Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 116, Issue 28, Pages 14216-14221Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1819016116
Keywords
Vibrio cholerae; biofilm; extracellular matrix; cell shape; chitin
Categories
Funding
- GANN Fellowship from Dartmouth College
- DFG (Collaborative Research Centre) [TRR 174]
- Swiss National Science Foundation [31003A_169377]
- Gabriella Giorgi-Cavaglieri Foundation
- National Science Foundation [MCB 1817342]
- Burke Award from Dartmouth College, a pilot award from the Cystic Fibrosis Foundation [STANTO15RO]
- NIH [P20-GM113132]
- Swiss National Science Foundation (SNF) [31003A_169377] Funding Source: Swiss National Science Foundation (SNF)
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Collective behavior in spatially structured groups, or biofilms, is the norm among microbes in their natural environments. Though biofilm formation has been studied for decades, tracing the mechanistic and ecological links between individual cell morphologies and the emergent features of cell groups is still in its infancy. Here we use single-cell-resolution confocal microscopy to explore biofilms of the human pathogen Vibrio cholerae in conditions mimicking its marine habitat. Prior reports have noted the occurrence of cellular filamentation in V. cholerae, with variable propensity to filament among both toxigenic and nontoxigenic strains. Using a filamenting strain of V. cholerae O139, we show that cells with this morphotype gain a profound competitive advantage in colonizing and spreading on particles of chitin, the material many marine Vibrio species depend on for growth in seawater. Furthermore, filamentous cells can produce biofilms that are independent of primary secreted components of the V. cholerae biofilm matrix; instead, filamentous biofilm architectural strength appears to derive at least in part from the entangled mesh of cells themselves. The advantage gained by filamentous cells in early chitin colonization and growth is countered in long-term competition experiments with matrix-secreting V. cholerae variants, whose densely packed biofilm structures displace competitors from surfaces. Overall, our results reveal an alternative mode of biofilm architecture that is dependent on filamentous cell morphology and advantageous in environments with rapid chitin particle turnover. This insight provides an environmentally relevant example of how cell morphology can impact bacterial fitness.
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