Physical Determinants of Amyloid Assembly in Biofilm Formation

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Physical Determinants of Amyloid Assembly in Biofilm Formation. / Andreasen, Maria; Meisl, Georg; Taylor, Jonathan D; Michaels, Thomas C T; Levin, Aviad; Otzen, Daniel E; Chapman, Matthew R; Dobson, Christopher M; Matthews, Steve J; Knowles, Tuomas P J.

In: mBio, Vol. 10, No. 1, e02279-18, 08.01.2019.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

Harvard

Andreasen, M, Meisl, G, Taylor, JD, Michaels, TCT, Levin, A, Otzen, DE, Chapman, MR, Dobson, CM, Matthews, SJ & Knowles, TPJ 2019, 'Physical Determinants of Amyloid Assembly in Biofilm Formation', mBio, vol. 10, no. 1, e02279-18. https://doi.org/10.1128/mBio.02279-18

APA

Andreasen, M., Meisl, G., Taylor, J. D., Michaels, T. C. T., Levin, A., Otzen, D. E., Chapman, M. R., Dobson, C. M., Matthews, S. J., & Knowles, T. P. J. (2019). Physical Determinants of Amyloid Assembly in Biofilm Formation. mBio, 10(1), [e02279-18]. https://doi.org/10.1128/mBio.02279-18

CBE

Andreasen M, Meisl G, Taylor JD, Michaels TCT, Levin A, Otzen DE, Chapman MR, Dobson CM, Matthews SJ, Knowles TPJ. 2019. Physical Determinants of Amyloid Assembly in Biofilm Formation. mBio. 10(1):Article e02279-18. https://doi.org/10.1128/mBio.02279-18

MLA

Vancouver

Andreasen M, Meisl G, Taylor JD, Michaels TCT, Levin A, Otzen DE et al. Physical Determinants of Amyloid Assembly in Biofilm Formation. mBio. 2019 Jan 8;10(1). e02279-18. https://doi.org/10.1128/mBio.02279-18

Author

Andreasen, Maria ; Meisl, Georg ; Taylor, Jonathan D ; Michaels, Thomas C T ; Levin, Aviad ; Otzen, Daniel E ; Chapman, Matthew R ; Dobson, Christopher M ; Matthews, Steve J ; Knowles, Tuomas P J. / Physical Determinants of Amyloid Assembly in Biofilm Formation. In: mBio. 2019 ; Vol. 10, No. 1.

Bibtex

@article{91bf63ce237e45be9064f7d057f0405c,
title = "Physical Determinants of Amyloid Assembly in Biofilm Formation",
abstract = "A wide range of bacterial pathogens have been shown to form biofilms, which significantly increase their resistance to environmental stresses, such as antibiotics, and are thus of central importance in the context of bacterial diseases. One of the major structural components of these bacterial biofilms are amyloid fibrils, yet the mechanism of fibril assembly and its importance for biofilm formation are currently not fully understood. By studying fibril formation in vitro, in a model system of two common but unrelated biofilm-forming proteins, FapC from Pseudomonas fluorescens and CsgA from Escherichia coli, we found that the two proteins have a common aggregation mechanism. In both systems, fibril formation proceeds via nucleated growth of linear fibrils exhibiting similar measured rates of elongation, with negligible fibril self-replication. These similarities between two unrelated systems suggest that convergent evolution plays a key role in tuning the assembly kinetics of functional amyloid fibrils and indicates that only a narrow window of mechanisms and assembly rates allows for successful biofilm formation. Thus, the amyloid assembly reaction is likely to represent a means for controlling biofilm formation, both by the organism and by possible inhibitory drugs.IMPORTANCE Biofilms are generated by bacteria, embedded in the formed extracellular matrix. The biofilm's function is to improve the survival of a bacterial colony through, for example, increased resistance to antibiotics or other environmental stresses. Proteins secreted by the bacteria act as a major structural component of this extracellular matrix, as they self-assemble into highly stable amyloid fibrils, making the biofilm very difficult to degrade by physical and chemical means once formed. By studying the self-assembly mechanism of the fibrils from their monomeric precursors in two unrelated bacteria, our experimental and theoretical approaches shed light on the mechanism of functional amyloid assembly in the context of biofilm formation. Our results suggest that fibril formation may be a rate-limiting step in biofilm formation, which in turn has implications on the protein self-assembly reaction as a target for potential antibiotic drugs.",
author = "Maria Andreasen and Georg Meisl and Taylor, {Jonathan D} and Michaels, {Thomas C T} and Aviad Levin and Otzen, {Daniel E} and Chapman, {Matthew R} and Dobson, {Christopher M} and Matthews, {Steve J} and Knowles, {Tuomas P J}",
note = "Copyright {\textcopyright} 2019 Andreasen et al.",
year = "2019",
month = jan,
day = "8",
doi = "10.1128/mBio.02279-18",
language = "English",
volume = "10",
journal = "mBio (Online)",
issn = "2150-7511",
publisher = "American Society for Microbiology",
number = "1",

}

RIS

TY - JOUR

T1 - Physical Determinants of Amyloid Assembly in Biofilm Formation

AU - Andreasen, Maria

AU - Meisl, Georg

AU - Taylor, Jonathan D

AU - Michaels, Thomas C T

AU - Levin, Aviad

AU - Otzen, Daniel E

AU - Chapman, Matthew R

AU - Dobson, Christopher M

AU - Matthews, Steve J

AU - Knowles, Tuomas P J

N1 - Copyright © 2019 Andreasen et al.

PY - 2019/1/8

Y1 - 2019/1/8

N2 - A wide range of bacterial pathogens have been shown to form biofilms, which significantly increase their resistance to environmental stresses, such as antibiotics, and are thus of central importance in the context of bacterial diseases. One of the major structural components of these bacterial biofilms are amyloid fibrils, yet the mechanism of fibril assembly and its importance for biofilm formation are currently not fully understood. By studying fibril formation in vitro, in a model system of two common but unrelated biofilm-forming proteins, FapC from Pseudomonas fluorescens and CsgA from Escherichia coli, we found that the two proteins have a common aggregation mechanism. In both systems, fibril formation proceeds via nucleated growth of linear fibrils exhibiting similar measured rates of elongation, with negligible fibril self-replication. These similarities between two unrelated systems suggest that convergent evolution plays a key role in tuning the assembly kinetics of functional amyloid fibrils and indicates that only a narrow window of mechanisms and assembly rates allows for successful biofilm formation. Thus, the amyloid assembly reaction is likely to represent a means for controlling biofilm formation, both by the organism and by possible inhibitory drugs.IMPORTANCE Biofilms are generated by bacteria, embedded in the formed extracellular matrix. The biofilm's function is to improve the survival of a bacterial colony through, for example, increased resistance to antibiotics or other environmental stresses. Proteins secreted by the bacteria act as a major structural component of this extracellular matrix, as they self-assemble into highly stable amyloid fibrils, making the biofilm very difficult to degrade by physical and chemical means once formed. By studying the self-assembly mechanism of the fibrils from their monomeric precursors in two unrelated bacteria, our experimental and theoretical approaches shed light on the mechanism of functional amyloid assembly in the context of biofilm formation. Our results suggest that fibril formation may be a rate-limiting step in biofilm formation, which in turn has implications on the protein self-assembly reaction as a target for potential antibiotic drugs.

AB - A wide range of bacterial pathogens have been shown to form biofilms, which significantly increase their resistance to environmental stresses, such as antibiotics, and are thus of central importance in the context of bacterial diseases. One of the major structural components of these bacterial biofilms are amyloid fibrils, yet the mechanism of fibril assembly and its importance for biofilm formation are currently not fully understood. By studying fibril formation in vitro, in a model system of two common but unrelated biofilm-forming proteins, FapC from Pseudomonas fluorescens and CsgA from Escherichia coli, we found that the two proteins have a common aggregation mechanism. In both systems, fibril formation proceeds via nucleated growth of linear fibrils exhibiting similar measured rates of elongation, with negligible fibril self-replication. These similarities between two unrelated systems suggest that convergent evolution plays a key role in tuning the assembly kinetics of functional amyloid fibrils and indicates that only a narrow window of mechanisms and assembly rates allows for successful biofilm formation. Thus, the amyloid assembly reaction is likely to represent a means for controlling biofilm formation, both by the organism and by possible inhibitory drugs.IMPORTANCE Biofilms are generated by bacteria, embedded in the formed extracellular matrix. The biofilm's function is to improve the survival of a bacterial colony through, for example, increased resistance to antibiotics or other environmental stresses. Proteins secreted by the bacteria act as a major structural component of this extracellular matrix, as they self-assemble into highly stable amyloid fibrils, making the biofilm very difficult to degrade by physical and chemical means once formed. By studying the self-assembly mechanism of the fibrils from their monomeric precursors in two unrelated bacteria, our experimental and theoretical approaches shed light on the mechanism of functional amyloid assembly in the context of biofilm formation. Our results suggest that fibril formation may be a rate-limiting step in biofilm formation, which in turn has implications on the protein self-assembly reaction as a target for potential antibiotic drugs.

U2 - 10.1128/mBio.02279-18

DO - 10.1128/mBio.02279-18

M3 - Journal article

C2 - 30622185

VL - 10

JO - mBio (Online)

JF - mBio (Online)

SN - 2150-7511

IS - 1

M1 - e02279-18

ER -