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Morphological plasticity as a bacterial survival strategy

Nature Reviews Microbiology volume 6, pages 162–168 (2008)Cite this article

Abstract

Bacteria have evolved complex systems to maintain consistent cell morphologies. Nevertheless, in certain circumstances, bacteria alter this highly regulated process to transform into filamentous organisms. Accumulating evidence attributes important biological roles to filamentation in stressful environments, including, but not limited to, sites of interaction between pathogenic bacteria and their hosts. Filamentation could represent an intended response to specific environmental cues that promote survival amidst the threats of consumption and killing.

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Figure 1: The SOS response.
Figure 2: Model of the UTI pathogenic cascade.
Figure 3: Protist by-products induce filamentation.
Figure 4: Filamentation of bacteria in response to environmental cues.

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References

  1. Duguay, A. R. & Silhavy, T. J. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694, 121–134 (2004).

    Article  CAS  PubMed  Google Scholar 

  2. Siu, L. K. Antibiotics: action and resistance in Gram-negative bacteria. J. Microbiol. Immunol. Infect. 35, 1–11 (2002).

    CAS  PubMed  Google Scholar 

  3. Chen, K., Sun, G. W., Chua, K. L. & Gan, Y. H. Modified virulence of antibiotic-induced Burkholderia pseudomallei filaments. Antimicrob. Agents Chemother. 49, 1002–1009 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Young, K. D. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 70, 660–703 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Zaritsky, A. On dimensional determination of rod-shaped bacteria. J. Theor. Biol. 54, 243–248 (1975).

    Article  CAS  PubMed  Google Scholar 

  6. Harry, E., Monahan, L. & Thompson, L. Bacterial cell division: the mechanism and its precison. Int. Rev. Cytol. 253, 27–94 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. Rothfield, L., Justice, S. & Garcia-Lara, J. Bacterial cell division. Annu. Rev. Genet. 33, 423–448 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Foxman, B. Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis. Mon. 49, 53–70 (2003).

    Article  PubMed  Google Scholar 

  9. Mulvey, M. A. et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282, 1494–1497 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Justice, S. S. et al. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc. Natl Acad. Sci. USA 101, 1333–1338 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Justice, S. S., Hunstad, D. A., Seed, P. C. & Hultgren, S. J. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc. Natl Acad. Sci. USA 103, 19884–19889 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Leroy, M. et al. Multiple consecutive lavage samplings reveal greater burden of disease and provide direct access to the nontypeable Haemophilus influenzae biofilm in experimental otitis media. Infect. Immun. 75, 4158–4172 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jurcisek, J. A. & Bakaletz, L. O. Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J. Bacteriol. 189, 3868–3875 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Belas, R. & Suvanasuthi, R. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J. Bacteriol. 187, 6789–6803 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Belas, R., Manos, J. & Suvanasuthi, R. Proteus mirabilis ZapA metalloprotease degrades a broad spectrum of substrates, including antimicrobial peptides. Infect. Immun. 72, 5159–5167 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Piao, Z., Sze, C. C., Barysheva, O., Iida, K. & Yoshida, S. Temperature-regulated formation of mycelial mat-like biofilms by Legionella pneumophila. Appl. Environ. Microbiol. 72, 1613–1622 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ogawa, M., Takade, A., Miyamoto, H., Taniguchi, H. & Yoshida, S. Morphological variety of intracellular microcolonies of Legionella species in Vero cells. Microbiol. Immunol. 45, 557–562 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Chauhan, A. et al. Mycobacterium tuberculosis cells growing in macrophages are filamentous and deficient in FtsZ rings. J. Bacteriol. 188, 1856–1865 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Abrahams, G. L. & Hensel, M. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell. Microbiol. 8, 728–737 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Rosenberger, C. M. & Finlay, B. B. Macrophages inhibit Salmonella typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J. Biol. Chem. 277, 18753–18762 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103–118 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Henry, T., Garcia-Del Portillo, F. & Gorvel, J. P. Identification of Salmonella functions critical for bacterial cell division within eukaryotic cells. Mol. Microbiol. 56, 252–267 (2005).

    Article  CAS  PubMed  Google Scholar 

  23. Lucchini, S., Liu, H., Jin, Q., Hinton, J. C. & Yu, J. Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect. Immun. 73, 88–102 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jones, A. L., Beveridge, T. J. & Woods, D. E. Intracellular survival of Burkholderia pseudomallei. Infect. Immun. 64, 782–790 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Cuccui, J. et al. Development of signature-tagged mutagenesis in Burkholderia pseudomallei to identify genes important in survival and pathogenesis. Infect. Immun. 75, 1186–1195 (2007).

    Article  CAS  PubMed  Google Scholar 

  26. Fields, B. S., Shotts, E. B. Jr, Feeley, J. C., Gorman, G. W. & Martin, W. T. Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis. Appl. Environ. Microbiol. 47, 467–471 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hilbi, H., Weber, S. S., Ragaz, C., Nyfeler, Y. & Urwyler, S. Environmental predators as models for bacterial pathogenesis. Environ. Microbiol. 9, 563–575 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nature Rev. Microbiol. 3, 537–546 (2005).

    Article  CAS  Google Scholar 

  29. Jurgens, K. & Matz, C. Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81, 413–434 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. Corno, G. & Jurgens, K. Direct and indirect effects of protist predation on population size structure of a bacterial strain with high phenotypic plasticity. Appl. Environ. Microbiol. 72, 78–86 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Miller, C. et al. SOS response induction by β-lactams and bacterial defense against antibiotic lethality. Science 305, 1629–1631 (2004).

    Article  CAS  PubMed  Google Scholar 

  32. Beaber, J. W., Hochhut, B. & Waldor, M. K. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427, 72–74 (2004).

    Article  CAS  PubMed  Google Scholar 

  33. Wagner, J. K. & Brun, Y. V. Out on a limb: how the Caulobacter stalk can boost the study of bacterial cell shape. Mol. Microbiol. 64, 28–33 (2007).

    Article  CAS  PubMed  Google Scholar 

  34. Wortinger, M. A., Quardokus, E. M. & Brun, Y. V. Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol. Microbiol. 29, 963–973 (1998).

    Article  CAS  PubMed  Google Scholar 

  35. Rooney, P. J. & Klein, B. S. Linking fungal morphogenesis with virulence. Cell. Microbiol. 4, 127–137 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Saville, S. P. et al. Inhibition of filamentation can be used to treat disseminated candidiasis. Antimicrob. Agents Chemother. 50, 3312–3316 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nemecek, J. C., Wuthrich, M. & Klein, B. S. Global control of dimorphism and virulence in fungi. Science 312, 583–588 (2006).

    Article  CAS  PubMed  Google Scholar 

  38. Janion, C. Some aspects of the SOS response system — a critical survey. Acta Biochim. Pol. 48, 599–610 (2001).

    CAS  PubMed  Google Scholar 

  39. Quillardet, P., Rouffaud, M. A. & Bouige, P. DNA array analysis of gene expression in response to UV irradiation in Escherichia coli. Res. Microbiol. 154, 559–572 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Mukherjee, A., Cao, C. & Lutkenhaus, J. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc. Natl Acad. Sci. USA 95, 2885–2890 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Trusca, D., Scott, S., Thompson, C. & Bramhill, D. Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J. Bacteriol. 180, 3946–3953 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Justice, S. S., Garcia-Lara, J. & Rothfield, L. I. Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery. Mol. Microbiol. 37, 410–423 (2000).

    Article  CAS  PubMed  Google Scholar 

  43. Cordell, S. C., Robinson, E. J. & Lowe, J. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl Acad. Sci. USA 100, 7889–7894 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Rather, P. N. Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol. 7, 1065–1073 (2005).

    Article  CAS  PubMed  Google Scholar 

  45. Allison, C., Coleman, N., Jones, P. L. & Hughes, C. Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect. Immun. 60, 4740–4746 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

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Author information

Authors and Affiliations

  1. Sheryl S. Justice is at the Center for Microbial Pathogenesis, The Research Institute at Nationwide Children's Hospital, Columbus, Ohio 43205, USA.,

    Sheryl S. Justice

  2. Lynette Cegelski and Scott J. Hultgren are at the Department of Molecular Microbiology, David A. Hunstad, Washington University School of Medicine, Saint Louis, Missouri 63110, USA.,

    David A. Hunstad, Lynette Cegelski & Scott J. Hultgren

  3. David A. Hunstad is also at the Department of Pediatrics, Washington University School of Medicine, Saint Louis, Missouri 63110, USA.,

    David A. Hunstad

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  1. Sheryl S. Justice
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Correspondence to Scott J. Hultgren.

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DATABASES

Entrez Genome Project

Burkholderia pseudomallei

Candida albicans

Caulobacter crescentus

Escherichia coli

Haemophilus influenzae

Legionella pneumophila

Mycobacterium tuberculosis

Proteus mirabilis

Salmonella typhimurium

Shigella flexneri

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Justice, S., Hunstad, D., Cegelski, L. et al. Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 6, 162–168 (2008). https://doi.org/10.1038/nrmicro1820

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