Skip to main content
Article thumbnail
Location of Repository

Role of mutation in pseudomonas aeruginosa biofilm development.

By Tim C. R. Conibear, Samuel L. Collins and Jeremy S. Webb

Abstract

The survival of bacteria in nature is greatly enhanced by their ability to grow within surface-associated communities called biofilms. Commonly, biofilms generate proliferations of bacterial cells, called microcolonies, which are highly recalcitrant, 3-dimensional foci of bacterial growth. Microcolony growth is initiated by only a subpopulation of bacteria within biofilms, but processes responsible for this differentiation remain poorly understood. <br/><br/>Under conditions of crowding and intense competition between bacteria within biofilms, microevolutionary processes such as mutation selection may be important for growth; however their influence on microcolony-based biofilm growth and architecture have not previously been explored. <br/><br/>To study mutation in-situ within biofilms, we transformed Pseudomonas aeruginosa cells with a green fluorescent protein gene containing a +1 frameshift mutation. <br/><br/>Transformed P. aeruginosa cells were non-fluorescent until a mutation causing reversion to the wildtype sequence occurs. Fluorescence-inducing mutations were observed in microcolony structures, but not in other biofilm cells, or in planktonic cultures of P. aeruginosa cells. Thus microcolonies may represent important foci for mutation and evolution within biofilms. <br/><br/>We calculated that microcolony-specific increases in mutation frequency were at least 100-fold compared with planktonically grown cultures. We also observed that mutator phenotypes can enhance microcolony-based growth of P. aeruginosa cells. For P. aeruginosa strains defective in DNA fidelity and error repair, we found that microcolony initiation and growth was enhanced with increased mutation frequency of the organism. <br/><br/>We suggest that microcolony-based growth can involve mutation and subsequent selection of mutants better adapted to grow on surfaces within crowded-cell environments. This model for biofilm growth is analogous to mutation selection that occurs during neoplastic progression and tumor development, and may help to explain why structural and genetic heterogeneity are characteristic features of bacterial biofilm populations

Topics: R1
Year: 2009
OAI identifier: oai:eprints.soton.ac.uk:146311
Provided by: e-Prints Soton
Download PDF:
Sorry, we are unable to provide the full text but you may find it at the following location(s):
  • http://dx.doi.org/10.1371/jour... (external link)
  • Suggested articles

    Citations

    1. (2006). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. doi
    2. (2001). A mutator phenotype in cancer. doi
    3. (1998). A novel bacterial reversion and forward mutation assay based on green fluorescent protein. doi
    4. (2001). A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. doi
    5. Ausubel FM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. doi
    6. (2002). Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. doi
    7. (2004). Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. doi
    8. (2003). Biofilm formation by Pseudomonas aeruginosa wildtype, flagella, and type IV pili mutants. doi
    9. (2004). Biofilms promote altruism. doi
    10. (2006). Cancer as an evolutionary and ecological process. doi
    11. (2003). Cell death in Pseudomonas aeruginosa biofilm development. doi
    12. (2001). Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. doi
    13. (2000). Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen.
    14. (2005). Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: A tool for identifying differentially regulated genes. doi
    15. (1994). Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. doi
    16. (2000). Development and dynamics of Pseudomonas sp. doi
    17. (2007). Differentiation and distribution of colistin- and sodium dodecyl sulfate-tolerant cells in Pseudomonas aeruginosa biofilms. doi
    18. (2001). Endogenous DNA damage and mutation. doi
    19. (2008). Endogenous oxidative stress produces diversity and adaptability in biofilm communities. doi
    20. (1997). Evolution of high mutation rates in experimental populations of E.
    21. (2008). Formation of Streptococcus pneumoniae nonphase-variable colony variants is due to increased mutation frequency present under biofilm growth conditions. doi
    22. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. doi
    23. (1981). Genetic and sequence analysis of frameshift mutations induced by ICR-191. doi
    24. (2001). Growth and detachment of cell clusters from mature mixed-species biofilms. doi
    25. (2000). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. doi
    26. (2003). Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. doi
    27. (2003). Horizontal acquisition of divergent chromosomal DNA in bacteria: effects of mutator phenotypes.
    28. (2006). Human cancers express a mutator phenotype. doi
    29. (2008). Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several Gram negative bacteria. doi
    30. (2008). Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria. doi
    31. (2004). Hypermutation and the preexistence of antibiotic-resistant Pseudomonas aeruginosa mutants: implications for susceptibility testing and treatment of chronic infections. doi
    32. (2003). Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. doi
    33. (2005). Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. doi
    34. (1999). Hypermutation targets a green fluorescent proteinencoding transgene in the presence of immunoglobulin enhancers. doi
    35. (1999). Internal hazards: baseline DNA damage by endogenous products of normal metabolism. doi
    36. (2003). Intracellular bacterial biofilm-like pods in urinary tract infections. doi
    37. (2003). Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. doi
    38. (2006). Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. doi
    39. (1998). Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. doi
    40. (2008). Measurements of accumulation and displacement at the single cell cluster level in Pseudomonas aeruginosa biofilms. doi
    41. MillerK,BostockJM, O’NeillAJ,ChopraI(2008)Increasedmutability of Pseudomonas aeruginosa in biofilms.
    42. (1996). Mutagenicity of acridines in a reversion assay based on tetracycline resistance in plasmid pBR322 in Escherichia coli. doi
    43. (2005). Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. doi
    44. (2005). Phenotypic differentiation and seeding dispersal in non-mucoid and mucoid Pseudomonas aeruginosa biofilms. doi
    45. (2002). Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm. doi
    46. (2000). Quantification of biofilm structures by the novel computer program COMSTAT.
    47. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms.
    48. (2003). Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. doi
    49. (2001). Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. doi
    50. (2005). Self-generated diversity produces ‘insurance effects’ in biofilm communities (vol 101, pg 16630, doi
    51. (2009). The developmental model of microbial biofilms: ten years of a paradigm up for review. doi
    52. (1983). The role of the microcolony mode of growth in the pathogenesis of Pseudomonas aeruginosa infections. doi
    53. (2007). Too many mutants with multiple mutations. doi

    To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.