Published January 7, 2014 | Version Supplemental Material + Published
Journal Article Open

Morphological optimization for access to dual oxidants in biofilms

  • 1. ROR icon Ames Research Center
  • 2. ROR icon California Institute of Technology
  • 3. ROR icon Search for Extraterrestrial Intelligence
  • 4. ROR icon Massachusetts Institute of Technology
  • 5. ROR icon Columbia University

Abstract

A major theme driving research in biology is the relationship between form and function. In particular, a longstanding goal has been to understand how the evolution of multicellularity conferred fitness advantages. Here we show that biofilms of the bacterium Pseudomonas aeruginosa produce structures that maximize cellular reproduction. Specifically, we develop a mathematical model of resource availability and metabolic response within colony features. This analysis accurately predicts the measured distribution of two types of electron acceptors: oxygen, which is available from the atmosphere, and phenazines, redox-active antibiotics produced by the bacterium. Using this model, we demonstrate that the geometry of colony structures is optimal with respect to growth efficiency. Because our model is based on resource dynamics, we also can anticipate shifts in feature geometry based on changes to the availability of electron acceptors, including variations in the external availability of oxygen and genetic manipulation that renders the cells incapable of phenazine production.

Additional Information

© 2014 National Academy of Sciences. Edited by James H. Brown, University of New Mexico, Albuquerque, NM, and approved November 8, 2013 (received for review August 16, 2013). We thank Alexa Price-Whelan for insightful discussion regarding this project and the manuscript. We thank Daniel Bellin for calculating the phenazine diffusion constant. This work was supported by a National Science Foundation Graduate Research Fellowship (C.P.K.), the Gordon and Betty Moore Foundation (C.P.K. and M.J.F.), the National Aeronautics and Space Administration (M.J.F.), the National Science Foundation (M.J.F.), a Gilliam Fellowship from the Howard Hughes Medical Institute (C.O.), a startup fund from Columbia University, and Research Grant 1 R01 AI103369-01A1 from the National Institute of Allergy and Infectious Diseases (to L.E.P.D.). Author contributions: C.P.K., M.J.F., and L.E.P.D. designed research; C.P.K., C.O., Z.M.-C., and L.E.P.D. performed research; C.P.K. and C.O. contributed new reagents/analytic tools; C.P.K., C.O., and L.E.P.D. analyzed data; and C.P.K., M.J.F., and L.E.P.D. wrote the paper. The authors declare no conflict of interest.

Attached Files

Published - PNAS-2014-Kempes-208-13.pdf

Supplemental Material - pnas.201315521SI.pdf

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Additional details

Identifiers

PMCID
PMC3890773
Eprint ID
43805
Resolver ID
CaltechAUTHORS:20140213-094447920

Funding

NSF Graduate Research Fellowship
Gordon and Betty Moore Foundation
NASA
NSF
Howard Hughes Medical Institute (HHMI)
Columbia University
NIH
1 R01 AI103369-01A1
National Institute of Allergy and Infectious Diseases

Dates

Created
2014-02-18
Created from EPrint's datestamp field
Updated
2021-11-10
Created from EPrint's last_modified field