) mutants of Pseudomonas aeruginosa demonstrate defective siderophore-mediated iron uptake, altered aerobic growth, and decreased superoxide dismutase and catalase activities. J. Bacteriol. 178:3996-4003
38. Horsburgh MJ, Ingham E, Foster SJ. 2001. In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J. Bacteriol. 183:468-475
39. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. 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
41. Datsenko KA, Wanner BL. 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
42. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006-2008
43. Davanloo P, Rosenberg AH, Dunn JJ, Studier FW. 1984. Cloning and expression of the gene for bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 81:2035-2039
44. Short JM, Fernandez JM, Sorge JA, Huse WD. 1988. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties. Nucleic Acids Res. 16:7583-7600