Filamentous bacteriophage promote biofilm assembly and function

Patrick R. Secor; Johanna M. Sweere; Lia A. Michaels; Andrey V. Malkovskiy; Daniel Lazzareschi; Ethan Katznelson; Jayakumar Rajadas; Michael E. Birnbaum; Allison Arrigoni; Kathleen R. Braun; Stephen P. Evanko; David A. Stevens; Werner Kaminsky; Pradeep K. Singh; William C. Parks; Paul L. Bollyky

doi:10.1016/j.chom.2015.10.013

Filamentous bacteriophage promote biofilm assembly and function

Patrick R. Secor
, Johanna M. Sweere
, Lia A. Michaels
, Andrey V. Malkovskiy
, Daniel Lazzareschi
, Ethan Katznelson
, Jayakumar Rajadas
, Michael E. Birnbaum
, Allison Arrigoni
, Kathleen R. Braun
, Stephen P. Evanko
, David A. Stevens
, Werner Kaminsky
, Pradeep K. Singh
, William C. Parks
, Paul L. Bollyky

Research output: Contribution to journal › Article › peer-review

246 Scopus citations

Abstract

Biofilms - communities of bacteria encased in a polymer-rich matrix - confer bacteria with the ability to persist in pathologic host contexts, such as the cystic fibrosis (CF) airways. How bacteria assemble polymers into biofilms is largely unknown. We find that the extracellular matrix produced by Pseudomonas aeruginosa self-assembles into a liquid crystal through entropic interactions between polymers and filamentous Pf bacteriophages, which are long, negatively charged filaments. This liquid crystalline structure enhances biofilm function by increasing adhesion and tolerance to desiccation and antibiotics. Pf bacteriophages are prevalent among P. aeruginosa clinical isolates and were detected in CF sputum. The addition of Pf bacteriophage to sputum polymers or serum was sufficient to drive their rapid assembly into viscous liquid crystals. Fd, a related bacteriophage of Escherichia coli, has similar biofilm-building capabilities. Targeting filamentous bacteriophage or the liquid crystalline organization of the biofilm matrix may represent antibacterial strategies.

Original language	English
Pages (from-to)	549-559
Number of pages	11
Journal	Cell Host and Microbe
Volume	18
Issue number	5
DOIs	https://doi.org/10.1016/j.chom.2015.10.013
State	Published - Nov 11 2015

Funding

This work was supported by National Institutes of Health grants HL098067, HL089455 (W.C.P.), R01 AI101307-03 (P.K.S.), and HL113294 (P.L.B.); the Microbiology Core of the NIDDK Cystic Fibrosis Research and Translation Center (DK089507); a Cystic Fibrosis Foundation Research Development Program Postdoctoral Fellowship to P.R.S.; and in part by UWPR95794 to the University of Washington’s Proteomics Resource, a grant from the Child Health Research Institute, Stanford Transdisciplinary Initiatives Program, and a gift to D.A.S. from Mr. John Flatley. A Gabilan Stanford Graduate Fellowship supported J.M.S. The authors declare no conflict of interest.

Funder number
DK089507
R01 AI101307-03, HL113294, P01HL098067
R01HL089455
UWPR95794

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10.1016/j.chom.2015.10.013

Cite this

Secor, P. R., Sweere, J. M., Michaels, L. A., Malkovskiy, A. V., Lazzareschi, D., Katznelson, E., Rajadas, J., Birnbaum, M. E., Arrigoni, A., Braun, K. R., Evanko, S. P., Stevens, D. A., Kaminsky, W., Singh, P. K., Parks, W. C., & Bollyky, P. L. (2015). Filamentous bacteriophage promote biofilm assembly and function. Cell Host and Microbe, 18(5), 549-559. https://doi.org/10.1016/j.chom.2015.10.013

@article{9750d26d3302458195b2fc2b9cbd1d0b,

title = "Filamentous bacteriophage promote biofilm assembly and function",

abstract = "Biofilms - communities of bacteria encased in a polymer-rich matrix - confer bacteria with the ability to persist in pathologic host contexts, such as the cystic fibrosis (CF) airways. How bacteria assemble polymers into biofilms is largely unknown. We find that the extracellular matrix produced by Pseudomonas aeruginosa self-assembles into a liquid crystal through entropic interactions between polymers and filamentous Pf bacteriophages, which are long, negatively charged filaments. This liquid crystalline structure enhances biofilm function by increasing adhesion and tolerance to desiccation and antibiotics. Pf bacteriophages are prevalent among P. aeruginosa clinical isolates and were detected in CF sputum. The addition of Pf bacteriophage to sputum polymers or serum was sufficient to drive their rapid assembly into viscous liquid crystals. Fd, a related bacteriophage of Escherichia coli, has similar biofilm-building capabilities. Targeting filamentous bacteriophage or the liquid crystalline organization of the biofilm matrix may represent antibacterial strategies.",

author = "Secor, \{Patrick R.\} and Sweere, \{Johanna M.\} and Michaels, \{Lia A.\} and Malkovskiy, \{Andrey V.\} and Daniel Lazzareschi and Ethan Katznelson and Jayakumar Rajadas and Birnbaum, \{Michael E.\} and Allison Arrigoni and Braun, \{Kathleen R.\} and Evanko, \{Stephen P.\} and Stevens, \{David A.\} and Werner Kaminsky and Singh, \{Pradeep K.\} and Parks, \{William C.\} and Bollyky, \{Paul L.\}",

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doi = "10.1016/j.chom.2015.10.013",

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Secor, PR, Sweere, JM, Michaels, LA, Malkovskiy, AV, Lazzareschi, D, Katznelson, E, Rajadas, J, Birnbaum, ME, Arrigoni, A, Braun, KR, Evanko, SP, Stevens, DA, Kaminsky, W, Singh, PK, Parks, WC & Bollyky, PL 2015, 'Filamentous bacteriophage promote biofilm assembly and function', Cell Host and Microbe, vol. 18, no. 5, pp. 549-559. https://doi.org/10.1016/j.chom.2015.10.013

TY - JOUR

T1 - Filamentous bacteriophage promote biofilm assembly and function

AU - Secor, Patrick R.

AU - Sweere, Johanna M.

AU - Michaels, Lia A.

AU - Malkovskiy, Andrey V.

AU - Lazzareschi, Daniel

AU - Katznelson, Ethan

AU - Rajadas, Jayakumar

AU - Birnbaum, Michael E.

AU - Arrigoni, Allison

AU - Braun, Kathleen R.

AU - Evanko, Stephen P.

AU - Stevens, David A.

AU - Kaminsky, Werner

AU - Singh, Pradeep K.

AU - Parks, William C.

AU - Bollyky, Paul L.

PY - 2015/11/11

Y1 - 2015/11/11

N2 - Biofilms - communities of bacteria encased in a polymer-rich matrix - confer bacteria with the ability to persist in pathologic host contexts, such as the cystic fibrosis (CF) airways. How bacteria assemble polymers into biofilms is largely unknown. We find that the extracellular matrix produced by Pseudomonas aeruginosa self-assembles into a liquid crystal through entropic interactions between polymers and filamentous Pf bacteriophages, which are long, negatively charged filaments. This liquid crystalline structure enhances biofilm function by increasing adhesion and tolerance to desiccation and antibiotics. Pf bacteriophages are prevalent among P. aeruginosa clinical isolates and were detected in CF sputum. The addition of Pf bacteriophage to sputum polymers or serum was sufficient to drive their rapid assembly into viscous liquid crystals. Fd, a related bacteriophage of Escherichia coli, has similar biofilm-building capabilities. Targeting filamentous bacteriophage or the liquid crystalline organization of the biofilm matrix may represent antibacterial strategies.

AB - Biofilms - communities of bacteria encased in a polymer-rich matrix - confer bacteria with the ability to persist in pathologic host contexts, such as the cystic fibrosis (CF) airways. How bacteria assemble polymers into biofilms is largely unknown. We find that the extracellular matrix produced by Pseudomonas aeruginosa self-assembles into a liquid crystal through entropic interactions between polymers and filamentous Pf bacteriophages, which are long, negatively charged filaments. This liquid crystalline structure enhances biofilm function by increasing adhesion and tolerance to desiccation and antibiotics. Pf bacteriophages are prevalent among P. aeruginosa clinical isolates and were detected in CF sputum. The addition of Pf bacteriophage to sputum polymers or serum was sufficient to drive their rapid assembly into viscous liquid crystals. Fd, a related bacteriophage of Escherichia coli, has similar biofilm-building capabilities. Targeting filamentous bacteriophage or the liquid crystalline organization of the biofilm matrix may represent antibacterial strategies.

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SN - 1931-3128

VL - 18

SP - 549

EP - 559

JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 5

ER -

Filamentous bacteriophage promote biofilm assembly and function

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