Vertical stratification of matrix production is essential for physical integrity and architecture of macrocolony biofilms of Escherichia coli

Environ Microbiol. 2015 Dec;17(12):5073-88. doi: 10.1111/1462-2920.12991. Epub 2015 Sep 10.

Abstract

Bacterial macrocolony biofilms grow into intricate three-dimensional structures that depend on self-produced extracellular polymers conferring protection, cohesion and elasticity to the biofilm. In Escherichia coli, synthesis of this matrix - consisting of amyloid curli fibres and cellulose - requires CsgD, a transcription factor regulated by the stationary phase sigma factor RpoS, and occurs in the nutrient-deprived cells of the upper layer of macrocolonies. Is this asymmetric matrix distribution functionally important or is it just a fortuitous by-product of an unavoidable nutrient gradient? In order to address this question, the RpoS-dependent csgD promoter was replaced by a vegetative promoter. This re-wiring of csgD led to CsgD and matrix production in both strata of macrocolonies, with the lower layer transforming into a rigid 'base plate' of growing yet curli-connected cells. As a result, the two strata broke apart followed by desiccation and exfoliation of the top layer. By contrast, matrix-free cells at the bottom of wild-type macrocolonies maintain colony contact with the humid agar support by flexibly filling the space that opens up under buckling areas of the macrocolony. Precisely regulated stratification in matrix-free and matrix-producing cell layers is thus essential for the physical integrity and architecture of E. coli macrocolony biofilms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / metabolism
  • Bacterial Proteins / genetics*
  • Biofilms / growth & development*
  • Escherichia coli / genetics*
  • Escherichia coli / physiology
  • Escherichia coli Proteins / genetics*
  • Extracellular Matrix / metabolism*
  • Promoter Regions, Genetic / genetics
  • Sigma Factor / genetics*
  • Trans-Activators / genetics*

Substances

  • Amyloid
  • Bacterial Proteins
  • CsgD protein, E coli
  • Escherichia coli Proteins
  • Sigma Factor
  • Trans-Activators
  • sigma factor KatF protein, Bacteria