1887

Abstract

A novel group of nitrogen-fixing plant-associated species has emerged in the last few years. The purpose of this investigation was to determine if these species possess an -acylhomoserine lactone (AHL) quorum-sensing (QS) cell–cell signalling system, and whether it is important for nitrogen fixation and other phenotypic features in . It was determined that , and other members of this species cluster, contain at least one highly conserved system, designated BraI/R, which produces and responds to -dodecanoyl-3-oxo-homoserine lactone (C12-3-oxo-AHL). The BraI/R AHL QS is not involved in the regulation of nitrogen fixation or in several other important phenotypes, indicating that it may not be a global regulatory system. The BraI/R system is similar to LasI/R of and, as with , there is a repressor gene, , between the genes. normally synthesizes very low levels of C12-3-oxo-AHL, but the situation dramatically changes when RsaL is missing since an mutant displays a marked increase in AHL production. This unique stringent regulation indicates that RsaL could be an on/off switch for AHL QS in and the ability to produce very high levels of AHL also questions the role of this molecule in the novel group of . The presence of a well-conserved and distinct AHL QS system among all the diazotrophic is a further indication that they are closely related, and that this system might play an important and conserved role in the lifestyle of this novel group of bacterial species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017780-0
2008-07-01
2020-03-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/7/2048.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017780-0&mimeType=html&fmt=ahah

References

  1. Achouak W., Christen R., Barakat M., Martel M. H., Heulin T.. 1999; Burkholderia caribensis sp. nov., an exopolysaccharide-producing bacterium isolated from vertisol microaggregates in Martinique. Int J Syst Bacteriol49:787–794
    [Google Scholar]
  2. Alexeyev M. F.. 1999; The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques26:824–826
    [Google Scholar]
  3. Baldani J. I., Caruso L., Baldani V. L. D., Goi S. R., Döbereiner J.. 1997a; Recent advances in BNF with non-legume plants. Soil Biol Biochem29:911–922
    [Google Scholar]
  4. Baldani V. L. D., Oliveira E., Balota E., Baldani J. I., Kirchhof G., Döbereiner J.. 1997b; Burkholderia brasilensis sp. nov. uma nova espécie de bactéria diazotrófica endofítica. An Acad Bras Cienc69:116
    [Google Scholar]
  5. Baldani V. L. D., Baldani J. I., Döbereiner J.. 2000; Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils30:485–491
    [Google Scholar]
  6. Bertani I., Venturi V.. 2004; Regulation of the N-acyl homoserine lactone-dependent quorum-sensing system in rhizosphere Pseudomonas putida WCS358 and cross-talk with the stationary-phase RpoS sigma factor and the global regulator GacA. Appl Environ Microbiol70:5493–5502
    [Google Scholar]
  7. Better M., Lewis B., Corbin D., Ditta G., Helinski D. R.. 1983; Structural relationships among Rhizobium meliloti symbiotic promoters. Cell35:479–485
    [Google Scholar]
  8. Bramer C. O., Vandamme P., da Silva L. F., Gomez J. G., Steinbuchel A.. 2001; Polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil. Int J Syst Evol Microbiol51:1709–1713
    [Google Scholar]
  9. Burris R. H.. 1972; Nitrogen fixation – assay methods and techniques. Methods Enzymol24:415–431
    [Google Scholar]
  10. Caballero-Mellado J., Martinez-Aguilar L., Paredes-Valdez G., Estrada-de los Santos P.. 2004; Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol54:1165–1172
    [Google Scholar]
  11. Caballero-Mellado J., Onofre-Lemus J., Estrada-de los Santos P., Martinez-Aguilar L.. 2007; The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol73:5308–5319
    [Google Scholar]
  12. Chen W. M., James E. K., Coenye T., Chou J. H., Barrios E., de Faria S. M., Elliott G. N., Sheu S. Y., Sprent J. I., Vandamme P.. other authors 2006; Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol56:1847–1851
    [Google Scholar]
  13. Coenye T., LiPuma J. J.. 2003; Molecular epidemiology of Burkholderia species. Front Biosci8:e55–e67
    [Google Scholar]
  14. Coenye T., Vandamme P.. 2003; Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol5:719–729
    [Google Scholar]
  15. Coenye T., Laevens S., Willems A., Ohlen M., Hannant W., Govan J. R., Gillis M., Falsen E., Vandamme P.. 2001; Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples. Int J Syst Evol Microbiol51:1099–1107
    [Google Scholar]
  16. Coenye T., Henry D., Speert D. P., Vandamme P.. 2004; Burkholderia phenoliruptrix sp. nov., to accommodate the 2,4,5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100. Syst Appl Microbiol27:623–627
    [Google Scholar]
  17. Devescovi G., Bigirimana J., Degrassi G., Cabrio L., LiPuma J. J., Kim J., Hwang I., Venturi V.. 2007; Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl Environ Microbiol73:4950–4958
    [Google Scholar]
  18. Dixon R., Kahn D.. 2004; Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol2:621–631
    [Google Scholar]
  19. Eberl L.. 2006; Quorum sensing in the genus Burkholderia. Int J Med Microbiol296:103–110
    [Google Scholar]
  20. Elliott G. N., Chen W. M., Chou J. H., Wang H. C., Sheu S. Y., Perin L., Reis V. M., Moulin L., Simon M. F.. other authors 2007; Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol173:168–180
    [Google Scholar]
  21. Estrada-de los Santos P., Bustillos-Cristales R., Caballero-Mellado J.. 2001; Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol67:2790–2798
    [Google Scholar]
  22. Figurski D. H., Helinski D. R.. 1979; Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A76:1648–1652
    [Google Scholar]
  23. Fuqua C., Parsek M. R., Greenberg E. P.. 2001; Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet35:439–468
    [Google Scholar]
  24. Gillis M., Tran Van V., Bardin R., Goor M., Hebbar P., Willems A., Sergers P., Kersters K., Heulin T., Fernandez M.. 1995; Polyphasic taxonomy in the genus Burkholderia leading to an embedded description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol45:274–289
    [Google Scholar]
  25. Gonzalez C. F., Venturi V., Engledow A. S.. 2007; The phytopathogenic Burkholderia. In Burkholderia: Molecular Microbiology and Genomics pp153–176 Edited by Coeyne T., Vandamme P.. Norwich, UK: Horizon Bioscience;
  26. Goris J., Dejonghe W., Falsen E., De Clerck E., Geeraerts B., Willems A., Top E. M., Vandamme P., De Vos P.. 2002; Diversity of transconjugants that acquired plasmid pJP4 or pEMT1 after inoculation of a donor strain in the A- and B-horizon of an agricultural soil and description of Burkholderia hospita sp.nov. and Burkholderia terricola sp. nov. Syst Appl Microbiol25:340–352
    [Google Scholar]
  27. Goris J., De Vos P., Caballero-Mellado J., Park J., Falsen E., Quensen J. F. III, Tiedje J. M., Vandamme P.. 2004; Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol54:1677–1681
    [Google Scholar]
  28. Huber B., Riedel K., Hentzer M., Heydorn A., Gotschlich A., Givskov M., Molin S., Eberl L.. 2001; The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology147:2517–2528
    [Google Scholar]
  29. Jain D. K., Patriquin D. G.. 1984; Characterization of a substance produced by Azospirillum which causes branching of wheat root hairs. Can J Microbiol313:206–210
    [Google Scholar]
  30. Juhas M., Eberl L., Tummler B.. 2005; Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol7:459–471
    [Google Scholar]
  31. Kim J., Kim J. G., Kang Y., Jang J. Y., Jog G. J., Lim J. Y., Kim S., Suga H., Nagamatsu T., Hwang I.. 2004; Quorum sensing and the LysR-type transcriptional activator ToxR regulate toxoflavin biosynthesis and transport in Burkholderia glumae. Mol Microbiol54:921–934
    [Google Scholar]
  32. King E. O., Ward M. K., Raney D. E.. 1954; Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med44:301–307
    [Google Scholar]
  33. Kohler T., Curty L. K., Barja F., van Delden C., Pechere J. C.. 2000; Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol182:5990–5996
    [Google Scholar]
  34. LiPuma J. J.. 2003; Burkholderia and emerging pathogens in cystic fibrosis. Semin Respir Crit Care Med24:681–692
    [Google Scholar]
  35. Mahenthiralingam E., Urban T. A., Goldberg J. B.. 2005; The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol3:144–156
    [Google Scholar]
  36. Martínez-Aguilar L., Díaz R., Pe·a-Cabrieles J. J., Estrada-de Los Santos P., Dunn M. F., Caballero-Mellado J.. 2008; Multichromosomal genome structure and confirmation of diazotrophy in novel plant-associated Burkholderia species. Appl Environ Microbiol in press
    [Google Scholar]
  37. McClean K. H., Winson M. K., Fish L., Taylor A., Chhabra S. R., Camara M., Daykin M., Lamb J. H., Swift S.. other authors 1997; Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology143:3703–3711
    [Google Scholar]
  38. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
  39. Murray T. S., Kazmierczak B. I.. 2006; FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J Bacteriol188:6995–7004
    [Google Scholar]
  40. O'Sullivan L. A., Mahenthiralingam E.. 2005; Biotechnological potential within the genus Burkholderia. Lett Appl Microbiol41:8–11
    [Google Scholar]
  41. Perin L., Martinez-Aguilar L., Castro-Gonzalez R., Estrada-de los Santos P., Cabellos-Avelar T., Guedes H. V., Reis V. M., Caballero-Mellado J.. 2006a; Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Appl Environ Microbiol72:3103–3110
    [Google Scholar]
  42. Perin L., Martinez-Aguilar L., Paredes-Valdez G., Baldani J. I., Estrada-de los Santos P., Reis V. M., Caballero-Mellado J.. 2006b; Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize. Int J Syst Evol Microbiol56:1931–1937
    [Google Scholar]
  43. Piper K. R., von Bodman S. B., Farrand S. K.. 1993; Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature362:448–450
    [Google Scholar]
  44. Rampioni G., Bertani I., Zennaro E., Polticelli F., Venturi V., Leoni L.. 2006; The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter. J Bacteriol188:815–819
    [Google Scholar]
  45. Rampioni G., Polticelli F., Bertani I., Righetti K., Venturi V., Zennaro E., Leoni L.. 2007a; The Pseudomonas quorum-sensing regulator RsaL belongs to the tetrahelical superclass of H-T-H proteins. J Bacteriol189:1922–1930
    [Google Scholar]
  46. Rampioni G., Schuster M., Greenberg E. P., Bertani I., Grasso M., Venturi V., Zennaro E., Leoni L.. 2007b; RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa. Mol Microbiol66:1557–1565
    [Google Scholar]
  47. Reis V. M., Estrada-de los Santos P., Tenorio-Salgado S., Vogel J., Stoffels M., Guyon S., Mavingui P., Baldani V. L., Schmid M.. other authors 2004; Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol54:2155–2162
    [Google Scholar]
  48. Riedel K., Hentzer M., Geisenberger O., Huber B., Steidle A., Wu H., Høiby N., Givskov M., Molin S., Eberl L.. 2001; N-Acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology147:3249–3262
    [Google Scholar]
  49. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
  50. Schwyn B., Neilands J. B.. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem160:47–56
    [Google Scholar]
  51. Sessitsch A., Coenye T., Sturz A. V., Vandamme P., Barka E. A., Salles J. F., Van Elsas J. D., Faure D., Reiter B.. other authors 2005; Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol55:1187–1192
    [Google Scholar]
  52. Shaw P. D., Ping G., Daly S. L., Cha C., Rinehart K. L., Farrand S. K., Cronan J. E. Jr. 1997; Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci U S A94:6036–6041
    [Google Scholar]
  53. Simon R., Priefer U., Puhler A.. 1983; A broad-host-range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology1:784–791
    [Google Scholar]
  54. Smith R. S., Iglewski B. H.. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol6:56–60
    [Google Scholar]
  55. Solis R., Bertani I., Degrassi G., Devescovi G., Venturi V.. 2006; Involvement of quorum sensing and RpoS in rice seedling blight caused by Burkholderia plantarii. FEMS Microbiol Lett259:106–112
    [Google Scholar]
  56. Stachel S. E., An G., Flores C., Nester E. W.. 1985; A Tn 3 lacZ transposon for the random generation of β-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J4:891–898
    [Google Scholar]
  57. Staskawicz B., Dahlbeck D., Keen N., Napoli C.. 1987; Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol169:5789–5794
    [Google Scholar]
  58. Tang Y. W., Bonner J.. 1948; The enzymatic inactivation of indole acetic acid; the physiology of the enzyme. Am J Bot35:570–578
    [Google Scholar]
  59. Vandamme P., Goris J., Chen W. M., de Vos P., Willems A.. 2002; Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol25:507–512
    [Google Scholar]
  60. Venturi V.. 2006; Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev30:274–291
    [Google Scholar]
  61. Venturi V., Friscina A., Bertani I., Devescovi G., Aguilar C.. 2004; Quorum sensing in the Burkholderia cepacia complex. Res Microbiol155:238–244
    [Google Scholar]
  62. Vial L., Groleau M. C., Dekimpe V., Deziel E.. 2007; Burkholderia diversity and versatility: an inventory of the extracellular products. J Microbiol Biotechnol17:1407–1429
    [Google Scholar]
  63. Viallard V., Poirier I., Cournoyer B., Haurat J., Wiebkin S., Ophel-Keller K., Balandreau J.. 1998; Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of[ Pseudomonas] phenazinium, [ Pseudomonas] pyrrocinia and [ Pseudomonas] glathei as Burkholderia. Int J Syst Bacteriol48:549–563
    [Google Scholar]
  64. Weber O. B., Baldani J. I., Döbereiner J.. 2000; Bactérias diazotróficas em mudas de bananeira. Pesq Agropec Bras35:2227–2285
    [Google Scholar]
  65. Yang H. C., Im W. T., Kim K. K., An D. S., Lee S. T.. 2006; Burkholderia terrae sp. nov., isolated from a forest soil. Int J Syst Evol Microbiol56:453–457
    [Google Scholar]
  66. Zhang H., Hanada S., Shigematsu T., Shibuya K., Kamagata Y., Kanagawa T., Kurane R.. 2000; Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE. Int J Syst Evol Microbiol50:743–749
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/017780-0
Loading
/content/journal/micro/10.1099/mic.0.2008/017780-0
Loading

Data & Media loading...

Most cited this month

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