Pseudomonas fluorescens pirates both ferrioxamine and ferricoelichelin Siderophores from Streptomyces ambofaciens

Applied and Environmental Microbiology

Volumn 81, Issue 9, 2015, Pages 3132-3141

  Galet, Justine ^a,b   Deveau, Aurélie ^a,c   Hôtel, Laurence ^a,b   Frey Klett, Pascale ^a,c   Leblond, Pierre ^a,b   Aigle, Bertrand ^a,b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; IRON; SOILS;

AEROBIC ENVIRONMENTS; BIOLOGICAL PROCESS; COMPETITIVE ENVIRONMENT; DESFERRIOXAMINE; MICROBIAL COMPETITION; PSEUDOMONAS FLUORESCENS; SIDEROPHORE SYNTHESIS; STREPTOMYCES AMBOFACIENS;

BACTERIA;

BACTERIUM; BIOAVAILABILITY; CHELATION; GENE EXPRESSION; INTERSPECIFIC INTERACTION; IRON; MUTATION; OXIC CONDITIONS; SOIL MICROORGANISM;

BACTERIA (MICROORGANISMS); PSEUDOMONAS FLUORESCENS; STREPTOMYCES; STREPTOMYCES AMBOFACIENS; STREPTOMYCES AMBOFACIENS ATCC 23877;

COELICHELIN; CULTURE MEDIUM; DEFEROXAMINE; FERRIC ION; FERRIOXAMINE; OLIGOPEPTIDE; SIDEROPHORE;

CHEMISTRY; CULTURE MEDIUM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGANISMAL INTERACTION; PSEUDOMONAS FLUORESCENS; STREPTOMYCES;

CULTURE MEDIA; DEFEROXAMINE; FERRIC COMPOUNDS; MICROBIAL INTERACTIONS; OLIGOPEPTIDES; PSEUDOMONAS FLUORESCENS; SIDEROPHORES; STREPTOMYCES;

EID: 84927792318     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03520-14     Document Type: Article

References (70)

1. Konovalova A, Søgaard-Andersen L. 2011. Close encounters: contactdependent interactions in bacteria. Mol Microbiol 81:297-301. http://dx.doi.org/10.1111/j.1365-2958.2011.07711.x.
2. Barry SM, Challis GL. 2009. Recent advances in siderophore biosynthesis. Curr Opin Chem Biol 13:205-215. http://dx.doi.org/10.1016/j.cbpa.2009.03.008.
3. Hider RC, Kong X. 2010. Chemistry and biology of siderophores. Nat Prod Rep 27:637. http://dx.doi.org/10.1039/b906679a.
4. Chu BC, Garcia-Herrero A, Johanson TH, Krewulak KD, Lau CK, Peacock RS, Slavinskaya Z, Vogel HJ. 2010. Siderophore uptake in bacteria and the battle for iron with the host; a bird's eye view. BioMetals 23:601-611. http://dx.doi.org/10.1007/s10534-010-9361-x.
5. Miethke M, Marahiel MA. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413-451. http://dx.doi.org/10.1128/MMBR.00012-07.
6. Dumas Z, Ross-Gillespie A, Kummerli R. 2013. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc Biol Sci 280:20131055. http://dx.doi.org/10.1098/rspb.2013.1055.
7. Luckey M, Pollack JR, Wayne R, Ames BN, Neilands JB. 1972. Iron uptake in Salmonella typhimurium: utilization of exogenous siderochromes as iron carriers. J Bacteriol 111:731-738.
8. Schubert S, Fischer D, Heesemann J. 1999. Ferric enterochelin transport in Yersinia enterocolitica: molecular and evolutionary aspects. J Bacteriol 181:6387-6395.
9. Cornelis P, Bodilis J. 2009. A survey of TonB-dependent receptors in fluorescent pseudomonads. Environ Microbiol Rep 1:256-262. http://dx.doi.org/10.1111/j.1758-2229.2009.00041.x.
10. Moon CD, Zhang X-X, Matthijs S, Schäfer M, Budzikiewicz H, Rainey PB. 2008. Genomic, genetic and structural analysis of pyoverdinemediated iron acquisition in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. BMC Microbiol 8:7. http://dx.doi.org/10.1186/1471-2180-8-7.
11. Champomier-Vergès M-C, Stintzi A, Meyer J-M. 1996. Acquisition of iron by the non-siderophore-producing Pseudomonas fragi. Microbiology 142:1191-1199. http://dx.doi.org/10.1099/13500872-142-5-1191.
12. Bäumler AJ, Hantke K. 1992. Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol 6:1309-1321. http://dx.doi.org/10.1111/j.1365-2958.1992.tb00852.x.
13. Berner I, Winkelmann G. 1990. Ferrioxamine transport mutants and the identification of the ferrioxamine receptor protein (FoxA) in Erwinia herbicola (Enterobacter agglomerans). Biol Met 2:197-202. http://dx.doi.org/10.1007/BF01141359.
14. Tanabe T, Funahashi T, Miyamoto K, Tsujibo H, Yamamoto S. 2011. Identification of genes, desR and desA, required for utilization of desferrioxamine B as a xenosiderophore in Vibrio furnissii. Biol Pharm Bull 34:570-574. http://dx.doi.org/10.1248/bpb.34.570.
15. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. 2012. Interspecies modulation of bacterial development through iron competition and siderophore piracy: xenosiderophores alter development in actinomycetes. Mol Microbiol 86:628-644. http://dx.doi.org/10.1111/mmi.12008.
16. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90. http://dx.doi.org/10.1038/nature11237.
17. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G, Podar M, Schadt CW. 2013. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8:e76382. http://dx.doi.org/10.1371/journal.pone.0076382.
18. Pinnert-Sindico S. 1954. Une nouvelle espece de Streptomyces productrice d'antibiotiques: Streptomyces ambofaciens n sp caracteres culturaux. Ann Inst Pasteur (Paris) 87:702-707.
19. Frey-Klett P, Pierrat JC, Garbaye J. 1997. Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Appl Environ Microbiol 63:139-144.
20. Deveau A, Brulé C, Palin B, Champmartin D, Rubini P, Garbaye J, Sarniguet A, Frey-Klett P. 2010. Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8: role of trehalose and thiamine in mutualistic interaction. Environ Microbiol Rep 2:560-568. http://dx.doi.org/10.1111/j.1758-2229.2010.00145.x.
21. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes, Norwich, United Kingdom.
22. Leblond P, Fischer G, Francou F-X, Berger F, Guérineau M, Decaris B. 1996. The unstable region of Streptomyces ambofaciens includes 210 kb terminal inverted repeats flanking the extremities of the linear chromosomal DNA. Mol Microbiol 19:261-271. http://dx.doi.org/10.1046/j.1365-2958.1996.366894.x.
23. Pang X, Aigle B, Girardet J-M, Mangenot S, Pernodet J-L, Decaris B, Leblond P. 2004. Functional angucycline-like antibiotic gene cluster in the terminal inverted repeats of the Streptomyces ambofaciens linear chromosome. Antimicrob Agents Chemother 48:575-588. http://dx.doi.org/10.1128/AAC.48.2.575-588.2004.
24. Pospiech A, Neumann B. 1995. A versatile quick-prep of genomic DNA from Gram-positive bacteria. Trends Genet 11:217-218. http://dx.doi.org/10.1016/S0168-9525(00)89052-6.
25. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
26. Buttner MJ, Chater KF, Bibb MJ. 1990. Cloning, disruption, and transcriptional analysis of three RNA polymerase sigma factor genes of Streptomyces coelicolor A3(2). J Bacteriol 172:3367-3378.
27. Deveau A, Gross H, Morin E, Karpinets T, Utturkar S, Mehnaz S, Martin F, Frey-Klett P, Labbé J. 2014. Genome sequence of the mycorrhizal helper bacterium Pseudomonas fluorescens BBc6R8. Genome Announc 2:e01152-13. http://dx.doi.org/10.1128/genomeA.01152-13.
28. Roth V, Aigle B, Bunet R, Wenner T, Fourrier C, Decaris B, Leblond P. 2004. Differential and cross-transcriptional control of duplicated genes encoding alternative sigma factors in Streptomyces ambofaciens. J Bacteriol 186:5355-5365. http://dx.doi.org/10.1128/JB.186.16.5355-5365.2004.
29. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
30. Fernández-Martínez LT, Sol RD, Evans MC, Fielding S, Herron PR, Chandra G, Dyson PJ. 2011. A transposon insertion single-gene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek 99:515-522. http://dx.doi.org/10.1007/s10482-010-9518-1.
31. Paget MSB, Chamberlin L, Atrih A, Foster SJ, Buttner MJ. 1999. Evidence that the extracytoplasmic function sigma factor E is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol 181:204-211.
32. Gamalero E, Fracchia L, Cavaletto M, Garbaye J, Frey-Klett P, Varese GC, Martinotti MG. 2003. Characterization of functional traits of two fluorescent pseudomonads isolated from basidiomes of ectomycorrhizal fungi. Soil Biol Biochem 35:55-65. http://dx.doi.org/10.1016/S0038-0717(02)00236-5.
33. Visca P, Leoni L, Wilson MJ, Lamont IL. 2002. Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177-1190. http://dx.doi.org/10.1046/j.1365-2958.2002.03088.x.
34. Ravel J, Cornelis P. 2003. Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11:195-200. http://dx.doi.org/10.1016/S0966-842X(03)00076-3.
35. Cornelis P. 2010. Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol 86:1637-1645. http://dx.doi.org/10.1007/s00253-010-2550-2.
36. Schalk IJ, Guillon L. 2013. Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol 15:1661-1673. http://dx.doi.org/10.1111/1462-2920.12013.
37. Barona-Gomez F, Lautru S, Francou F-X, Leblond P, Pernodet J-L, Challis GL. 2006. Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology 152:3355-3366. http://dx.doi.org/10.1099/mic.0.29161-0.
38. Barona-Gómez F, Wong U, Giannakopulos AE, Derrick PJ, Challis GL. 2004. Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126:16282-16283. http://dx.doi.org/10.1021/ja045774k.
39. Lautru S, Deeth RJ, Bailey LM, Challis GL. 2005. Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat Chem Biol 1:265-269. http://dx.doi.org/10.1038/nchembio731.
40. Floriano B, Bibb M. 1996. afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21:385-396. http://dx.doi.org/10.1046/j.1365-2958.1996.6491364.x.
41. Patel P, Song L, Challis GL. 2010. Distinct extracytoplasmic siderophore binding proteins recognize ferrioxamines and ferricoelichelin in Streptomyces coelicolor A3(2). Biochemistry 49:8033-8042. http://dx.doi.org/10.1021/bi100451k.
42. Llamas MA, Sparrius M, Kloet R, Jimenez CR, Vandenbroucke-Grauls C, Bitter W. 2006. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 188:1882-1891. http://dx.doi.org/10.1128/JB.188.5.1882-1891.2006.
43. Hartney SL, Mazurier S, Kidarsa TA, Quecine MC, Lemanceau P, Loper JE. 2011. TonB-dependent outer-membrane proteins and siderophore utilization in Pseudomonas fluorescens Pf-5. BioMetals 24:193-213. http://dx.doi.org/10.1007/s10534-010-9385-2.
44. Yamanaka K. 2005. Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151:2899-2905. http://dx.doi.org/10.1099/mic.0.28139-0.
45. Joshi F, Archana G, Desai A. 2006. Siderophore cross-utilization amongst rhizospheric bacteria and the role of their differential affinities for Fe3+ on growth stimulation under iron-limited conditions. Curr Microbiol 53:141-147. http://dx.doi.org/10.1007/s00284-005-0400-8.
46. Funahashi T, Tanabe T, Miyamoto K, Tsujibo H, Maki J, Yamamoto S. 2013. Characterization of a gene encoding the outer membrane receptor for ferric enterobactin in Aeromonas hydrophila ATCC 7966(T). Biosci Biotechnol Biochem 77:353-360. http://dx.doi.org/10.1271/bbb.120774.
47. Tomaras AP, Crandon JL, McPherson CJ, Banevicius MA, Finegan SM, Irvine RL, Brown MF, O'Donnell JP, Nicolau DP. 2013. Adaptationbased resistance to siderophore-conjugated antibacterial agents by Pseudomonas aeruginosa. Antimicrob Agents Chemother 57:4197-4207. http://dx.doi.org/10.1128/AAC.00629-13.
48. Miethke M, Kraushaar T, Marahiel MA. 2013. Uptake of xenosiderophores in Bacillus subtilis occurs with high affinity and enhances the folding stabilities of substrate binding proteins. FEBS Lett 587:206-213. http://dx.doi.org/10.1016/j.febslet.2012.11.027.
49. Veggi D, Gentile MA, Cantini F, Lo Surdo P, Nardi-Dei V, Seib KL, Pizza M, Rappuoli R, Banci L, Savino S, Scarselli M. 2012. The factor H binding protein of Neisseria meningitidis interacts with xenosiderophores in vitro. Biochemistry 51:9384-9393. http://dx.doi.org/10.1021/bi301161w.
50. Weber M, Taraz K, Budzikiewicz H, Geoffroy V, Meyer J-M. 2000. The structure of a pyoverdine from Pseudomonas sp. CFML 96.188 and its relation to other pyoverdines with a cyclic C-terminus. BioMetals 13: 301-309. http://dx.doi.org/10.1023/A:1009235421503.
51. Barelmann I, Fernández DU, Budzikiewicz H, Meyer J-M. 2003. The pyoverdine from Pseudomonas chlororaphis D-TR133 showing mutual acceptance with the pyoverdine of Pseudomonas fluorescens CHA0. BioMetals 16:263-270. http://dx.doi.org/10.1023/A:1020615830765.
52. Ueda K, Kawai S, Ogawa H, Kiyama A, Kubota T, Kawanobe H, Beppu T. 2000. Wide distribution of interspecific stimulatory events on antibiotic production and sporulation among Streptomyces species. J Antibiot 53:979-982. http://dx.doi.org/10.7164/antibiotics.53.979.
53. Garbaye J, Duponnois R, Wahl JL. 1990. The bacteria associated with Laccaria laccata ectomycorrhizas or sporocarps: effect of symbiosis establishment on Douglas fir. Symbiosis Rehovot 9:267-273.
54. Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M. 2001. Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol 3:691-698. http://dx.doi.org/10.1046/j.1462-2920.2001.00243.x.
55. Nazaret S, Brothier E, Ranjard L. 2003. Shifts in diversity and microscale distribution of the adapted bacterial phenotypes due to Hg(II) spiking in soil. Microb Ecol 45:259-269. http://dx.doi.org/10.1007/s00248-002-2035-7.
56. Srifuengfung S, Assanasen S, Tuntawiroon M, Meejanpetch S. 2010. Comparison between Pseudomonas aeruginosa siderophores and desferrioxamine for iron acquisition from ferritin. Asian Biomed 4:631-635.
57. Müller G, Raymond KN. 1984. Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J Bacteriol 160: 304-312.
58. Meiwes J, Fiedler H-P, Zähner H, Konetschny-Rapp S, Jung G. 1990. Production of desferrioxamine E and new analogues by directed fermentation and feeding fermentation. Appl Microbiol Biotechnol 32:505-510.
59. Kadi N, Oves-Costales D, Barona-Gomez F, Challis GL. 2007. A new family of ATP-dependent oligomerization-macrocyclization biocatalysts. Nat Chem Biol 3:652-656. http://dx.doi.org/10.1038/nchembio.2007.23.
60. Nett M, Ikeda H, Moore BS. 2009. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26:1362-1384. http://dx.doi.org/10.1039/b817069j.
61. Kobayakawa F, Kodani S. 2012. Screening of streptomycetes for production of desferrioxamines. J Pure Appl Microbiol 6:1553-1558.
62. Martinez JS, Haygood MG, Butler A. 2001. Identification of a natural desferrioxamine siderophore produced by a marine bacterium. Limnol Oceanogr 46:420-424. http://dx.doi.org/10.4319/lo.2001.46.2.0420.
63. Essén SA, Johnsson A, Bylund D, Pedersen K, Lundström US. 2007. Siderophore production by Pseudomonas stutzeri under aerobic and anaerobic conditions. Appl Environ Microbiol 73:5857-5864. http://dx.doi.org/10.1128/AEM.00072-07.
64. Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW. 2011. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35: 652-680. http://dx.doi.org/10.1111/j.1574-6976.2011.00269.x.
65. Deiss K, Hantke K, Winkelmann G. 1998. Molecular recognition of siderophores: a study with cloned ferrioxamine receptors (FoxA) from Erwinia herbicola and Yersinia enterocolitica. Biometals 11:131-137. http://dx.doi.org/10.1023/A:1009230012577.
66. Cordero OX, Ventouras L-A, DeLong EF, Polz MF. 2012. Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc Natl Acad Sci U S A 109:20059-20064. http://dx.doi.org/10.1073/pnas.1213344109.
67. Bailey MJ, Lilley AK, Thompson IP, Rainey PB, Ellis RJ. 1995. Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; stability and potential for marker gene transfer. Mol Ecol 4:755-763. http://dx.doi.org/10.1111/j.1365-294X.1995.tb00276.x.
68. Compeau G, Al-Achi BJ, Platsouka E, Levy SB. 1988. Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl Environ Microbiol 54:2432-2438.
69. Holloway BW. 1955. Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13:572-581. http://dx.doi.org/10.1099/00221287-13-3-572.
70. Frey-Klett P, Chavatte M, Clausse M-L, Courrier S, Roux CL, Raaijmakers J, Martinotti MG, Pierrat J-C, Garbaye J. 2005. Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317-328. http://dx.doi.org/10.1111/j.1469-8137.2004.01212.x.