Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis

MicrobiologyOpen

Volumn 5, Issue 3, 2016, Pages 512-526

  Esmaeel, Qassim ^a   Pupin, Maude ^b,c   Kieu, Nam Phuong ^d   Chataigné, Gabrielle ^a   Béchet, Max ^a   Deravel, Jovana ^a   Krier, François ^a   Höfte, Monica ^d   Jacques, Philippe ^a   Leclère, Valérie ^a,b,c  

^a Cité scientifique   (France)

^b UNIV LILLE   (France)

^c INRIA   (France)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Burkholderia; genome mining; lipopeptide; NRPS; siderophore

Indexed keywords

BURKHOMYCIN; LIPOPEPTIDE; LIPOPROTEIN; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; NONRIBOSOMAL PEPTIDE SYNTHETASE; PHYMABACTIN; SIDEROPHORE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BIOLOGICAL PEST CONTROL; BURKHOLDERIA; BURKHOLDERIA AMBIFARIA; BURKHOLDERIA PHYMATUM; BURKHOLDERIA PSEUDOMALLEI; BURKHOLDERIACEAE; CONTROLLED STUDY; ENZYME ASSAY; GENE CLUSTER; GENOME ANALYSIS; GENOME MINING; INFORMATION PROCESSING; MOLECULAR DYNAMICS; NONHUMAN; NONRIBOSOMAL PEPTIDE SYNTHETASE GENE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL;

EID: 84974667584     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.347     Document Type: Article

References (51)

1. Abe, M., and T. Nakazawa. 1994. Characterization of haemolytic and antifungal substance, cepalycin, from Pseudomonas cepacia. Microbiol. Immunol. 38:1–9.
2. Adler, C., N. S. Corbalán, M. R. Seyedsayamdost, M. F. Pomares, R. E. de Cristóbal, J. Clardy, et al. 2012. Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS ONE 7:e46754.
3. Anand, S., M. V. R. Prasad, G. Yadav, N. Kumar, J. Shehara, M. Z. Ansari, et al. 2010. SBSPKS: structure based sequence analysis of polyketide synthases. Nucl. Acids Res. 38:W487–W496.
4. Bachmann, B. O., and J. Ravel. 2009. In silico prediction of microbial secondary metabolic pathways from DNA sequence data. Meth. Enzymol. 458:181–217.
5. Balibar, C., F. Vaillancourt, and C. Walsh. 2005. Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains. Chem. Biol. 12:1189–1200.
6. Barelmann, I., J. M. Meyer, K. Taraz, and H. Budzikiewicz. 1996. Cepaciachelin, a new catecholate siderophore from Burkholderia (Pseudomonas) cepacia. Z. Naturforsch. 51C:627–630.
7. Caballero-Mellado, J., J. Onofre-Lemus, P. Estrada-de Los Santos, and L. Martínez-Aguilar. 2007. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl. Environ. Microbiol. 73:5308–5319.
8. Caboche, S., M. Pupin, V. Leclère, A. Fontaine, P. Jacques, and G. Kucherov. 2008. NORINE: a database of nonribosomal peptides. Nucl. Acids Res. 36:D326–D331.
9. Caboche, S., M. Pupin, V. Leclère, P. Jacques, and G. Kucherov. 2009. Structural pattern matching of nonribosomal peptides. BMC Struct. Biol. 9:15.
10. Caradec, T., M. Pupin, A. Vanvlassenbroeck, M.-D. Devignes, M. Smaïl-Tabbone, P. Jacques, et al. 2014. Prediction of monomer isomery in Florine: a workflow dedicated to nonribosomal peptide discovery. PLoS ONE 9:e85667.
11. Cheng, A. C., and B. J. Currie. 2005. Melioidosis: epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 18:383–416.
12. Coenye, T., P. Vandamme, J. R. W. Govan, and J. J. LiPuma. 2001. Taxonomy and identification of the Burkholderia cepacia complex. J. Clin. Microbiol. 39:3427–3436.
13. Cole, J. R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, et al. 2009. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucl. Acids Res. 37:D141–D145.
14. Cornelis, P., and S. Matthijs. 2002. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ. Microbiol. 4:787–798.
15. Cox, C. D., K. L. Jr Rinehart, M. L. Moore, and J. C. Jr Cook. 1981. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 78:4256–4260.
16. D'aes, J., N. P. Kieu, V. Leclère, C. Tokarski, F. E. Olorunleke, K. De Maeyer, et al. 2014. To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ. Microbiol. 16: 2282–2300.
17. De Bruijn, I., M. De Kock, M. Yang, P. De Waard, T. Van Beek, and J. Raaijmakers. 2007. Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol. Microbiol. 63:417–428.
18. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791.
19. Franke, J., K. Ishida, and C. Hertweck. 2014. Evolution of siderophore pathways in human pathogenic bacteria. J. Am. Chem. Soc. 136:5599–5602.
20. Franke, J., K. Ishida, and C. Hertweck. 2015. Plasticity of the malleobactin pathway and its impact on siderophore action in human pathogenic bacteria. Chem. Eur. J. 21:8010–8014.
21. Gasser, V., L. Guillon, O. Cunrath, and I. J. Schalk. 2015. Cellular organization of siderophore biosynthesis in Pseudomonas aeruginosa: evidence for siderosomes. J. Inorg. Chem. 148:27–34.
22. Gu, G., L. Smith, N. Wang, H. Wang, and S. E. Lu. 2009. Biosynthesis of an antifungal oligopeptide in Burkholderia contaminans strain MS14. Biochem. Biophys. Res. Commun. 380:328–332.
23. Hammer, P. E., W. Burd, D. S. Hill, J. M. Ligon, and K. H. van Pée. 1999. Conservation of the pyrrolnitrin biosynthetic gene cluster among six pyrrolnitrin-producing strains. FEMS Microbiol. Lett. 180:39–44.
24. Lackner, G., N. Moebius, L. P. Partida-Martinez, S. Boland, and C. Hertweck. 2011. Evolution of an endofungal lifestyle: deductions from the Burkholderia rhizoxinica genome. BMC Genom. 12:210.
25. Landy, M., G. H. Warren, S. B. Rosenman, and L. G. Colio. 1948. Bacillomycin – an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc. Soc. Biol. Med. 67:539–541.
26. Lautru, S., D. Oves-Costales, J. L. Pernodet, and G. L. Challis. 2007. MbtH-like protein-mediated cross-talk between non-ribosomal peptide antibiotic and siderophore biosynthetic pathways in Streptomyces coelicolor M145. Microbiology 153:1405–1412.
27. Leclère, V., R. Marti, M. Béchet, P. Fickers, and P. Jacques. 2006. The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface-active properties. Arch. Microbiol. 186:475–483.
28. Lim, Y., S. J. Suh, S. Kim, B. Hyun, C. Kim, and C. H. Lee. 1994. Cepacidine A, a novel antifungal antibiotic produced by Pseudomonas cepacia. II. Physico-chemical properties and structure lucidation. J. Antibiot. 47:1406–1416.
29. Lin, Z., J. O. Falkinham, K. A. Tawfik, P. Jeffs, B. Bray, G. Dubay, et al. 2012. Burkholdines from Burkholderia ambifaria: antifungal agents and possible virulence factors. J. Nat. Prod. 75:1518–1523.
30. Mahenthiralingam, E., and J. B. Goldberg. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144–156.
31. Mahenthiralingam, E., A. Baldwin, and C. G. Dowson. 2008. Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J. Appl. Microbiol. 104:1539–1551.
32. Marahiel, M. A. 2009. Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J. Pept. Sci. 15:799–807.
33. Michel, L., A. Bachelard, and C. Reimmann. 2007. Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 153:1508–1518.
34. Nierman, W. C., D. DeShazer, H. S. Kim, H. Tettelin, K. E. Nelson, T. Feldblyum, et al. 2004. Structural flexibility in the Burkholderia mallei genome. Proc. Natl. Acad. Sci. USA 101:14246–14251.
35. Ongena, M., and P. Jacques. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16:115–125.
36. Pauwelyn, E., C. J. Huang, M. Ongena, V. Leclère, P. Jacques, P. Bleyaert, et al. 2013. New linear lipopeptides produced by Pseudomonas cichorii SF1-54 are involved in virulence, swarming motility, and biofilm formation. Mol. Plant Microbe Interac. 26:585–598.
37. Payne, S. M. 1994. Detection, isolation, and characterization of siderophores. Methods Enzymol. 235:329–344.
38. Roongsawang, N., K. Washio, and M. Morikawa. 2011. Diversity of nonribosomal peptide synthetases involved in the biosynthesis of lipopeptide biosurfactants. Int. J. Mol. Sci. 12:141–172.
39. Röttig, M., M. H. Medema, K. Blin, T. Weber, C. Rausch, and O. Kohlbacher. 2011. NRPSpredictor2—a web server for predicting NRPS adenylation domain specificity. Nucl. Acids Res. 39:W362–W367.
40. Royer, M., R. Koebnik, M. Marguerettaz, V. Barbe, G. Robin, C. Brin, et al. 2013. Genome mining reveals the genus Xanthomonas to be a promising reservoir for new bioactive non-ribosomally synthesized peptides. BMC Genom. 14:658.
41. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406–425.
42. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47–56.
43. Shanks, R. M. Q., N. C. Caiazza, S. M. Hinsa, C. M. Toutain, and G. A. O'Toole. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from Gram-negative bacteria. Appl. Environ. Microbiol. 72:5027–5036.
44. Sharma, A., and B. N. Johri. 2003. Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol. Res. 158:243–248.
45. Sokol, P. A., and D. E. Woods. 1988. Effect of pyochelin on Pseudomonas cepacia respiratory infections. Microb. Pathog. 5:197–205.
46. Tamura, K., M. Nei, and S. Kumar. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101:11030–11035.
47. Tamura, K., G. Stecher, D. Peterson, A. Filipski, and S. Kumar. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729.
48. Tawfik, K. A., P. Jeffs, B. Bray, G. Dubay, J. O. Falkinham, M. Mesbah, et al. 2010. Burkholdines 1097 and 1229, potent antifungal peptides from Burkholderia ambifaria 2.2N. Org. Lett. 12:664–666.
49. Vial, L., M. Groleau, V. Dekimpe, and E. Deziel. 2007. Burkholderia diversity and versatility: an inventory of the extracellular products. J. Microbiol. Biotechnol. 17:1407–1429.
50. Weber, T., K. Blin, S. Duddela, D. Krug, H.U. Kim, R. Bruccoleri, et al. 2015. antiSMASH 3.0 — a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucl Acids Res. 43:W237–W243.
51. Winsor, G. L., B. Khaira, T. Van Rossum, R. Lo, M. D. Whiteside, and F. S. L. Brinkman. 2008. The Burkholderia genome database: facilitating flexible queries and comparative analyses. Bioinformatics 24:2803–2804.