1887

Abstract

One of the mechanisms employed by the opportunistic pathogen to acquire the essential element iron is the production and release of two ferric iron chelating compounds (siderophores), ornibactin and pyochelin. Here we show that is also able to take advantage of a range of siderophores produced by other bacteria and fungi (‘xenosiderophores’) that chelate iron exclusively by means of hydroxamate groups. These include the tris-hydroxamate siderophores ferrioxamine B, ferrichrome, ferricrocin and triacetylfusarinine C, the bis-hydroxamates alcaligin and rhodotorulic acid, and the monohydroxamate siderophore cepabactin. We also show that of the 24 TonB-dependent transporters encoded by the genome, two (FhuA and FeuA) are involved in the uptake of hydroxamate xenosiderophores, with FhuA serving as the exclusive transporter of iron-loaded ferrioxamine B, triacetylfusarinine C, alcaligin and rhodotorulic acid, while both FhuA and FeuA are able to translocate ferrichrome-type siderophores across the outer membrane. Finally, we identified FhuB, a putative cytoplasmic membrane-anchored ferric-siderophore reductase, as being obligatory for utilization of all of the tested bis- and tris-hydroxamate xenosiderophores apart from alcaligin.

Funding
This study was supported by the:
  • Ministry of Higher Education, Malaysia
    • Principle Award Recipient: SyakiraMohammed Hussein
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001425
2024-01-08
2024-05-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/1/mic001425.html?itemId=/content/journal/micro/10.1099/mic.0.001425&mimeType=html&fmt=ahah

References

  1. Tavares M, Kozak M, Balola A, Sá-Correia I. Burkholderia cepacia complex bacteria: a feared contamination risk in water-based pharmaceutical products. Clin Microbiol Rev 2020; 33:139–19 [View Article] [PubMed]
    [Google Scholar]
  2. Bylund J, Campsall PA, Ma RC, Conway B-AD, Speert DP. Burkholderia cenocepacia induces neutrophil necrosis in chronic granulomatous disease. J Immunol 2005; 174:3562–3569 [View Article] [PubMed]
    [Google Scholar]
  3. Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 2010; 16:821–830 [View Article] [PubMed]
    [Google Scholar]
  4. Sokol PA. Production and utilization of pyochelin by clinical isolates of Pseudomonas cepacia. J Clin Microbiol 1986; 23:560–562 [View Article] [PubMed]
    [Google Scholar]
  5. Stephan H, Freund S, Beck W, Jung G, Meyer JM et al. Ornibactins–a new family of siderophores from Pseudomonas. Biometals 1993; 6:93–100 [View Article] [PubMed]
    [Google Scholar]
  6. Darling P, Chan M, Cox AD, Sokol PA. Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 1998; 66:874–877 [View Article] [PubMed]
    [Google Scholar]
  7. Mathew A, Eberl L, Carlier AL. A novel siderophore-independent strategy of iron uptake in the genus Burkholderia. Mol Microbiol 2014; 91:805–820 [View Article] [PubMed]
    [Google Scholar]
  8. Tyrrell J, Whelan N, Wright C, Sá-Correia I, McClean S et al. Investigation of the multifaceted iron acquisition strategies of Burkholderia cenocepacia. Biometals 2015; 28:367–380 [View Article] [PubMed]
    [Google Scholar]
  9. Thomas MS. Iron acquisition mechanisms of the Burkholderia cepacia complex. Biometals 2007; 20:431–452 [View Article] [PubMed]
    [Google Scholar]
  10. Silale A, van den Berg B. TonB-dependent transport across the bacterial outer membrane. Annu Rev Microbiol 2023; 77:67–88 [View Article] [PubMed]
    [Google Scholar]
  11. Noinaj N, Guillier M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 2010; 64:43–60 [View Article] [PubMed]
    [Google Scholar]
  12. Celia H, Noinaj N, Buchanan SK. Structure and stoichiometry of the Ton molecular motor. Int J Mol Sci 2020; 21:375 [View Article] [PubMed]
    [Google Scholar]
  13. Somboon K, Melling O, Lejeune M, Bardiaux B, Delepelaire P et al. Dynamic interplay between a TonB-dependent transporter and a TonB-like protein in a membrane environment. Biophys J 2022; 121:430a [View Article]
    [Google Scholar]
  14. Sokol PA. Tn5 insertion mutants of Pseudomonas aeruginosa deficient in surface expression of ferripyochelin-binding protein. J Bacteriol 1987; 169:3365–3368 [View Article] [PubMed]
    [Google Scholar]
  15. Alice AF, López CS, Lowe CA, Ledesma MA, Crosa JH. Genetic and transcriptional analysis of the siderophore malleobactin biosynthesis and transport genes in the human pathogen Burkholderia pseudomallei K96243. J Bacteriol 2006; 188:1551–1566 [View Article] [PubMed]
    [Google Scholar]
  16. Sokol PA, Darling P, Lewenza S, Corbett CR, Kooi CD. Identification of a siderophore receptor required for ferric ornibactin uptake in Burkholderia cepacia. Infect Immun 2000; 68:6554–6560 [View Article] [PubMed]
    [Google Scholar]
  17. Cuív PO, Clarke P, Lynch D, O’Connell M. Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J Bacteriol 2004; 186:2996–3005 [View Article] [PubMed]
    [Google Scholar]
  18. Michel L, Bachelard A, Reimmann C. Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology (Reading) 2007; 153:1508–1518 [View Article] [PubMed]
    [Google Scholar]
  19. Cunrath O, Gasser V, Hoegy F, Reimmann C, Guillon L et al. A cell biological view of the siderophore pyochelin iron uptake pathway in Pseudomonas aeruginosa. Environ Microbiol 2015; 17:171–185 [View Article] [PubMed]
    [Google Scholar]
  20. Schalk IJ, Perraud Q. Pseudomonas aeruginosa and its multiple strategies to access iron. Environ Microbiol 2023; 25:811–831 [View Article] [PubMed]
    [Google Scholar]
  21. Luscher A, Moynié L, Auguste PS, Bumann D, Mazza L et al. TonB-dependent receptor repertoire of Pseudomonas aeruginosa for uptake of siderophore-drug conjugates. Antimicrob Agents Chemother 2018; 62:e00097-18 [View Article] [PubMed]
    [Google Scholar]
  22. Normant V, Josts I, Kuhn L, Perraud Q, Fritsch S et al. Nocardamine-dependent iron uptake in Pseudomonas aeruginosa: exclusive involvement of the FoxA outer membrane transporter. ACS Chem Biol 2020; 15:2741–2751 [View Article] [PubMed]
    [Google Scholar]
  23. Llamas MA, Sparrius M, Kloet R, Jiménez CR, Vandenbroucke-Grauls C et al. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 2006; 188:1882–1891 [View Article] [PubMed]
    [Google Scholar]
  24. Hannauer M, Barda Y, Mislin GLA, Shanzer A, Schalk IJ. The ferrichrome uptake pathway in Pseudomonas aeruginosa involves an iron release mechanism with acylation of the siderophore and recycling of the modified desferrichrome. J Bacteriol 2010; 192:1212–1220 [View Article] [PubMed]
    [Google Scholar]
  25. Ankenbauer RG, Quan HN. FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol 1994; 176:307–319 [View Article] [PubMed]
    [Google Scholar]
  26. Poole K, Neshat S, Krebes K, Heinrichs DE. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacteriol 1993; 175:4597–4604 [View Article] [PubMed]
    [Google Scholar]
  27. Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ. An efflux pump is involved in secretion of newly synthesized siderophore by Pseudomonas aeruginosa. FEBS Lett 2010; 584:4751–4755 [View Article] [PubMed]
    [Google Scholar]
  28. Chan DCK, Burrows LL. Pseudomonas aeruginosa FpvB is a high-affinity transporter for xenosiderophores ferrichrome and ferrioxamine B. J Mol Biol 2022e03149-22 [View Article]
    [Google Scholar]
  29. Schalk IJ, Guillon L. Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways. Amino Acids 2013; 44:1267–1277 [View Article] [PubMed]
    [Google Scholar]
  30. Braun V, Pramanik A, Gwinner T, Köberle M, Bohn E. Sideromycins: tools and antibiotics. Biometals 2009; 22:3–13 [View Article] [PubMed]
    [Google Scholar]
  31. Essén SA, Bylund D, Holmström SJM, Moberg M, Lundström US. Quantification of hydroxamate siderophores in soil solutions of podzolic soil profiles in Sweden. Biometals 2006; 19:269–282 [View Article] [PubMed]
    [Google Scholar]
  32. Ahmed E, Holmström SJM. The effect of soil horizon and mineral type on the distribution of siderophores in soil. Geochim Cosmochim Acta 2014; 131:184–195 [View Article]
    [Google Scholar]
  33. Butt AT, Banyard CD, Haldipurkar SS, Agnoli K, Mohsin MI et al. The Burkholderia cenocepacia iron starvation σ factor, OrbS, possesses an on-board iron sensor. Nucleic Acids Res 2022; 50:3709–3726 [View Article] [PubMed]
    [Google Scholar]
  34. Clowes RC, Hayes W. Experiments in Microbial Genetics Oxford: Blackwell Scientific Publications; 1968
    [Google Scholar]
  35. Barrett AR, Kang Y, Inamasu KS, Son MS, Vukovich JM et al. Genetic tools for allelic replacement in Burkholderia species. Appl Environ Microbiol 2008; 74:4498–4508 [View Article] [PubMed]
    [Google Scholar]
  36. Shastri S, Spiewak HL, Sofoluwe A, Eidsvaag VA, Asghar AH et al. An efficient system for the generation of marked genetic mutants in members of the genus Burkholderia. Plasmid 2017; 89:49–56 [View Article] [PubMed]
    [Google Scholar]
  37. Hanahan D, Jessee J, Bloom FR. Plasmid transformation of Escherichia coli and other bacteria. Meth Enzymol 1991; 204:63–113
    [Google Scholar]
  38. Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S et al. Structural insights into the function of type VI secretion system TssA subunits. Nat Commun 2018; 9: [View Article]
    [Google Scholar]
  39. Herrero M, de Lorenzo V, Timmis KN. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 1990; 172:6557–6567 [View Article] [PubMed]
    [Google Scholar]
  40. De Lorenzo V, Timmis KN. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5-and Tn10-derived minitransposons. Meth Enzymol 1994; 235:386–405
    [Google Scholar]
  41. Powell PE, Szaniszlo PJ, Reid CP. Confirmation of occurrence of hydroxamate siderophores in soil by a novel Escherichia coli bioassay. Appl Environ Microbiol 1983; 46:1080–1083 [View Article] [PubMed]
    [Google Scholar]
  42. Koedding J, Howard P, Kaufmann L, Polzer P, Lustig A et al. Dimerization of TonB is not essential for its binding to the outer membrane siderophore receptor FhuA of Escherichia coli. J Biol Chem 2004; 279:9978–9986 [View Article] [PubMed]
    [Google Scholar]
  43. Asghar AH, Shastri S, Dave E, Wowk I, Agnoli K et al. The pobA gene of Burkholderia cenocepacia encodes a group I Sfp-type phosphopantetheinyltransferase required for biosynthesis of the siderophores ornibactin and pyochelin. Microbiology (Reading) 2011; 157:349–361 [View Article] [PubMed]
    [Google Scholar]
  44. Meyer J-M. Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron translocation. J Gen Microbiol 1992; 138:951–958 [View Article] [PubMed]
    [Google Scholar]
  45. Peacock RS, Weljie AM, Peter Howard S, Price FD, Vogel HJ. The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J Mol Biol 2005; 345:1185–1197 [View Article] [PubMed]
    [Google Scholar]
  46. Cuív PO, Keogh D, Clarke P, O’Connell M. FoxB of Pseudomonas aeruginosa functions in the utilization of the xenosiderophores ferrichrome, ferrioxamine B, and schizokinen: evidence for transport redundancy at the inner membrane. J Bacteriol 2007; 189:284–287 [View Article] [PubMed]
    [Google Scholar]
  47. Josts I, Veith K, Normant V, Schalk IJ, Tidow H. Structural insights into a novel family of integral membrane siderophore reductases. Proc Natl Acad Sci USA 2021; 118:2101–2118 [View Article]
    [Google Scholar]
  48. Boulanger P, le Maire M, Bonhivers M, Dubois S, Desmadril M et al. Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 1996; 35:14216–14224 [View Article] [PubMed]
    [Google Scholar]
  49. Hartmann A, Fiedler HP, Braun V. Uptake and conversion of the antibiotic albomycin by Escherichia coli K-12. Eur J Biochem 1979; 99:517–524 [View Article] [PubMed]
    [Google Scholar]
  50. Pramanik A, Braun V. Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6. J Bacteriol 2006; 188:3878–3886 [View Article] [PubMed]
    [Google Scholar]
  51. Imbert M, Béchet M, Blondeau R. Comparison of the main siderophores produced by some species of Streptomyces. Curr Microbiol 1995; 31:129–133 [View Article]
    [Google Scholar]
  52. Andersen D, Renshaw JC, Wiebe MG. Rhodotorulic acid production by Rhodotorula mucilaginosa. Mycol Res 2003; 107:949–956 [View Article] [PubMed]
    [Google Scholar]
  53. Barona-Gómez F, Lautru S, Francou F-X, Leblond P, Pernodet J-L et al. Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology (Reading) 2006; 152:3355–3366 [View Article] [PubMed]
    [Google Scholar]
  54. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O et al. Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog 2007; 3:1195–1207 [View Article] [PubMed]
    [Google Scholar]
  55. Wallner A, Blatzer M, Schrettl M, Sarg B, Lindner H et al. Ferricrocin, a siderophore involved in intra- and transcellular iron distribution in Aspergillus fumigatus. Appl Environ Microbiol 2009; 75:4194–4196 [View Article] [PubMed]
    [Google Scholar]
  56. Oide S, Berthiller F, Wiesenberger G, Adam G, Turgeon BG. Individual and combined roles of malonichrome, ferricrocin, and TAFC siderophores in Fusarium graminearum pathogenic and sexual development. Front Microbiol 2014; 5:759 [View Article] [PubMed]
    [Google Scholar]
  57. Soe CZ, Telfer TJ, Levina A, Lay PA, Codd R. Simultaneous biosynthesis of putrebactin, avaroferrin and bisucaberin by Shewanella putrefaciens and characterisation of complexes with iron(III), molybdenum(VI) or chromium(V). J Inorg Biochem 2016; 162:207–215 [View Article] [PubMed]
    [Google Scholar]
  58. Nagano Y, Elborn JS, Millar BC, Walker JM, Goldsmith CE et al. Comparison of techniques to examine the diversity of fungi in adult patients with cystic fibrosis. Med Mycol 2010; 48:166–176 [View Article]
    [Google Scholar]
  59. Poore TS, Meier M, Towler E, Martiniano SL, Brinton JT et al. Clinical characteristics of people with cystic fibrosis and frequent fungal infection. Pediatr Pulmonol 2022; 57:152–161 [View Article] [PubMed]
    [Google Scholar]
  60. Atkin CL, Neilands JB, Phaff HJ. Rhodotorulic acid from species of Leucosporidium, Rhodosporidium, Rhodotorula, Sporidiobolus, and Sporobolomyces, and a new alanine-containing ferrichrome from Cryptococcus melibiosum. J Bacteriol 1970; 103:722–733 [View Article] [PubMed]
    [Google Scholar]
  61. Moore CH, Foster LA, Gerbig DG, Dyer DW, Gibson BW. Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica. J Bacteriol 1995; 177:1116–1118 [View Article] [PubMed]
    [Google Scholar]
  62. Li X, Hu Y, Gong J, Zhang L, Wang G. Comparative genome characterization of Achromobacter members reveals potential genetic determinants facilitating the adaptation to a pathogenic lifestyle. Appl Microbiol Biotechnol 2013; 97:6413–6425 [View Article] [PubMed]
    [Google Scholar]
  63. Charlang G, Ng B, Horowitz NH, Horowitz RM. Cellular and extracellular siderophores of Aspergillus nidulans and Penicillium chrysogenum. Mol Cell Biol 1981; 1:94–100 [View Article] [PubMed]
    [Google Scholar]
  64. Hördt W, Römheld V, Winkelmann G. Fusarinines and dimerum acid, mono- and dihydroxamate siderophores from Penicillium chrysogenum, improve iron utilization by strategy I and strategy II plants. Biometals 2000; 13:37–46 [View Article] [PubMed]
    [Google Scholar]
  65. Haas H, Schoeser M, Lesuisse E, Ernst JF, Parson W et al. Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem J 2003; 371:505–513 [View Article] [PubMed]
    [Google Scholar]
  66. Hummel W, Diekmann H. Preliminary characterization of ferrichrome synthetase from Aspergillus quadricinctus. Biochim Biophys Acta 1981; 657:313–320 [View Article] [PubMed]
    [Google Scholar]
  67. Manno G, Dalmastri C, Tabacchioni S, Vandamme P, Lorini R et al. Epidemiology and clinical course of Burkholderia cepacia complex infections, particularly those caused by different Burkholderia cenocepacia strains, among patients attending an Italian Cystic Fibrosis Center. J Clin Microbiol 2004; 42:1491–1497 [View Article] [PubMed]
    [Google Scholar]
  68. Ghysels B, Dieu BTM, Beatson SA, Pirnay J-P, Ochsner UA et al. FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. Microbiology (Reading) 2004; 150:1671–1680 [View Article] [PubMed]
    [Google Scholar]
  69. Ghysels B, Ochsner U, Möllman U, Heinisch L, Vasil M et al. The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol Lett 2005; 246:167–174 [View Article] [PubMed]
    [Google Scholar]
  70. Cornelis P, Dingemans J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol 2013; 3:75 [View Article] [PubMed]
    [Google Scholar]
  71. Otero-Asman JR, García-García AI, Civantos C, Quesada JM, Llamas MA. Pseudomonas aeruginosa possesses three distinct systems for sensing and using the host molecule haem. Environ Microbiol 2019; 21:4629–4647 [View Article] [PubMed]
    [Google Scholar]
  72. Yeats C, Rawlings ND, Bateman A. The PepSY domain: a regulator of peptidase activity in the microbial environment?. Trends Biochem Sci 2004; 29:169–172 [View Article] [PubMed]
    [Google Scholar]
  73. van Delden C, Page MGP, Köhler T. Involvement of Fe uptake systems and AmpC β-lactamase in susceptibility to the siderophore monosulfactam BAL30072 in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2013; 57:2095–2102 [View Article] [PubMed]
    [Google Scholar]
  74. Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P et al. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. Bioinformatics 202208 [View Article]
    [Google Scholar]
  75. Ganne G, Brillet K, Basta B, Roche B, Hoegy F et al. Iron release from the siderophore pyoverdine in Pseudomonas aeruginosa involves three new actors: FpvC, FpvG, and FpvH. ACS Chem Biol 2017; 12:1056–1065 [View Article] [PubMed]
    [Google Scholar]
  76. Roche B, Mislin GLA, Schalk IJ. Identification of the fatty acid coenzyme-A ligase FadD1 as an interacting partner of FptX in the Pseudomonas aeruginosa pyochelin pathway. FEBS Lett 2021; 595:370–378 [View Article] [PubMed]
    [Google Scholar]
  77. Imperi F, Tiburzi F, Visca P. Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2009; 106:20440–20445 [View Article] [PubMed]
    [Google Scholar]
  78. Brillet K, Ruffenach F, Adams H, Journet L, Gasser V et al. An ABC transporter with two periplasmic binding proteins involved in iron acquisition in Pseudomonas aeruginosa. ACS Chem Biol 2012; 7:2036–2045 [View Article] [PubMed]
    [Google Scholar]
  79. Bonneau A, Roche B, Schalk IJ. Iron acquisition in Pseudomonas aeruginosa by the siderophore pyoverdine: an intricate interacting network including periplasmic and membrane proteins. Sci Rep 2020; 10:120 [View Article] [PubMed]
    [Google Scholar]
  80. Roche B, Garcia-Rivera MA, Normant V, Kuhn L, Hammann P et al. A role for PchHI as the ABC transporter in iron acquisition by the siderophore pyochelin in Pseudomonas aeruginosa. Environ Microbiol 2022; 24:866–877 [View Article] [PubMed]
    [Google Scholar]
  81. Pramanik A, Stroeher UH, Krejci J, Standish AJ, Bohn E et al. Albomycin is an effective antibiotic, as exemplified with Yersinia enterocolitica and Streptococcus pneumoniae. Int J Med Microbiol 2007; 297:459–469 [View Article] [PubMed]
    [Google Scholar]
  82. Braun V, Günthner K, Hantke K, Zimmermann L. Intracellular activation of albomycin in Escherichia coli and Salmonella typhimurium. J Bacteriol 1983; 156:308–315 [View Article] [PubMed]
    [Google Scholar]
  83. Saha A, Dutta S, Nandi N. Inhibition of seryl tRNA synthetase by seryl nucleoside moiety (SB-217452) of albomycin antibiotic. J Biomol Struct Dyn 2020; 38:2440–2454 [View Article] [PubMed]
    [Google Scholar]
  84. Zeng Y, Roy H, Patil PB, Ibba M, Chen S. Characterization of two seryl-tRNA synthetases in albomycin-producing Streptomyces sp. strain ATCC 700974. Antimicrob Agents Chemother 2009; 53:4619–4627 [View Article] [PubMed]
    [Google Scholar]
  85. Stefanska AL, Fulston M, Houge-frydrych CSV, Jones JJ, Warr SR. A potent Seryl tRNA synthetase inhibitor SB-217452 isolated from a Streptomyces species. J Antibiot 2000; 53:1346–1353 [View Article]
    [Google Scholar]
  86. Rivera GSM, Beamish CR, Wencewicz TA. Immobilized FhuD2 siderophore-binding protein enables purification of salmycin sideromycins from Streptomyces violaceus DSM 8286. ACS Infect Dis 2018; 4:845–859 [View Article] [PubMed]
    [Google Scholar]
  87. Vértesy L, Aretz W, Fehlhaber H, Kogler H. Salmycin A–D, Antibiotika aus Streptomyces violaceus, DSM 8286, mit Siderophor‐Aminoglycosid‐Struktur. Helvetica Chimica Acta 1995; 78:46–60 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001425
Loading
/content/journal/micro/10.1099/mic.0.001425
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error