Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa

Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen T, Dow JM (2008)
Molecular Microbiology 68(1): 75-86.

Journal Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ;
Abstract
Interspecies signalling through the action of diffusible signal molecules can influence the behaviour of organisms growing in polymicrobial communities. Stenotrophomonas maltophilia and Pseudomonas aeruginosa occur ubiquitously in the environment and can be found together in diverse niches including the rhizosphere of plants and the cystic fibrosis lung. In mixed species biofilms, S. maltophilia substantially influenced the architecture of P. aeruginosa structures, which developed as extended filaments. This effect depended upon the synthesis of the diffusible signal factor (DSF) by S. maltophilia and could be mimicked by the addition of synthetic DSF. This response of P. aeruginosa to DSF required PA1396, a sensor kinase with an input domain of related amino acid sequence to the sensory input domain of RpfC, which is responsible for DSF perception in xanthomonads. Mutation of PA1396 or addition of DSF to P. aeruginosa led to increased levels of a number of proteins with roles in bacterial stress tolerance, including those implicated in resistance to cationic antimicrobial peptides. This effect was associated with increased tolerance to polymyxins. Homologues of PA1396 occur in a number of phytopathogenic and plant-associated pseudomonads, suggesting that modulation of bacterial behaviour through DSF-mediated interspecies signalling with xanthomonads is a phenomenon that occurs widely.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

Ryan RP, Fouhy Y, Garcia BF, et al. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Molecular Microbiology. 2008;68(1):75-86.
Ryan, R. P., Fouhy, Y., Garcia, B. F., Watt, S. A., Niehaus, K., Yang, L., Tolker-Nielsen, T., et al. (2008). Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Molecular Microbiology, 68(1), 75-86.
Ryan, R. P., Fouhy, Y., Garcia, B. F., Watt, S. A., Niehaus, K., Yang, L., Tolker-Nielsen, T., and Dow, J. M. (2008). Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Molecular Microbiology 68, 75-86.
Ryan, R.P., et al., 2008. Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Molecular Microbiology, 68(1), p 75-86.
R.P. Ryan, et al., “Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa”, Molecular Microbiology, vol. 68, 2008, pp. 75-86.
Ryan, R.P., Fouhy, Y., Garcia, B.F., Watt, S.A., Niehaus, K., Yang, L., Tolker-Nielsen, T., Dow, J.M.: Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Molecular Microbiology. 68, 75-86 (2008).
Ryan, Robert P., Fouhy, Yvonne, Garcia, Belen Fernandez, Watt, Steven A., Niehaus, Karsten, Yang, Liang, Tolker-Nielsen, Tim, and Dow, J. Maxwell. “Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa”. Molecular Microbiology 68.1 (2008): 75-86.
This data publication is cited in the following publications:
This publication cites the following data publications:

58 Citations in Europe PMC

Data provided by Europe PubMed Central.

Control of Biofilms with the Fatty Acid Signaling Molecule cis-2-Decenoic Acid.
Marques CN, Davies DG, Sauer K., Pharmaceuticals (Basel) 8(4), 2015
PMID: 26610524
Cooperative pathogenicity in cystic fibrosis: Stenotrophomonas maltophilia modulates Pseudomonas aeruginosa virulence in mixed biofilm.
Pompilio A, Crocetta V, De Nicola S, Verginelli F, Fiscarelli E, Di Bonaventura G., Front Microbiol 6(), 2015
PMID: 26441885
Decoding the genetic and functional diversity of the DSF quorum-sensing system in Stenotrophomonas maltophilia.
Huedo P, Yero D, Martinez-Servat S, Ruyra A, Roher N, Daura X, Gibert I., Front Microbiol 6(), 2015
PMID: 26284046
Fungal β-1,3-glucan increases ofloxacin tolerance of Escherichia coli in a polymicrobial E. coli/Candida albicans biofilm.
De Brucker K, Tan Y, Vints K, De Cremer K, Braem A, Verstraeten N, Michiels J, Vleugels J, Cammue BP, Thevissen K., Antimicrob. Agents Chemother. 59(6), 2015
PMID: 25753645
Antimicrobial resistance in some gram-negative bacteria isolated from the bovine ejaculate.
Kilburn C, Rooks DJ, McCarthy AJ, Murray RD., Reprod. Domest. Anim. 48(3), 2013
PMID: 23331295
Implications of interspecies signaling for virulence of bacterial and fungal pathogens.
Holcombe LJ, O'Gara F, Morrissey JP., Future Microbiol 6(7), 2011
PMID: 21797692

40 References

Data provided by Europe PubMed Central.

Quorum sensing in Escherichia coli and Salmonella.
Walters M, Sperandio V., Int. J. Med. Microbiol. 296(2-3), 2006
PMID: 16487745
Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover.
Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Camara M, Williams P, Dow JM., Proc. Natl. Acad. Sci. U.S.A. 103(17), 2006
PMID: 16611728
Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth.
Rickard AH, Palmer RJ Jr, Blehert DS, Campagna SR, Semmelhack MF, Egland PG, Bassler BL, Kolenbrander PE., Mol. Microbiol. 60(6), 2006
PMID: 16796680
Contribution of the PhoP-PhoQ and PmrA-PmrB two-component regulatory systems to Mg2+-induced gene regulation in Pseudomonas aeruginosa.
McPhee JB, Bains M, Winsor G, Lewenza S, Kwasnicka A, Brazas MD, Brinkman FS, Hancock RE., J. Bacteriol. 188(11), 2006
PMID: 16707691
Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms.
Haagensen JA, Klausen M, Ernst RK, Miller SI, Folkesson A, Tolker-Nielsen T, Molin S., J. Bacteriol. 189(1), 2007
PMID: 17041046
Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa.
Hoffman LR, Deziel E, D'Argenio DA, Lepine F, Emerson J, McNamara S, Gibson RL, Ramsey BW, Miller SI., Proc. Natl. Acad. Sci. U.S.A. 103(52), 2006
PMID: 17172450
Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia.
Fouhy Y, Scanlon K, Schouest K, Spillane C, Crossman L, Avison MB, Ryan RP, Dow JM., J. Bacteriol. 189(13), 2007
PMID: 17468254
Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria.
Cha C, Gao P, Chen YC, Shaw PD, Farrand SK., Mol. Plant Microbe Interact. 11(11), 1998
PMID: 9805399
A LuxR homologue of Xanthomonas oryzae pv. oryzae is required for optimal rice virulence
FERLUGA S, BIGIRIMANA J, HOFTE M, VENTURI V., Mol. Plant Pathol. 8(4), 2007
PMID: IND43926185
Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review.
Zavascki AP, Goldani LZ, Li J, Nation RL., J. Antimicrob. Chemother. 60(6), 2007
PMID: 17878146
Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS.
Colnaghi Simionato AV, da Silva DS, Lambais MR, Carrilho E., J Mass Spectrom 42(10), 2007
PMID: 17902112
A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition.
Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH., ISME J 2(1), 2008
PMID: 18049456

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 18312265
PubMed | Europe PMC

Search this title in

Google Scholar