Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing

Elife. 2021 Feb 17:10:e64145. doi: 10.7554/eLife.64145.

Abstract

Life in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential gene CRISPR interference knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture with wild type. Partial knockdown of some translation-related genes reduced growth rates and led to out-competition. Media composition led some knockdowns to compete differentially as biofilm versus non-biofilm colonies. Cells depleted for the alanine racemase AlrA died in monoculture but survived in a biofilm colony co-culture via nutrient sharing. Rescue was enhanced in biofilm colony co-culture with a matrix-deficient parent due to a mutualism involving nutrient and matrix sharing. We identified several examples of mutualism involving matrix sharing that occurred in three-dimensional biofilm colonies but not when cultured in two dimensions. Thus, growth in a three-dimensional colony can promote genetic diversity through sharing of secreted factors and may drive evolution of mutualistic behavior.

Keywords: AlrA; B. subtilis; CRISPRi; D-alanine; ecology; essential genes; extracellular matrix; infectious disease; microbiology; surface growth.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine Racemase / genetics
  • Alanine Racemase / metabolism
  • Bacillus subtilis / genetics
  • Bacillus subtilis / growth & development*
  • Biofilms / growth & development*
  • Clustered Regularly Interspaced Short Palindromic Repeats
  • Culture Media
  • Gene Expression Regulation, Bacterial
  • Gene Knockdown Techniques
  • Symbiosis*

Substances

  • Culture Media
  • Alanine Racemase

Associated data

  • Dryad/10.5061/dryad.79cnp5htm