Bifunctionality of a biofilm matrix protein controlled by redox state

Sofia Arnaouteli, Ana Sofia Ferreira, Marieke Schor, Ryan J. Morris, Keith M. Bromley, Jeanyoung Jo, Krista L. Cortez, Tetyana Sukhodub, Alan R. Prescott, Lars E. P. Dietrich, Cait E. MacPhee (Lead / Corresponding author), Nicola R. Stanley-Wall (Lead / Corresponding author)

Research output: Contribution to journalArticle

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Abstract

Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats, but despite this many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacterium Bacillus subtilis depend on the production of the secreted film-forming protein BslA. Here we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, while dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.
Original languageEnglish
Pages (from-to)E6184-E6191
Number of pages8
JournalProceedings of the National Academy of Sciences
Volume114
Issue number30
Early online date11 Jul 2017
DOIs
Publication statusPublished - 25 Jul 2017

Fingerprint

Biofilms
Oxidation-Reduction
Dimerization
Proteins
Gram-Positive Bacteria
Amino Acid Substitution
Bacillus subtilis
Disulfides
Cysteine
Ecosystem
Electrons
Bacteria

Keywords

  • Bacillus subtilis
  • Biofilm
  • BsIA
  • Genetically separable
  • Redox state
  • Dimerisation

Cite this

Arnaouteli, Sofia ; Ferreira, Ana Sofia ; Schor, Marieke ; Morris, Ryan J. ; Bromley, Keith M. ; Jo, Jeanyoung ; Cortez, Krista L. ; Sukhodub, Tetyana ; Prescott, Alan R. ; Dietrich, Lars E. P. ; MacPhee, Cait E. ; Stanley-Wall, Nicola R. / Bifunctionality of a biofilm matrix protein controlled by redox state. In: Proceedings of the National Academy of Sciences. 2017 ; Vol. 114, No. 30. pp. E6184-E6191.
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title = "Bifunctionality of a biofilm matrix protein controlled by redox state",
abstract = "Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats, but despite this many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacterium Bacillus subtilis depend on the production of the secreted film-forming protein BslA. Here we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, while dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.",
keywords = "Bacillus subtilis, Biofilm, BsIA, Genetically separable, Redox state, Dimerisation",
author = "Sofia Arnaouteli and Ferreira, {Ana Sofia} and Marieke Schor and Morris, {Ryan J.} and Bromley, {Keith M.} and Jeanyoung Jo and Cortez, {Krista L.} and Tetyana Sukhodub and Prescott, {Alan R.} and Dietrich, {Lars E. P.} and MacPhee, {Cait E.} and Stanley-Wall, {Nicola R.}",
note = "Work was supported by the Biotechnology and Biological Sciences Research Council [BB/L006804/1; BB/L006979/1; BB/M013774/1; BB/N022254/1]. We acknowledge the Dundee Imaging Facility, Dundee, supported by the 'Wellcome Trust Technology Platform' award [097945/B/11/Z] for help with experiments. JJ was supported by NIH training grant 5T32GM008798, LEPD was supported by NIH grant R01AI103369.",
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month = "7",
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Arnaouteli, S, Ferreira, AS, Schor, M, Morris, RJ, Bromley, KM, Jo, J, Cortez, KL, Sukhodub, T, Prescott, AR, Dietrich, LEP, MacPhee, CE & Stanley-Wall, NR 2017, 'Bifunctionality of a biofilm matrix protein controlled by redox state', Proceedings of the National Academy of Sciences, vol. 114, no. 30, pp. E6184-E6191. https://doi.org/10.1073/pnas.1707687114

Bifunctionality of a biofilm matrix protein controlled by redox state. / Arnaouteli, Sofia; Ferreira, Ana Sofia; Schor, Marieke; Morris, Ryan J.; Bromley, Keith M.; Jo, Jeanyoung ; Cortez, Krista L.; Sukhodub, Tetyana; Prescott, Alan R.; Dietrich, Lars E. P.; MacPhee, Cait E. (Lead / Corresponding author); Stanley-Wall, Nicola R. (Lead / Corresponding author).

In: Proceedings of the National Academy of Sciences, Vol. 114, No. 30, 25.07.2017, p. E6184-E6191.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Bifunctionality of a biofilm matrix protein controlled by redox state

AU - Arnaouteli, Sofia

AU - Ferreira, Ana Sofia

AU - Schor, Marieke

AU - Morris, Ryan J.

AU - Bromley, Keith M.

AU - Jo, Jeanyoung

AU - Cortez, Krista L.

AU - Sukhodub, Tetyana

AU - Prescott, Alan R.

AU - Dietrich, Lars E. P.

AU - MacPhee, Cait E.

AU - Stanley-Wall, Nicola R.

N1 - Work was supported by the Biotechnology and Biological Sciences Research Council [BB/L006804/1; BB/L006979/1; BB/M013774/1; BB/N022254/1]. We acknowledge the Dundee Imaging Facility, Dundee, supported by the 'Wellcome Trust Technology Platform' award [097945/B/11/Z] for help with experiments. JJ was supported by NIH training grant 5T32GM008798, LEPD was supported by NIH grant R01AI103369.

PY - 2017/7/25

Y1 - 2017/7/25

N2 - Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats, but despite this many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacterium Bacillus subtilis depend on the production of the secreted film-forming protein BslA. Here we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, while dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.

AB - Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats, but despite this many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacterium Bacillus subtilis depend on the production of the secreted film-forming protein BslA. Here we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, while dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.

KW - Bacillus subtilis

KW - Biofilm

KW - BsIA

KW - Genetically separable

KW - Redox state

KW - Dimerisation

U2 - 10.1073/pnas.1707687114

DO - 10.1073/pnas.1707687114

M3 - Article

VL - 114

SP - E6184-E6191

JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

SN - 0027-8424

IS - 30

ER -