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Dispersal from Microbial Biofilms

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  • Authors: Nicolas Barraud1, Staffan Kjelleberg2, Scott A. Rice4
  • Editors: Mahmoud Ghannoum6, Matthew Parsek7, Marvin Whiteley8, Pranab Mukherjee9
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, NSW 2052, Australia; 2: Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, NSW 2052, Australia; 3: The Singapore Centre for Environmental Life Sciences Engineering, and the School of Biological Sciences, Nanyang Technological University, Singapore 639798; 4: Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, NSW 2052, Australia; 5: The Singapore Centre for Environmental Life Sciences Engineering, and the School of Biological Sciences, Nanyang Technological University, Singapore 639798; 6: Case Western Reserve University, Cleveland, OH; 7: University of Washington, Seattle, WA; 8: University of Texas at Austin, Austin, TX; 9: Case Western Reserve University, Cleveland, OH
    • Source: microbiolspec November 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.MB-0015-2014
  • Received 09 September 2014 Accepted 30 September 2014 Published 20 November 2015
  • Staffan Kjelleberg, [email protected]
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  • Abstract:

    One common feature of biofilm development is the active dispersal of cells from the mature biofilm, which completes the biofilm life cycle and allows for the subsequent colonization of new habitats. Dispersal is likely to be critical for species survival and appears to be a precisely regulated process that involves a complex network of genes and signal transduction systems. Sophisticated molecular mechanisms control the transition of sessile biofilm cells into dispersal cells and their coordinated detachment and release in the bulk liquid. Dispersal cells appear to be specialized and exhibit a unique phenotype different from biofilm or planktonic bacteria. Further, the dispersal population is characterized by a high level of heterogeneity, reminiscent of, but distinct from, that in the biofilm, which could potentially allow for improved colonization under various environmental conditions. Here we review recent advances in characterizing the molecular mechanisms that regulate biofilm dispersal events and the impact of dispersal in a broader ecological context. Several strategies that exploit the mechanisms controlling biofilm dispersal to develop as applications for biofilm control are also presented.

  • Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from Microbial Biofilms. Microbiol Spectrum 3(6):MB-0015-2014. doi:10.1128/microbiolspec.MB-0015-2014.

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/content/journal/microbiolspec/10.1128/microbiolspec.MB-0015-2014
2015-11-20
2020-07-05

Abstract:

One common feature of biofilm development is the active dispersal of cells from the mature biofilm, which completes the biofilm life cycle and allows for the subsequent colonization of new habitats. Dispersal is likely to be critical for species survival and appears to be a precisely regulated process that involves a complex network of genes and signal transduction systems. Sophisticated molecular mechanisms control the transition of sessile biofilm cells into dispersal cells and their coordinated detachment and release in the bulk liquid. Dispersal cells appear to be specialized and exhibit a unique phenotype different from biofilm or planktonic bacteria. Further, the dispersal population is characterized by a high level of heterogeneity, reminiscent of, but distinct from, that in the biofilm, which could potentially allow for improved colonization under various environmental conditions. Here we review recent advances in characterizing the molecular mechanisms that regulate biofilm dispersal events and the impact of dispersal in a broader ecological context. Several strategies that exploit the mechanisms controlling biofilm dispersal to develop as applications for biofilm control are also presented.

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Dispersal from Microbial Biofilms
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Citation: Barraud N, Kjelleberg S, Rice S. 2015. Dispersal from microbial biofilms. microbiolspec 3(6): doi:10.1128/microbiolspec.MB-0015-2014
/content/microbiolspec/10.1128/microbiolspec.MB-0015-2014.fig1
FIGURE 1
Microscopic images of biofilm microcolonies during seeding dispersal. (A-B) Motile cells appear in mature biofilm microcolonies. (A) Single frame of a mature microcolony. (B) Picture showing the average of 30 frames captured over a 1-second period. The highly motile cells “average” out and appear blurred in the center of the microcolony, demonstrating the extent of the motile region (white arrow in panels A and B). The sessile “wall” region is indicated by the black arrows in panel A (taken from reference 26 , with permission from the publisher). (C) Live/dead staining of a 7-day-old biofilm reveals patterns of cell death inside biofilm structures that occur simultaneously with biofilm dispersal, as indicated by the formation of hollow biofilm structures. Live cells are green and dead cells are red (adapted from reference 56 , copyright © American Society for Microbiology). (D) XZ cross-view of the biofilm in panel C (XY view) at the location indicated by the white line.
microbiolspec/3/6/MB-0015-2014-fig1_thmb.gif
microbiolspec/3/6/MB-0015-2014-fig1.gif
Image of FIGURE 1

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FIGURE 1

Microscopic images of biofilm microcolonies during seeding dispersal. (A-B) Motile cells appear in mature biofilm microcolonies. (A) Single frame of a mature microcolony. (B) Picture showing the average of 30 frames captured over a 1-second period. The highly motile cells “average” out and appear blurred in the center of the microcolony, demonstrating the extent of the motile region (white arrow in panels A and B). The sessile “wall” region is indicated by the black arrows in panel A (taken from reference 26 , with permission from the publisher). (C) Live/dead staining of a 7-day-old biofilm reveals patterns of cell death inside biofilm structures that occur simultaneously with biofilm dispersal, as indicated by the formation of hollow biofilm structures. Live cells are green and dead cells are red (adapted from reference 56 , copyright © American Society for Microbiology). (D) XZ cross-view of the biofilm in panel C (XY view) at the location indicated by the white line.

Source: microbiolspec November 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.MB-0015-2014
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FIGURE 2
Effectors of biofilm dispersal. Bacteria within the center of microcolonies induce a number of mechanisms to degrade and solubilize the biofilm EPS matrix and extracellular appendages such as fimbriae that immobilize cells. When the interior of the microcolony becomes fluid, cells begin to show signs of motility, and a breach is made in the microcolony wall through which dispersal cells are released.
microbiolspec/3/6/MB-0015-2014-fig2_thmb.gif
microbiolspec/3/6/MB-0015-2014-fig2.gif
Image of FIGURE 2

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FIGURE 2

Effectors of biofilm dispersal. Bacteria within the center of microcolonies induce a number of mechanisms to degrade and solubilize the biofilm EPS matrix and extracellular appendages such as fimbriae that immobilize cells. When the interior of the microcolony becomes fluid, cells begin to show signs of motility, and a breach is made in the microcolony wall through which dispersal cells are released.

Source: microbiolspec November 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.MB-0015-2014
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FIGURE 3
Physiological traits of planktonic, biofilm, and dispersal cells. Symbols are defined in Figure 2 .
microbiolspec/3/6/MB-0015-2014-fig3_thmb.gif
microbiolspec/3/6/MB-0015-2014-fig3.gif
Image of FIGURE 3

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FIGURE 3

Physiological traits of planktonic, biofilm, and dispersal cells. Symbols are defined in Figure 2 .

Source: microbiolspec November 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.MB-0015-2014
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FIGURE 4
A range of strategies targeting dispersal have been developed to control biofilms and biofilm-related infections. (a) BdcA protein with enhanced c-di-GMP binding ( 124 ). (b) Oroidin and synthetic derivatives that were identified as potent dispersal inducers after screening chemical libraries ( 125 ). (c) Diffusible fatty acid signal cis-2-decenoic acid ( 23 ). (d) Furanone 30, a synthetic QS inhibitor derived from natural furanone compounds isolated from the red alga ( 131 ). (e) Fimbrolide-nitroester with dual action QS inhibition and NO release ( 134 ). (f) β-lactam-NO prodrugs for the targeted delivery of NO to infectious biofilms ( 132 ). (g) Controlled delivery of NO using nanoparticles ( 135 ). (h) Catalytic generation of NO from endogenous nitrite sources to disperse and prevent biofilm for long-term applications ( 138 ).
microbiolspec/3/6/MB-0015-2014-fig4_thmb.gif
microbiolspec/3/6/MB-0015-2014-fig4.gif
Image of FIGURE 4

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FIGURE 4

A range of strategies targeting dispersal have been developed to control biofilms and biofilm-related infections. (a) BdcA protein with enhanced c-di-GMP binding ( 124 ). (b) Oroidin and synthetic derivatives that were identified as potent dispersal inducers after screening chemical libraries ( 125 ). (c) Diffusible fatty acid signal cis-2-decenoic acid ( 23 ). (d) Furanone 30, a synthetic QS inhibitor derived from natural furanone compounds isolated from the red alga ( 131 ). (e) Fimbrolide-nitroester with dual action QS inhibition and NO release ( 134 ). (f) β-lactam-NO prodrugs for the targeted delivery of NO to infectious biofilms ( 132 ). (g) Controlled delivery of NO using nanoparticles ( 135 ). (h) Catalytic generation of NO from endogenous nitrite sources to disperse and prevent biofilm for long-term applications ( 138 ).

Source: microbiolspec November 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.MB-0015-2014
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