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Protein Homeostasis Impairment Alters Phenotypic Heterogeneity of Biofilm Communities

Matavacas, Judith LU and von Wachenfeldt, Claes LU (2025) In Molecular Microbiology 124(1). p.1-19
Abstract

Biofilms are highly organized, cooperating communities of microorganisms encased in a self-produced extracellular matrix, providing resilience against external stress such as antimicrobial agents and host defenses. A hallmark of biofilms is their phenotypic heterogeneity, which enhances the overall growth and survival of the community. In this study, we demonstrate that removing the dnaK and tig genes encoding the core molecular chaperones DnaK (Hsp70 homolog) and Trigger factor disrupted protein homeostasis in Bacillus subtilis and resulted in the formation of an extremely mucoid biofilm with aberrant architecture, compromised structural integrity, and altered phenotypic heterogeneity. These changes include a large reduction in the... (More)

Biofilms are highly organized, cooperating communities of microorganisms encased in a self-produced extracellular matrix, providing resilience against external stress such as antimicrobial agents and host defenses. A hallmark of biofilms is their phenotypic heterogeneity, which enhances the overall growth and survival of the community. In this study, we demonstrate that removing the dnaK and tig genes encoding the core molecular chaperones DnaK (Hsp70 homolog) and Trigger factor disrupted protein homeostasis in Bacillus subtilis and resulted in the formation of an extremely mucoid biofilm with aberrant architecture, compromised structural integrity, and altered phenotypic heterogeneity. These changes include a large reduction in the motile subpopulation and an overrepresentation of matrix producers and endospores. Overproduction of poly-γ-glutamic acid contributed crucially to the mucoid phenotype and aberrant biofilm architecture. Homeostasis impairment, triggered by elevated temperatures, in wild-type cells led to mucoid and aberrant biofilm phenotypes similar to those observed in strains lacking both dnaK and tig. Our findings show that disruption of protein homeostasis, whether due to the absence of molecular chaperones or because of environmental factors, severely changes biofilm features.

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organization
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type
Contribution to journal
publication status
published
subject
keywords
Bacillus subtilis, DnaK, molecular chaperone, phenotypic heterogeneity, proteostasis, trigger factor
in
Molecular Microbiology
volume
124
issue
1
pages
19 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:105005188002
  • pmid:40243034
ISSN
0950-382X
DOI
10.1111/mmi.15366
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2025 The Author(s). Molecular Microbiology published by John Wiley & Sons Ltd.
id
1ca8b2bc-7e62-459d-bfaf-939589f5678e
date added to LUP
2025-08-15 14:52:59
date last changed
2025-08-16 03:00:03
@article{1ca8b2bc-7e62-459d-bfaf-939589f5678e,
  abstract     = {{<p>Biofilms are highly organized, cooperating communities of microorganisms encased in a self-produced extracellular matrix, providing resilience against external stress such as antimicrobial agents and host defenses. A hallmark of biofilms is their phenotypic heterogeneity, which enhances the overall growth and survival of the community. In this study, we demonstrate that removing the dnaK and tig genes encoding the core molecular chaperones DnaK (Hsp70 homolog) and Trigger factor disrupted protein homeostasis in Bacillus subtilis and resulted in the formation of an extremely mucoid biofilm with aberrant architecture, compromised structural integrity, and altered phenotypic heterogeneity. These changes include a large reduction in the motile subpopulation and an overrepresentation of matrix producers and endospores. Overproduction of poly-γ-glutamic acid contributed crucially to the mucoid phenotype and aberrant biofilm architecture. Homeostasis impairment, triggered by elevated temperatures, in wild-type cells led to mucoid and aberrant biofilm phenotypes similar to those observed in strains lacking both dnaK and tig. Our findings show that disruption of protein homeostasis, whether due to the absence of molecular chaperones or because of environmental factors, severely changes biofilm features.</p>}},
  author       = {{Matavacas, Judith and von Wachenfeldt, Claes}},
  issn         = {{0950-382X}},
  keywords     = {{Bacillus subtilis; DnaK; molecular chaperone; phenotypic heterogeneity; proteostasis; trigger factor}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{1--19}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Microbiology}},
  title        = {{Protein Homeostasis Impairment Alters Phenotypic Heterogeneity of Biofilm Communities}},
  url          = {{http://dx.doi.org/10.1111/mmi.15366}},
  doi          = {{10.1111/mmi.15366}},
  volume       = {{124}},
  year         = {{2025}},
}