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...

Full description

Bibliographic Details
Main Authors: Michael Porter, Fordyce A. Davidson, Cait E. MacPhee, Nicola R. Stanley-Wall
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:Biofilm
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2590207522000168
_version_ 1811201477036736512
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
record_format Article
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
work_keys_str_mv AT michaelporter systematicmicroscopicalanalysisrevealsobligatesynergybetweenextracellularmatrixcomponentsduringbacillussubtiliscolonybiofilmdevelopment
AT fordyceadavidson systematicmicroscopicalanalysisrevealsobligatesynergybetweenextracellularmatrixcomponentsduringbacillussubtiliscolonybiofilmdevelopment
AT caitemacphee systematicmicroscopicalanalysisrevealsobligatesynergybetweenextracellularmatrixcomponentsduringbacillussubtiliscolonybiofilmdevelopment
AT nicolarstanleywall systematicmicroscopicalanalysisrevealsobligatesynergybetweenextracellularmatrixcomponentsduringbacillussubtiliscolonybiofilmdevelopment