The hydroxamate siderophore rhequichelin is required for virulence of the pathogenic actinomycete Rhodococcus equi

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4106-4114

  Miranda CasoLuengo, Raúl ^a   Coulson, Garry B ^b   Miranda CasoLuengo, Aleksandra ^a   Vázquez Boland, José A ^c,d   Hondalus, Mary K ^b   Meijer, Wim G ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF LEÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2,2' BIPYRIDINE; BIPYRIDINE; NONRIBOSOMAL PEPTIDE SYNTHETASE; RHEQUICHELIN; SERINE; SIDEROPHORE; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ACTINOMYCETALES INFECTION; ACTINOMYCETE RHODOCOCCUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME MODIFICATION; GENE DELETION; GENE STRUCTURE; GENETIC TRANSDUCTION; LUNG INFECTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; BACTERIAL PROTEINS; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HYDROXAMIC ACIDS; IRON; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, SCID; OLIGOPEPTIDES; PEPTIDE SYNTHASES; RHODOCOCCUS EQUI; SIDEROPHORES; VIRULENCE; VIRULENCE FACTORS;

EID: 84870819639     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00678-12     Document Type: Article

References (53)

1. Andrews SC, Robinson AK, Rodriguez-Quinones F. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
2. Barton MD, Hughes KL. 1984. Ecology of Rhodococcus equi. Vet. Micro-biol. 9:65-76.
3. Bell KS, Philp JC, Aw DWJ, Christofi N. 1998. The genus Rhodococcus. J. Appl. Microbiol. 85:195-210.
4. Bosello M, Robbel L, Linne U, Xie X, Marahiel MA. 2011. Biosynthesis of the siderophore rhodochelin requires the coordinated expression of three independent gene clusters in Rhodococcus jostii RHA1. J. Am. Chem. Soc. 133:4587-4595.
5. Brock JH, Williams PH, Liceaga J, Wooldridge KG. 1991. Relative availability of transferrin-bound iron and cell-derived iron to aerobactin-producing and enterochelin-producing strains of Escherichia coli and to other microorganisms. Infect. Immun. 59:3185-3190.
6. Butcher PD, Mangan JA, Monahan IM. 1998. Intracellular gene expression. Analysis of RNA from mycobacteria in macrophages using RT-PCR. Methods Mol. Biol. 101:285-306.
7. Carrano CJ, Jordan M, Drechsel H, Schmid DG, Winkelmann G. 2001. Heterobactins: a new class of siderophores from Rhodococcus erythropolis IGTS8 containing both hydroxamate and catecholate donor groups. Bio-metals 14:119-125.
8. Cendrowski S, MacArthur W, Hanna P. 2004. Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol. Microbiol. 51:407-417.
9. Challis GL. 2005. A widely distributed bacterial pathway for siderophore biosynthesisindependentofnonribosomalpeptidesynthetases. Chembio-chem 6:601-611.
10. Challis GL, Ravel J, Townsend CA. 2000. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 7:211-224.
11. Conti E, Stachelhaus T, Marahiel MA, Brick P. 1997. Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J. 16:4174-4183.
12. Crosa JH, Walsh CT. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol. Mol. Biol. Rev. 66:223-249.
13. De Voss JJ, et al. 2000. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. U. S. A. 97:1252-1257.
14. Dhungana S, et al. 2007. Purification and characterization of rhodobac-tin:a mixed ligand siderophore from Rhodococcus rhodochrousstrain OFS. Biometals 20:853-867.
15. Felnagle EA, et al. 2010. MbtH-like proteins as integral components of bacterial nonribosomal peptide synthetases. Biochemistry 49:8815-8817.
16. Fernandez-Mora E, Polidori M, Lührmann A, Schaible UE, Haas A. 2005. Maturation ofRhodococcus equi-containing vacuolesisarrested after completion of the early endosome stage. Traffic 6:635-653.
17. Garcia EC, Brumbaugh AR, Mobley HL. 2011. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect. Immun. 79:1225-1235.
18. Giguère S, et al. 1999. Role of the 85-kilobase plasmid and plasmid-encoded virulence-associated protein A in intracellular survival and virulence of Rhodococcus equi. Infect. Immun. 67:3548-3557.
19. Hondalus MK, Mosser DM. 1994. Survival and replication of Rhodococ-cus equi in macrophages. Infect. Immun. 62:4167-4175.
20. Hughes KL, Sulaiman I. 1987. The ecology of Rhodococcus equi and physicochemical influences on growth. Vet. Microbiol. 14:241-250.
21. Jain S, Bloom BR, Hondalus MK. 2003. Deletion of vapA encoding virulence associated protein A attenuates the intracellular actinomycete Rhodococcus equi. Mol. Microbiol. 50:115-128.
22. Kelly BG, Wall DW, Boland CA, Meijer WG. 2002. Isocitrate lyase of the facultative intracellular pathogen Rhodococcus equi. Microbiology 148: 793-798.
23. Köster W. 2001. ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res. Microbiol. 152:291-301.
24. Letek M, et al. 2010. The genome of a pathogenic rhodococcus: cooptive virulence underpinned by key gene acquisitions. PLoS Genet. 6:e1001145. doi:10.1371/journal.pgen.1001145.
25. Lin H, Fischbach MA, Liu DR, Walsh CT. 2005. In vitro characterization of salmochelin and enterobactin trilactone hydrolases IroD, IroE, and Fes. J. Am. Chem. Soc. 127:11075-11084.
26. Lührmann A, et al. 2004. Necrotic death of Rhodococcus equi-infected macrophages is regulated by virulence-associated plasmids. Infect. Im-mun. 72:853-862.
27. Mangan MW, Meijer WG. 2001. Random insertion mutagenesis of the intracellular pathogen Rhodococcus equi using transposomes. FEMS Mi-crobiol. Lett. 205:243-246.
28. Mies KA, Wirgau JI, Crumbliss AL. 2006. Ternary complex formation facilitatesaredox mechanism for iron release from a siderophore. Biomet-als 19:115-126.
29. Miranda-Casoluengo R, et al. 2005. The iron-regulated iupABC operon is required for saprophytic growth of the intracellular pathogenRhodococcus equi at low iron concentrations. J. Bacteriol. 187:3438-3444.
30. Miranda-Casoluengo R, Prescott JF, Vazquez-Boland JA, Meijer WG. 2008. The intracellular pathogen Rhodococcus equi produces a catecholate siderophore required for saprophytic growth. J.Bacteriol. 190:1631-1637.
31. Muscatello G, et al. 2007. Rhodococcus equi infection in foals: the science of 'rattles'. Equine Vet. J. 39:470-478.
32. Nagy I, et al. 1995. Degradation of the thiocarbamate herbicide EPTC (S-ethyl dipropylcarbamothioate) and biosafening by Rhodococcus sp. strain NI86/21 involve an inducible cytochrome P-450 system and aldehyde dehydrogenase. J. Bacteriol. 177:676-687
33. Neilands JB. 1981. Microbial iron compounds. Annu. Rev. Biochem. 50:715-731.
34. Perry RD, Balbo PB, Jones HA, Fetherston JD, DeMoll E. 1999. Yers-iniabactin from Yersinia pestis: biochemical characterization ofthe sidero-phore and its role in iron transport and regulation. Microbiology 145: 1181-1190.
35. Ratledge C. 2007. Iron metabolism and infection. Food Nutr. Bull. 28: S515-S523.
36. Rausch C, Weber T, Kohlbacher O, Wohlleben W, Huson DH. 2005. Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res. 33:5799-5808.
37. Rohde KH, Abramovitch RB, Russell DG. 2007. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2:352-364.
38. Röttig M, et al. 2011. NRPSpredictor2-a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 39:W362-W367.
39. Russell DA, Byrne GA, O'Connell EP, Boland CA, Meijer WG. 2004. The LysR-type transcriptional regulator VirR is required for expression of the virulence gene vapA of Rhodococcus equi ATCC 33701. J. Bacteriol. 186:5576-5584.
40. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Takai S, et al. 1991. Association between a large plasmid and 15- to 17-kilodalton antigens in virulent Rhodococcus equi. Infect. Immun. 59: 4056-4060.
42. Takase H, Nitanai H, Hoshino K, Otani T. 2000. Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68:1834-1839.
43. Toyooka K, Takai S, Kirikae T. 2005. Rhodococcus equi can survive a phagolysosomal environment in macrophages by suppressing acidification of the phagolysosome. J. Med. Microbiol. 54:1007-1015.
44. van der Geize R, JW de Hessels GI, Grommen AW, Jacobs AA, Dijkhui-zen L. 2008. A novel method to generate unmarked gene deletions in the intracellular pathogen Rhodococcus equi using 5-fluorocytosine conditional lethality. Nucleic Acids Res. 36:e151.
45. van der Geize R, Dijkhuizen L. 2004. Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr. Opin. Microbiol. 7:255-261.
46. Vishniac W, Santer M. 1957. The thiobacilli. Microbiol. Rev. 21:195-213.
47. Visser MB, Majumdar S, Hani E, Sokol PA. 2004. Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect. Immun. 72:2850-2857.
48. von Bargen K, Haas A. 2009. Molecular and infection biology of the horse pathogen Rhodococcus equi. FEMS Microbiol. Rev. 33:870-891.
49. Wagner D, et al. 2005. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 174:1491-1500.
50. Wagner D, et al. 2006. Elemental analysis of the Mycobacterium avium phagosome in Balb/c mouse macrophages. Biochem. Biophys. Res. Com-mun. 344:1346-1351.
51. Wandersman C, Delepelaire P. 2004. Bacterial iron sources: from sidero-phores to hemophores. Annu. Rev. Microbiol. 58:611-647.
52. Yu S, Fiss E, Jacobs WR, Jr. 1998. Analysis of the exochelin locus in Mycobacterium smegmatis: biosynthesis genes have homology with genes of the peptide synthetase family. J. Bacteriol. 180:4676-4685.
53. Zhu W, et al. 1998. Exochelin genes in Mycobacterium smegmatis: identification of an ABC transporter and two non-ribosomal peptide synthe-tase genes. Mol. Microbiol. 29:629-639.