Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development
Single-species bacterial colony biofilms often present recurring morphologies that are thought to be of benefit to the population of cells within and are known to be dependent on the self-produced extracellular matrix. However, much remains unknown in terms of the developmental process at the single...
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Format: | Article |
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Elsevier
2022-12-01
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Series: | Biofilm |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2590207522000168 |
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author | Michael Porter Fordyce A. Davidson Cait E. MacPhee Nicola R. Stanley-Wall |
author_facet | Michael Porter Fordyce A. Davidson Cait E. MacPhee Nicola R. Stanley-Wall |
author_sort | Michael Porter |
collection | DOAJ |
description | Single-species bacterial colony biofilms often present recurring morphologies that are thought to be of benefit to the population of cells within and are known to be dependent on the self-produced extracellular matrix. However, much remains unknown in terms of the developmental process at the single cell level. Here, we design and implement systematic time-lapse imaging and quantitative analyses of the growth of Bacillus subtilis colony biofilms. We follow the development from the initial deposition of founding cells through to the formation of large-scale complex structures. Using the model biofilm strain NCIB 3610, we examine the movement dynamics of the growing biomass and compare them with those displayed by a suite of otherwise isogenic matrix-mutant strains. Correspondingly, we assess the impact of an incomplete matrix on biofilm morphologies and sessile growth rate. Our results indicate that radial expansion of colony biofilms results from the division of bacteria at the biofilm periphery rather than being driven by swelling due to fluid intake. Moreover, we show that lack of exopolysaccharide production has a negative impact on cell division rate, and the extracellular matrix components act synergistically to give the biomass the structural strength to produce aerial protrusions and agar substrate-deforming ability. |
first_indexed | 2024-04-12T02:22:17Z |
format | Article |
id | doaj.art-6ac3ea9d2002420cbc7f91d2fb7c163c |
institution | Directory Open Access Journal |
issn | 2590-2075 |
language | English |
last_indexed | 2024-04-12T02:22:17Z |
publishDate | 2022-12-01 |
publisher | Elsevier |
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series | Biofilm |
spelling | doaj.art-6ac3ea9d2002420cbc7f91d2fb7c163c2022-12-22T03:52:05ZengElsevierBiofilm2590-20752022-12-014100082Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm developmentMichael Porter0Fordyce A. Davidson1Cait E. MacPhee2Nicola R. Stanley-Wall3Division of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, DD1 5EH, United KingdomDivision of Mathematics, School of Science and Engineering, University of Dundee, Dundee, DD1 4HN, United KingdomSchool of Physics and Astronomy, The University of Edinburgh, Edinburgh, EH9 3FD, UKDivision of Molecular Microbiology, School of Life Sciences, University of Dundee, Dundee, DD1 5EH, United Kingdom; Corresponding author.Single-species bacterial colony biofilms often present recurring morphologies that are thought to be of benefit to the population of cells within and are known to be dependent on the self-produced extracellular matrix. However, much remains unknown in terms of the developmental process at the single cell level. Here, we design and implement systematic time-lapse imaging and quantitative analyses of the growth of Bacillus subtilis colony biofilms. We follow the development from the initial deposition of founding cells through to the formation of large-scale complex structures. Using the model biofilm strain NCIB 3610, we examine the movement dynamics of the growing biomass and compare them with those displayed by a suite of otherwise isogenic matrix-mutant strains. Correspondingly, we assess the impact of an incomplete matrix on biofilm morphologies and sessile growth rate. Our results indicate that radial expansion of colony biofilms results from the division of bacteria at the biofilm periphery rather than being driven by swelling due to fluid intake. Moreover, we show that lack of exopolysaccharide production has a negative impact on cell division rate, and the extracellular matrix components act synergistically to give the biomass the structural strength to produce aerial protrusions and agar substrate-deforming ability.http://www.sciencedirect.com/science/article/pii/S2590207522000168Bacillus subtilisColony biofilm developmentBiofilm morphologyExtracellular matrixBiofilm microscopy |
spellingShingle | Michael Porter Fordyce A. Davidson Cait E. MacPhee Nicola R. Stanley-Wall Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development Biofilm Bacillus subtilis Colony biofilm development Biofilm morphology Extracellular matrix Biofilm microscopy |
title | Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development |
title_full | Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development |
title_fullStr | Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development |
title_full_unstemmed | Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development |
title_short | Systematic microscopical analysis reveals obligate synergy between extracellular matrix components during Bacillus subtilis colony biofilm development |
title_sort | systematic microscopical analysis reveals obligate synergy between extracellular matrix components during bacillus subtilis colony biofilm development |
topic | Bacillus subtilis Colony biofilm development Biofilm morphology Extracellular matrix Biofilm microscopy |
url | http://www.sciencedirect.com/science/article/pii/S2590207522000168 |
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