Evolutionary Adaptations of Biofilms Infecting Cystic Fibrosis Lungs Promote Mechanical Toughness By Adjusting Polysaccharide Production

Author(s)

Kristin Kovach, University of Texas at Austin
Megan Davis-Fields, University of Texas at Austin
Yasuhiko Irie, University of DaytonFollow
Kanishk Jain, University of Texas at Austin
Shashvat Doorwar, University of Texas at Austin
Katherine Vuong, University of Texas at Austin
Numa Dhamani, University of Texas at Austin
Kishore Mohanty, University of Texas at Austin
Ahmed Touhami, University of Texas at Austin
Vernita D. Gordon, University of Texas at Austin

Document Type

Article

Publication Date

1-23-2017

Publication Source

npj Biofilms and Microbiomes

Abstract

Biofilms are communities of microbes embedded in a matrix of extracellular polymeric substances, largely polysaccharides. Multiple types of extracellular polymeric substances can be produced by a single bacterial strain. The distinct polymer components of biofilms are known to provide chemical protection, but little is known about how distinct extracellular polysaccharides may also protect biofilms against mechanical stresses such as shear or phagocytic engulfment. Decades-long infections of Pseudomonas. aeruginosa biofilms in the lungs of cystic fibrosis patients are natural models for studies of biofilm fitness under pressure from antibiotics and the immune system. In cystic fibrosis infections, production of the extracellular polysaccharide alginate has long been known to increase with time and to chemically protect biofilms. More recently, it is being recognized that chronic cystic fibrosis infections also evolve to increase production of another extracellular polysaccharide, Psl; much less is known about Psl’s protective benefits to biofilms. We use oscillatory bulk rheology, on biofilms grown from longitudinal clinical isolates and from genetically-manipulated lab strains, to show that increased Psl stiffens biofilms and increases biofilm toughness, which is the energy cost to cause the biofilm to yield mechanically. Further, atomic force microscopy measurements reveal greater intercellular cohesion for higher Psl expression. Of the three types of extracellular polysaccharides produced by P. aeruginosa, only Psl increases the stiffness. Stiffening by Psl requires CdrA, a protein that binds to mannose groups on Psl and is a likely cross-linker for the Psl components of the biofilm matrix. We compare the elastic moduli of biofilms to the estimated stresses exerted by neutrophils during phagocytosis, and infer that increased Psl could confer a mechanical protection against phagocytic clearance.

ISBN/ISSN

2055-5008

Document Version

Published Version

Comments

This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/ 4.0/

Copyright

Copyright © 2017, the authors

Publisher

Nature Partner Journals in partnership with Nanyang Technological University

Peer Reviewed

yes

eCommons Citation

Kovach, Kristin; Davis-Fields, Megan; Irie, Yasuhiko; Jain, Kanishk; Doorwar, Shashvat; Vuong, Katherine; Dhamani, Numa; Mohanty, Kishore; Touhami, Ahmed; and Gordon, Vernita D., "Evolutionary Adaptations of Biofilms Infecting Cystic Fibrosis Lungs Promote Mechanical Toughness By Adjusting Polysaccharide Production" (2017). Biology Faculty Publications. 216.
https://ecommons.udayton.edu/bio_fac_pub/216