1887

Abstract

The Burkholderia cepacia complex (Bcc) comprises a group of 24 species, many of which are opportunistic pathogens of immunocompromised patients and also are widely distributed in agricultural soils. Several Bcc strains synthesize strain-specific antagonistic compounds. In this study, the broad killing activity of B. cenocepacia TAtl-371, a Bcc strain isolated from the tomato rhizosphere, was characterized. This strain exhibits a remarkable antagonism against bacteria, yeast and fungi including other Bcc strains, multidrug-resistant human pathogens and plant pathogens. Genome analysis of strain TAtl-371 revealed several genes involved in the production of antagonistic compounds: siderophores, bacteriocins and hydrolytic enzymes. In pursuit of these activities, we observed growth inhibition of Candida glabrata and Paraburkholderia phenazinium that was dependent on the iron concentration in the medium, suggesting the involvement of siderophores. This strain also produces a previously described lectin-like bacteriocin (LlpA88) and here this was shown to inhibit only Bcc strains but no other bacteria. Moreover, a compound with an m/z 391.2845 with antagonistic activity against Tatumella terrea SHS 2008 was isolated from the TAtl-371 culture supernatant. This strain also contains a phage-tail-like bacteriocin (tailocin) and two chitinases, but the activity of these compounds was not detected. Nevertheless, the previous activities are not responsible for the whole antimicrobial spectrum of TAtl-371 seen on agar plates, suggesting the presence of other compounds yet to be found. In summary, we observed a diversified antimicrobial activity for strain TAtl-371 and believe it supports the biotechnological potential of this Bcc strain as a source of new antimicrobials.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000675
2018-07-20
2019-08-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/9/1072.html?itemId=/content/journal/micro/10.1099/mic.0.000675&mimeType=html&fmt=ahah

References

  1. Sawana A, Adeolu M, Gupta RS. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 2014;5:429 [CrossRef][PubMed]
    [Google Scholar]
  2. Dobritsa AP, Samadpour M. Transfer of eleven Burkholderia species to the genus Paraburkholderia and proposal of Caballeronia gen. nov., a new genus to accommodate twelve species of Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol 2016;66:4085
    [Google Scholar]
  3. Lopes-Santos L, Castro DBA, Ferreira-Tonin M, Corrêa DBA, Weir BS et al. Reassessment of the taxonomic position of Burkholderia andropogonis and description of Robbsia andropogonis gen. nov., comb. nov. Antonie van Leeuwenhoek 2017;110:727736 [CrossRef][PubMed]
    [Google Scholar]
  4. Beukes CW, Palmer M, Manyaka P, Chan WY, Avontuur JR et al. Genome data provides high support for generic boundaries in Burkholderia sensu lato. Front Microbiol 2017;8:1154 [CrossRef][PubMed]
    [Google Scholar]
  5. Weber CF, King GM. Volcanic soils as sources of novel co-oxidizing Paraburkholderia and Burkholderia: Paraburkholderia hiiakae sp. nov., Paraburkholderia metrosideri sp. nov., Paraburkholderia paradisi sp. nov., Paraburkholderia peleae sp. nov., and Burkholderia alpina sp. nov. a member of the Burkholderia cepacia complex. Front Microbiol 2017;8:207 [CrossRef][PubMed]
    [Google Scholar]
  6. Baldwin A, Mahenthiralingam E, Drevinek P, Vandamme P, Govan JR et al. Environmental Burkholderia cepacia complex isolates in human infections. Emerg Infect Dis 2007;13:458–461 [CrossRef][PubMed]
    [Google Scholar]
  7. Vial L, Groleau MC, Dekimpe V, Déziel E. Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol 2007;17:1407[PubMed]
    [Google Scholar]
  8. Lim Y, Suh J-w, Kim S, Hyun B, Kim C et al. Cepacidine A, a novel antifungal antibiotic produced by Pseudomonas cepacia. J Antibiot 1994;47:1406
    [Google Scholar]
  9. Bisacchi GS, Hockstein DR, Koster WH, Parker WL, Rathnum ML et al. Xylocandin: a new complex of antifungal peptides. J Antibiot 1987;40:1520
    [Google Scholar]
  10. Schellenberg B, Bigler L, Dudler R. Identification of genes involved in the biosynthesis of the cytotoxic compound glidobactin from a soil bacterium. Environ Microbiol 2007;9:1640–1650 [CrossRef][PubMed]
    [Google Scholar]
  11. Gu G, Smith L, Wang N, Wang H, Lu SE. Biosynthesis of an antifungal oligopeptide in Burkholderia contaminans strain MS14. Biochem Biophys Res Commun 2009;380:328–332 [CrossRef][PubMed]
    [Google Scholar]
  12. Lu SE, Novak J, Austin FW, Gu G, Ellis D et al. Occidiofungin, a unique antifungal glycopeptide produced by a strain of Burkholderia contaminans. Biochemistry 2009;48:8312 [CrossRef][PubMed]
    [Google Scholar]
  13. Tawfik KA, Jeffs P, Bray B, Dubay G, Falkinham JO et al. Burkholdines 1097 and 1229, potent antifungal peptides from Burkholderia ambifaria 2.2N. Org Lett 2010;12:664–666 [CrossRef][PubMed]
    [Google Scholar]
  14. Lin Z, Falkinham JO, Tawfik KA, Jeffs P, Bray B et al. Burkholdines from Burkholderia ambifaria: antifungal agents and possible virulence factors. J Nat Prod 2012;75:1518–1523 [CrossRef][PubMed]
    [Google Scholar]
  15. Kirinuki T, Ichiba T, Katayama K. General survey of action site of altericidins on metabolism of Alternaria kikuchiana and Ustilago maydis. J Pestic Sci 1984;9:601–610 [CrossRef]
    [Google Scholar]
  16. de los Santos-Villalobos S, Barrera-Galicia GC, Miranda-Salcedo MA, Peña-Cabriales JJ. Burkholderia cepacia XXVI siderophore with biocontrol capacity against Colletotrichum gloeosporioides. World J Microbiol Biotechnol 2012;28:2615–2623 [CrossRef][PubMed]
    [Google Scholar]
  17. Groenhagen U, Baumgartner R, Bailly A, Gardiner A, Eberl L et al. Production of bioactive volatiles by different Burkholderia ambifaria strains. J Chem Ecol 2013;39:892–906 [CrossRef][PubMed]
    [Google Scholar]
  18. Cartwright DK, Chilton WS, Benson DM. Pyrrolnitrin and phenazine production by Pseudomonas cepacia, strain 5.5B, a biocontrol agent of Rhizoctonia solani. Appl Microbiol Biotechnol 1995;43:211–216 [CrossRef]
    [Google Scholar]
  19. Ghequire MG, de Canck E, Wattiau P, van Winge I, Loris R et al. Antibacterial activity of a lectin-like Burkholderia cenocepacia protein. Microbiologyopen 2013;2:566575 [CrossRef][PubMed]
    [Google Scholar]
  20. Ghequire MG, De Mot R. Distinct colicin M-like bacteriocin-immunity pairs in Burkholderia. Sci Rep 2015;5:17368 [CrossRef][PubMed]
    [Google Scholar]
  21. Marshall K, Shakya S, Greenhill AR, Padill G, Baker A et al. Antibiosis of Burkholderia ubonensis againist Burkholderia pseudomallei, the causative agent for melioidosis. Southeast Asian J Trop Med Public Health 2010;41:904[PubMed]
    [Google Scholar]
  22. Ghequire MGK, De Mot R. The Tailocin Tale: Peeling off Phage Tails. Trends Microbiol 2015;23:587–590 [CrossRef][PubMed]
    [Google Scholar]
  23. Yao GW, Duarte I, Le TT, Carmody L, LiPuma JJ et al. A Broad-Host-Range Tailocin from Burkholderia cenocepacia. Appl Environ Microbiol 2017;83:e03414-1603416 [CrossRef][PubMed]
    [Google Scholar]
  24. Ong KS, Aw YK, Lee LH, Yule CM, Cheow YL et al. Burkholderia paludis sp. nov., an antibiotic-siderophore producing novel Burkholderia cepacia complex species, isolated from Malaysian tropical peat swamp soil. Front Microbiol 2016;7:7 [CrossRef][PubMed]
    [Google Scholar]
  25. Deng P, Foxfire A, Xu J, Baird SM, Jia J et al. The siderophore product ornibactin is required for the bactericidal activity of Burkholderia contaminans MS14. Appl Environ Microbiol 2017;83:e00051-17 [CrossRef][PubMed]
    [Google Scholar]
  26. Parker WL, Rathnum ML, Seiner V, Trejo WH, Principe PA et al. Cepacin A and cepacin B, two new antibiotics produced by Pseudomonas cepacia. J Antibiot 1984;37:431–440 [CrossRef][PubMed]
    [Google Scholar]
  27. Hunter WJ, Manter DK. Antimicrobial properties of an oxidizer produced by Burkholderia cenocepacia P525. Curr Microbiol 2014;68:610–614 [CrossRef][PubMed]
    [Google Scholar]
  28. Mahenthiralingam E, Song L, Sass A, White J, Wilmot C et al. Enacyloxins are products of an unusual hybrid modular polyketide synthase encoded by a cryptic Burkholderia ambifaria Genomic Island. Chem Biol 2011;18:665–677 [CrossRef][PubMed]
    [Google Scholar]
  29. Arima K, Imanaka H, Kousaka M, Fukuta A, Tamura G. Pyrrolnitrin, a new antibiotic substance, produced by Pseudomonas. Agric Biol Chem 1964;28:575–576 [CrossRef]
    [Google Scholar]
  30. Imanaka H, Kousaka M, Tamura G, Arima K. Studies on pyrrolnitrin, a new antibiotic. II. Taxonomic studies on pyrrolnitrin-producing strain. J Antibiot 1965;18:205
    [Google Scholar]
  31. McLoughlin TJ, Quinn JP, Bettermann A, Bookland R. Pseudomonas cepacia suppression of sunflower wilt fungus and role of antifungal compounds in controlling the disease. Appl Environ Microbiol 1992;58:1760[PubMed]
    [Google Scholar]
  32. Jayaswal RK, Fernandez M, Upadhyay RS, Visintin L, Kurz M et al. Antagonism of Pseudomonas cepacia against phytopathogenic fungi. Curr Microbiol 1993;26:17–22 [CrossRef][PubMed]
    [Google Scholar]
  33. Burkhead KD, Schisler DA, Slininger PJ. Pyrrolnitrin production by biological control agent Pseudomonas cepacia B37w in culture and in colonized wounds of potatoes. Appl Environ Microbiol 1994;60:2031[PubMed]
    [Google Scholar]
  34. El-Banna N, Winkelmann G. Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes. J Appl Microbiol 1998;85:69–78 [CrossRef][PubMed]
    [Google Scholar]
  35. Hwang J, Chilton WS, Benson DM. Pyrrolnitrin production by Burkholderia cepacia and biocontrol of Rhizoctonia stem rot of poinsettia. Biological Control 2002;25:56–63 [CrossRef]
    [Google Scholar]
  36. Sultan Z, Park K, Lee SY, Park JK, Varughese T et al. Novel oxidized derivatives of antifungal pyrrolnitrin from the bacterium Burkholderia cepacia K87. J Antibiot 2008;61:420–425 [CrossRef][PubMed]
    [Google Scholar]
  37. Huang X, Zhang N, Yong X, Yang X, Shen Q. Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiol Res 2012;167:135–143 [CrossRef][PubMed]
    [Google Scholar]
  38. Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M et al. Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiologyopen 2016;5:512–526 [CrossRef][PubMed]
    [Google Scholar]
  39. Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martínez-Aguilar L. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 2007;73:5308–5319 [CrossRef][PubMed]
    [Google Scholar]
  40. Vandamme P, Holmes B, Coenye T, Goris J, Mahenthiralingam E et al. Burkholderia cenocepacia sp. nov. – a new twist to an old story. Res Microbiol 2003;154:91–96 [CrossRef][PubMed]
    [Google Scholar]
  41. Estrada-de los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J. Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol 2013;67:51–60 [CrossRef][PubMed]
    [Google Scholar]
  42. Baldwin A, Mahenthiralingam E, Thickett KM, Honeybourne D, Maiden MC et al. Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 2005;43:4665–4673 [CrossRef][PubMed]
    [Google Scholar]
  43. Sajjan US, Sun L, Goldstein R, Forstner JF. Cable (cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cblA major subunit pilin gene and novel morphology of the assembled appendage fibers. J Bacteriol 1995;177:10301038 [CrossRef][PubMed]
    [Google Scholar]
  44. Mahenthiralingam E, Simpson DA, Speert DP. Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J Clin Microbiol 1997;35:808[PubMed]
    [Google Scholar]
  45. de los Santos PE, Parret AH, de Mot R. Stress-related Pseudomonas genes involved in production of bacteriocin LlpA. FEMS Microbiol Lett 2005;244:243–250 [CrossRef][PubMed]
    [Google Scholar]
  46. Baños Guevara PE, Zavaleta Mejía E, Colinas León MT, Romero L I, Gutiérrez Alonso JG. Control biológico de Colletotrichum gloeosporioides [(Penz.) Penz. y Sacc.] en papaya maradol roja (Carica papaya L.) y fisiología postcosecha de frutos infectados. Rev Mex Fito 2004;22:
    [Google Scholar]
  47. Andrade-Pavón D, Cuevas-Hernández RI, Trujillo-Ferrara JG, Hernández-Rodríguez C, Ibarra JA et al. Recombinant 3-hydroxy 3-methyl glutaryl-CoA reductase from Candida glabrata (Rec-CgHMGR) obtained by heterologous expression, as a novel therapeutic target model for testing synthetic drugs. Appl Biochem Biotechnol 2017;182:1478–1490 [CrossRef][PubMed]
    [Google Scholar]
  48. Eid J, Fehr A, Gray J, Luong K, Lyle J et al. Real-time DNA sequencing from single polymerase molecules. Science 2009;323:133–138 [CrossRef][PubMed]
    [Google Scholar]
  49. Weber T, Blin K, Duddela S, Krug D, Kim HU et al. antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 2015;43:W237–W243 [CrossRef][PubMed]
    [Google Scholar]
  50. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010;5:e11147 [CrossRef][PubMed]
    [Google Scholar]
  51. Kumar H, Dubey RC, Maheshwari DK. Seed-coating fenugreek with Burkholderia rhizobacteria enhances yield in field trials and can combat Fusarium wilt. Rhizosphere 2017;3:92–99 [CrossRef]
    [Google Scholar]
  52. Schwyn B, Neilands JB. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987;160:47–56 [CrossRef][PubMed]
    [Google Scholar]
  53. Green M, Sambrook J. Molecular Clonin: A Laboratory Manual Cold Spring Harbor Laboratory Press; 2012
    [Google Scholar]
  54. Parret AH, Wyns L, de Mot R, Loris R. Overexpression, purification and crystallization of bacteriocin LlpA from Pseudomonas sp. BW11M1. Acta Crystallogr D Biol Crystallogr 2004;60:1922–1924 [CrossRef][PubMed]
    [Google Scholar]
  55. Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S et al. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int 2016;23:3984–3999 [CrossRef][PubMed]
    [Google Scholar]
  56. Depoorter E, Bull MJ, Peeters C, Coenye T, Vandamme P et al. Burkholderia: an update on taxonomy and biotechnological potential as antibiotic producers. Appl Microbiol Biotechnol 2016;100:5215–5229 [CrossRef][PubMed]
    [Google Scholar]
  57. Tscherner M, Schwarzmüller T, Kuchler K. Pathogenesis and antifungal drug resistance of the human fungal pathogen Candida glabrata. Pharmaceuticals 2011;4:169–186 [CrossRef]
    [Google Scholar]
  58. Salehi M, Ghasemian A, Shokouhi Mostafavi SK, Nojoomi F, Ashiani D et al. The epidemiology of Candida species isolated from urinary tract infections. Arch Clin Infect Dis 2016;11:e37743 [CrossRef]
    [Google Scholar]
  59. Ben Ayed H, Hmidet N, Béchet M, Chollet M, Chataigné G et al. Identification and biochemical characteristics of lipopeptides from Bacillus mojavensis A21. Process Biochem 2014;49:1699–1707 [CrossRef]
    [Google Scholar]
  60. Bizani D, Brandelli A. Characterization of a bacteriocin produced by a newly isolated Bacillus sp. strain 8 A. J Appl Microbiol 2002;93:512–519 [CrossRef][PubMed]
    [Google Scholar]
  61. Shin MS, Han SK, Ryu JS, Kim KS, Lee WK. Isolation and partial characterization of a bacteriocin produced by Pediococcus pentosaceus K23-2 isolated from Kimchi. J Appl Microbiol 2008;105:331–339 [CrossRef][PubMed]
    [Google Scholar]
  62. Teixeira ML, Dalla Rosa A, Brandelli A. Characterization of an antimicrobial peptide produced by Bacillus subtilis subsp. spizezinii showing inhibitory activity towards Haemophilus parasuis. Microbiology 2013;159:980–988 [CrossRef][PubMed]
    [Google Scholar]
  63. Bernal G, Illanes A, Ciampi L. Isolation and partial purification of a metabolite from a mutant strain of Bacillus sp. with antibiotic activity against plant pathogenic agents. Electron J Biotechnol 2002;5:7 [CrossRef]
    [Google Scholar]
  64. Quan CS, Zheng W, Liu Q, Ohta Y, Fan SD. Isolation and characterization of a novel Burkholderia cepacia with strong antifungal activity against Rhizoctonia solani. Appl Microbiol Biotechnol 2006;72:1276–1284 [CrossRef][PubMed]
    [Google Scholar]
  65. Ahmed E, Holmström SJ. Siderophores in environmental research: roles and applications. Microb Biotechnol 2014;7:196–208 [CrossRef][PubMed]
    [Google Scholar]
  66. Parret AH, Schoofs G, Proost P, De Mot R. Plant lectin-like bacteriocin from a rhizosphere-colonizing Pseudomonas isolate. J Bacteriol 2003;185:897–908 [CrossRef][PubMed]
    [Google Scholar]
  67. Ghequire MG, Li W, Proost P, Loris R, de Mot R. Plant lectin-like antibacterial proteins from phytopathogens Pseudomonas syringae and Xanthomonas citri. Environ Microbiol Rep 2012;4:373–380 [CrossRef][PubMed]
    [Google Scholar]
  68. Ghequire MG, Garcia-Pino A, Lebbe EK, Spaepen S, Loris R et al. Structural determinants for activity and specificity of the bacterial toxin LlpA. PLoS Pathog 2013;9:e1003199 [CrossRef][PubMed]
    [Google Scholar]
  69. Yao GW, Duarte I, Le TT, Carmody L, LiPuma JJ et al. A broad-host-range tailocin from Burkholderia cenocepacia. Appl Environ Microbiol 2017;83:e03414-16 [CrossRef][PubMed]
    [Google Scholar]
  70. Swain DM, Yadav SK, Tyagi I, Kumar R, Kumar R et al. A prophage tail-like protein is deployed by Burkholderia bacteria to feed on fungi. Nat Commun 2017;8:404 [CrossRef][PubMed]
    [Google Scholar]
  71. Shimosaka M, Fukumori Y, Narita T, Zhang X, Kodaira R et al. The bacterium Burkholderia gladioli strain CHB101 produces two different kinds of chitinases belonging to families 18 and 19 of the glycosyl hydrolases. J Biosci Bioeng 2001;91:103–105 [CrossRef][PubMed]
    [Google Scholar]
  72. Kong H, Shimosaka M, Ando Y, Nishiyama K, Fujii T et al. Species-specific distribution of a modular family 19 chitinase gene in Burkholderia gladioli. FEMS Microbiol Ecol 2001;37:135–141 [CrossRef]
    [Google Scholar]
  73. Ogawa K, Yoshida N, Kariya K, Ohnishi C, Ikeda R. Purification and characterization of a novel chitinase from Burkholderia cepacia strain KH2 isolated from the bed log of Lentinus edodes, Shiitake mushroom. J Gen Appl Microbiol 2002;48:25–33 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000675
Loading
/content/journal/micro/10.1099/mic.0.000675
Loading

Data & Media loading...

Supplementary File 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