Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance

Nature Communications

Volumn 4, Issue , 2013, Pages

  Kim, Kwang Sun ^a,b   Lee, Soohyun ^a   Ryu, Choong Min ^a,b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 BUTANEDIONE; GLYOXYLIC ACID; TRANSCRIPTION FACTOR SOX;

ANTIBIOTIC RESISTANCE; ARRAY; COLIFORM BACTERIUM; GENE EXPRESSION; INTERSPECIFIC INTERACTION; MOLECULAR ANALYSIS; ORGANIC ACID; PHYSIOLOGY; SIGNAL; VOLATILE ORGANIC COMPOUND;

ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SENSING; ESCHERICHIA COLI; GENE ACTIVITY; GENE EXPRESSION; LOCOMOTION; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION;

AMPICILLIN; ANTI-BACTERIAL AGENTS; BACILLUS SUBTILIS; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; KINETICS; LOCOMOTION; PHENOTYPE; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; VOLATILE ORGANIC COMPOUNDS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84878525214     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2789     Document Type: Article

References (69)

1. Sifri, C. D. Quorum sensing: Bacteria talk sense. Clin. Infect. Dis. 47, 1070-1076 (2008)
2. Mangwani, N., Dash, H. R., Chauhan, A. & Das, S. Bacterial quorum sensing: functional features and potential applications in biotechnology. J. Mol. Microbiol. Biotechnol. 22, 215-227 (2012)
3. Baca-DeLancey, R. R., South, M. M., Ding, X. & Rather, P. N. Escherichia coli genes regulated by cell-to-cell signaling. Proc. Natl Acad. Sci. USA 96, 4610-4614 (1999) (Pubitemid 29190384)
4. Davies, D. G. et al. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298 (1998) (Pubitemid 28178075)
5. Piper, K. R., Beck von Bodman, S. & Farrand, S. K. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362, 448-450 (1993) (Pubitemid 23107367)
6. Lee, J. H. & Lee, J. Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34, 426-444 (2010)
7. Hughes, D. T. & Sperandio, V. Inter-kingdom signaling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6, 111-120 (2008)
8. Williams, P. Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 153, 3923-3938 (2007)
9. Ng, W. L. & Bassler, B. L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43, 197-222 (2009)
10. Hayes, C. S., Aoki, S. K. & Low, D. A. Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 44, 71-90 (2010)
11. Pesci, E. C. New signal molecules on the quorum sensing block: response. Trends Microbiol. 8, 103-104 (2000) (Pubitemid 30155477)
12. Kesarwani, M. et al. A quorum sensing regulated small volatile molecule reduces acute virulence and promotes chromic infection phenotypes. PLoS Pathog. 7, e1002192 (2011)
13. Heal, R. D. & Parsons, A. T. Novel intercellular communication system in Escherichia coli that confers antibiotic resistance between physically separated populations. J. Appl. Microbiol. 92, 1116-1122 (2002) (Pubitemid 34535492)
14. Bernier, S. P., Le'toffé, S., Delepierre, M. & Ghigo, J. M. Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol. Microbiol. 81, 705-716 (2011)
15. Zou, C. S., Mo, M. H., Gu, Y. Q., Zhou, J. P. & Zhang, K. Q. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol. Biochem. 39, 2371-2379 (2007)
16. Kai, M. et al. Bacterial volatiles and their action potential. Appl. Microbiol. Biotechnol. 81, 1001-1012 (2009)
17. Bari, W., Song, Y. & Yoon, S. S. Suppressed induction of proinflammatory cytokines by a unique metabolite produced by Vibrio cholera O1 El Tor biotype in cultured host cells. Infect. Immun. 79, 3149-3158.
18. Ryu, C. M. et al. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 4927-4932 (2003)
19. Ryu, C. M. et al. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134, 1017-1026 (2004)
20. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011)
21. Fierer, N. et al. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl Acad. Sci. USA 109, 21390-21395 (2012)
22. Aizenberg-Gershtein, Y., Vaizel-Ohayon, D. & Halpern, M. Structure of bacterial communities in diverse freshwater habitats. Can. J. Microbiol. 58, 326-335 (2012)
23. Brandl, K. et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455, 804-807 (2008)
24. Burkholder, P. R. & Giles, N. H. Induced biochemical mutations in Bacillus subtilis. Amer. J. Bot. 34, 345 (1947)
25. Ara, K. et al. Bacillus minimum genome factory: effective utilization of microbial genome information. Biotechnol. Appl. Biochem. 46, 169-178 (2007) (Pubitemid 46587485)
26. Ashburner, M. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (2000) (Pubitemid 30257031)
27. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. & Tanabe, M. KEGG for integration and interpretation of large-scale molecular datasets. Nucleic Acids Res. 40, D109-D114 (2012)
28. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006)
29. Datsenko, K. & Wanner, B. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640- 6645 (2000) (Pubitemid 30412767)
30. Wood, T. K., Gonza'lez Barrios, A. F., Herzberg, M. & Lee, J. Motility influences biofilm architecture in Escherichia coli. Appl. Microbiol. Biotechnol. 72, 361-367 (2006) (Pubitemid 44273060)
31. Bachman, B. J. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36, 525-557 (1972)
32. Keren, I., Shah, D., Spoering, A., Kaldalu, N. & Lewis, K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180 (2004) (Pubitemid 39603206)
33. Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A. & Collins, J. J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797-810 (2007) (Pubitemid 47332566)
34. Shah, D. et al. Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6, 53 (2006)
35. Lewis, K. Multidrug tolerance of biofilms and persister cells. In Bacterial Biofilms. (ed. Romeo, T.) 107-131 (Springer-Verlag, Berlin, Germany, 2008)
36. Ezra, D., Hess, W. M. & Strobel, G. A. New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 150, 4023- 4031 (2004) (Pubitemid 40045331)
37. Strobel, G. A. et al. Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: isolation, characterization and experimental establishment in the host plant. Microbiology 153, 2613-2620 (2007) (Pubitemid 47262050)
38. Bukvicki, D. et al. Identification of volatile components of Liverwort (Porella cordaeana) extracts using GC/MS-SPME and their antimicrobial activity. Molecules 17, 6982-6995 (2012)
39. Bochner, B. R., Gadzinski, P. & Panomitros, E. Phenotype microarrays for highthroughput phenotypic testing and assay of gene function. Genome Res. 11, 1246-1255 (2001) (Pubitemid 32677299)
40. Moyed, H. S. & Bertrand, K. P. Hipa, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155, 768-775 (1983) (Pubitemid 13048115)
41. Korch, S. B., Henderson, T. A. & Hill, T. M. Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199-1213 (2003) (Pubitemid 37475853)
42. Korch, S. B. & Hill, T. M. Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J. Bacteriol. 188, 3626-3836 (2006)
43. Schumacher, M. A. et al. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323, 396-401 (2009)
44. Farag, M. A., Ryu, C. M., Summer, L. W. & Pare, P. W. GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67, 2262-2268 (2006) (Pubitemid 44415915)
45. Lee, D. J., Minchin, S. D. & Busby, S. J. W. Activating transcription in bacteria. Annu. Rev. Microbiol. 66, 125-152 (2012)
46. Zaslaver, A. et al. A comprehensive library of fluorescent transcriptional reporters of Escherichia coli. Nat. Methods 3, 623-628 (2006) (Pubitemid 44123429)
47. Keseler, I. M. et al. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41, D605-D612 (2013)
48. Levy, S. B. & Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10, S122-S129 (2004) (Pubitemid 40018235)
49. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug. Discov. 2, 114-122 (2003) (Pubitemid 37361643)
50. Adnan, M., Morton, G., Singh, J. & Hadi, S. Contribution of rpoS and bolA genes in biofilm formation in Escherichia coli K-12 MG1655. Mol. Cell. Biochem. 342, 207-213 (2010)
51. Nijland, R. & Burgess, J. G. Bacterial olfaction. Biotechnol. J. 5, 974-977 (2010)
52. Betterton, E. A. The partitioning of ketones between the gas and aqueous phases. Atmos. Environ. 25A, 1473-1477 (1991)
53. Saxena, P. & Hildermann, L. M. Water-soluble organics in atmosphere particles: a critical review of the literature and application of thermodynamics to identify candidate compounds. J. Atmos. Chem. 24, 57-109 (1996)
54. Jay, J. M. Antimicrobial properties of diacetyl. Appl. Environ. Microbiol. 44, 525-532 (1982) (Pubitemid 12065605)
55. Hedgecock, L. W. & Jones, L. R. Antibacterial activity of diacetyl. Bact. Proc. 127-128 (1950)
56. Martineau, B. & Henick-Kling, T. Formation and degradation of diacetyl in wine during alcoholic fermentation with Saccharomyces cerevisiae strain EC 1118 and malolactic fermentation with Leuconostoc oenos strain MCW. Am. J. Enol. Vitic 46, 442-448 (1995)
57. Fedan, J. S., Dowdy, J. A., Fedan, K. B. & Hubbs, A. F. Popcorn worker's lung: In vitro exposure to diacetyl, an ingredient in microwave popcorn butter flavoring, increases reactivity to methacholine. Toxicol. Appl. Pharmacol. 215, 17-22 (2006) (Pubitemid 44118401)
58. Hubbs, A. F. et al. Respiratory toxicologic pathology of inhaled diacetyl in sprague-dawley rats. Toxicol. Pathol. 36, 330-344 (2008) (Pubitemid 351534484)
59. Morgan, D. L., Flake, G. P., Kirby, P. J. & Paalmer, S. M. Respiratory toxicity of diacetyl in C57BL/6 mice. Toxicol. Sci. 103, 169-180 (2008) (Pubitemid 351524488)
60. Bokulich, N. A., Joseph, C. M. L., Allen, G., Benson, A. K. & Mills, D. A. Next-generation sequencing reveals significant bacterial diversity of botrytized wine. PLoS One 7, e36357 (2012)
61. Lim, J. et al. Complete genome sequence of Burkholderia glumae BGR1. J. Bacteriol. 191, 3758-3759 (2009)
62. Kornberg, H. L. The role and control of the glyoxylate cycle in Esherichia coli. Biochem J. 99, 1-11 (1966)
63. Alber, B. E., Spanheimer, R., Ebenau-Jehle, C. & Fuchs, G. Study of an alternate glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol. Microbiol. 61, 297-309 (2006) (Pubitemid 44356564)
64. Winsor, G. L. et al. Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-600 (2011)
65. Kim, J. F. et al. Genome sequence of the polymyxin-producing plant-probiotic rhizobacterium Paenibacillus polymyxa E681. J. Bacteriol. 192, 6103-6104 (2010)
66. Yoon, S. H. et al. Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol. 13, R37 (2012)
67. Saeed, A. I. et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378 (2003) (Pubitemid 36184095)
68. Kim, K. S. et al. A novel fluorescent reporter system for monitoring and identifying RNase III activity and its target RNAs. RNA Biol. 9, 1167-1176 (2012)
69. Ren, D. et al. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl. Environ. Microbiol. 71, 4022-4034 (2005). (Pubitemid 40980575)