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Motilities Swimming, Swarming, and Twitching Adherent Phenotypic Initiation of Biofilm Formation by Pseudomonas aeruginosa 57RP Correlates with Emergence of Hyperpiliated and Highly Adherent Phenotypic Variants Deficient in Swimming, Swarming, and Twitching Motilities Eric Déziel, Yves Comeau and Richard Villemur Downloaded from J. Bacteriol. 2001, 183(4):1195. DOI: 10.1128/JB.183.4.1195-1204.2001. Updated information and services can be found at: http://jb.asm.org/ http://jb.asm.org/content/183/4/1195 These include: REFERENCES This article cites 51 articles, 26 of which can be accessed free at: http://jb.asm.org/content/183/4/1195#ref-list-1 on May 5, 2014 by INRS-Institut Armand-Frappier CONTENT ALERTS Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more» Information about commercial reprint orders: http://journals.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/ JOURNAL OF BACTERIOLOGY, Feb. 2001, p. 1195–1204 Vol. 183, No. 4 0021-9193/01/$04.00ϩ0 DOI: 10.1128/JB.183.4.1195–1204.2001 Copyright © 2001, American Society for Microbiology. All Rights Reserved. Initiation of Biofilm Formation by Pseudomonas aeruginosa 57RP Correlates with Emergence of Hyperpiliated and Highly Adherent Phenotypic Variants Deficient in Swimming, Swarming, and Twitching Motilities 1,2 2 1 ERIC DE´ZIEL, YVES COMEAU, AND RICHARD VILLEMUR * Downloaded from INRS-Institut Armand-Frappier-Microbiologie et Biotechnologie, Laval, Que´bec, Canada H7V 1B7,1 and Civil, Geological, and Mining Engineering Department, E´cole Polytechnique de Montre´al, Montre´al, Que´bec, Canada H3C 3A72 Received 14 July 2000/Accepted 16 November 2000 Pseudomonas aeruginosa is a ubiquitous environmental bacterium capable of forming biofilms on surfaces as a survival strategy. It exhibits a large variety of competition/virulence factors, such as three types of motilities: flagellum-mediated swimming, flagellum-mediated swarming, and type IV pilus-mediated twitching. A strategy http://jb.asm.org/ frequently used by bacteria to survive changing environmental conditions is to create a phenotypically heter- ogeneous population by a mechanism called phase variation. In this report, we describe the characterization of phenotypic variants forming small, rough colonies that spontaneously emerged when P. aeruginosa 57RP was cultivated as a biofilm or in static liquid cultures. These small-colony (S) variants produced abundant type IV fimbriae, displayed defective swimming, swarming, and twitching motilities, and were impaired in chemotaxis. They also autoaggregated in liquid cultures and rapidly initiated the formation of strongly adherent biofilms. In contrast, the large-colony variant (parent form) was poorly adherent, homogeneously dispersed in liquid cultures, and produced scant polar fimbriae. Further analysis of the S variants demonstrated differences in a variety of other phenotypic traits, including increased production of pyocyanin and pyoverdine and reduced on May 5, 2014 by INRS-Institut Armand-Frappier elastase activity. Under appropriate growth conditions, cells of each phenotype switched to the other phenotype at a fairly high frequency. We conclude that these S variants resulted from phase variation and were selectively enriched when P. aeruginosa 57RP was grown as a biofilm or in static liquid cultures. We propose that phase variation ensures the prior presence of phenotypic forms well adapted to initiate the formation of a biofilm as soon as environmental conditions are favorable. Pseudomonas aeruginosa is a gram-negative bacterium found sible for the flagellum-independent mode of surface translo- in almost every ecological niche, including soil, water, and cation called twitching motility (9, 41, 48). plants. It is also an important opportunistic pathogen of hu- Bacteria in natural habitats usually grow as biofilms, orga- mans, primarily infecting immunocompromised patients (17). nized communities of cells embedded in an extracellular poly- Recent reports indicate that environmental and clinical P. saccharide matrix and attached to a surface (5). In recent aeruginosa strains are functionally equivalent and taxonomi- years, much has been learned about how cells initiate biofilm cally indistinguishable (14). The success of P. aeruginosa in formation (43, 49). Escherichia coli mutants defective in bio- various environments is attributed to its broad metabolic ver- film formation were found either to lack the ability to produce satility and its elaboration of many cell-associated and secreted type 1 pili or to be nonmotile (37). Similarly, flagellar motility virulence/survival factors (47). and type IV pilus-based twitching motility have been shown to Among the cell surface structures of P. aeruginosa, the polar be required for the initial attachment and development of a flagellum is responsible for a mode of motility in aqueous biofilm by P. aeruginosa (34). environment called swimming. As for most other motile bac- Biofilm bacteria display particular phenotypes that distin- teria, direction of movement is biased by chemotactic re- guish them from their freely growing counterparts (5, 49). The sponses to chemical stimuli (6, 31, 46). Flagella also mediate a differential expression of a large number of genes is known to mode of social motility known as swarming, recently described occur in the initial steps of biofilm formation (5, 38), such as for the first time in P. aeruginosa (39). Other cell surface the upregulation of exopolysaccharide synthesis following bac- structures acting as virulence/survival factors are type IV pili. terial adhesion to a surface (10, 38). However, a regulatory These polar fimbriae are presumably the principal adhesins, system controlling the conversion to the biofilm phenotype has mediating the adherence to eukaryotic cell surfaces (18) and not been described. probably to abiotic surfaces as well (41). They are also respon- A strategy that bacteria use to rapidly adapt and survive when environmental conditions change is to create a pheno- typically diverse population by a mechanism called phase vari- ation, that is, the high-frequency and reversible switching of * Corresponding author. INRS-Institut Armand-Frappier-Microbi- ologie et Biotechnologie, 531 Boul. des Prairies, Laval, Que´bec, Can- phenotypic traits (13). In gram-negative bacteria, the expres- ada H7V 1B7. Phone: (450) 687-5010. Fax: (450) 686-5501. E-mail: sion of a number of cell surface structures and outer mem- [email protected]. brane proteins, especially those linked to adhesion, aggrega- 1195 1196 DE´ZIEL ET AL. J. BACTERIOL. tion, and colonial morphology, is known to be regulated by tuberculin syringe with a disposable 25-gauge needle (Terumo Medical Corp., ␮ phase-variable mechanisms (reviewed in reference 22). Elkton, Md.) was filled with 100 l of Bushnell-Haas (BH) mineral salts medium (Difco) containing 0.1% tryptone as a chemoattractant. Cells were grown in LB As a part of a research project aimed at understanding the at 37°C to the logarithmic phase, washed, and resuspended in BH. A 100-␮l physiological mechanisms used by P. aeruginosa to access and sample of this bacterial suspension was drawn into a 200-␮l pipette tip. The catabolize hydrophobic, poorly bioavailable substrates such pe- syringe was then inserted and tightly fit into the tip with 3 mm of the needle troleum hydrocarbons (11), we have observed the spontaneous inserted into the cell suspension. Control capillaries containing only BH were emergence of alternate phenotypic forms growing as small, performed with each assay. Duplicate apparatus were incubated at 37°C for 45 min, and the content of the syringe was then diluted in 25 mM PBS and plated rough colonies when P. aeruginosa 57RP was cultivated as a onto TSA plates for cell enumeration. biofilm or in static liquid cultures (E. De´ziel, Y. Comeau, and Biofilm formation assay with polystyrene culture tubes. The biofilm formation R. Villemur, Abstr. 99th Gen. Meet. Am. Soc. Microbiol., protocol was adapted from that of O’Toole and Kolter (35). Polystyrene 12- by abstr. K-57, 1999). Since colonial morphology reflects the dif- 75-mm tubes containing 0.5 ml of BDT medium (BH mineral salts medium Downloaded from supplemented with 0.2% dextrose and 0.5% tryptone) were inoculated from ferential expression of components on cell surfaces within the overnight LB cultures and incubated at 32°C without agitation. At regular time colony, we hypothesized that the adherence and/or motility intervals, triplicate tubes were rinsed thoroughly with water, and a 1% solution behavior of this small colony phenotype might be altered. of crystal violet was added to stain the attached cells. After 10 to 15 min of In this report, we describe the isolation and characterization incubation at room temperature, the tubes were rinsed with water, and the of phenotypic variants of P. aeruginosa 57RP. In contrast with biomass of attached cells (biofilm) was quantified by solubilization of the dye in 2 ml of 95% ethanol. The absorbance was measured at 600 nm with a spectro- the large-colony (L) variant (parent form), the small-colony photometer. (S) variants produced abundant polar fimbriae, displayed re- Sensitivity to oxidative stress. The disk assay of Hassett et al. (21) was used to duced flagellar (chemotactic) and twitching motilities, and rap- test the sensitivity of cells to oxidative stress. Briefly, 100-␮l aliquots from http://jb.asm.org/ idly initiated the formation of strongly adherent biofilms. Un- cultures in mid-log or stationary phases of growth were uniformly spread on TSA and medium A (25) plates containing 2% agar. Sterile Whatman no. 1 filter der appropriate growth conditions, cells of each phenotype ␮ paper disks (7-mm diameter) impregnated with 10 l of 30% H2O2 were placed switched to the other phenotype at a fairly high frequency, in triplicate on each plate. The diameter of the zone of growth inhibition around suggesting that these S variants resulted from a reversible each disk was measured after5hofincubation at 37°C. phase variation phenomenon and were selectively enriched Production of exoproducts. (i) Pyocyanin. Bacteria were grown for 30 h at when P.
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