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Abstract

The self-produced biofilm provides beneficial protection for the
enclosed cells, but the costly production of matrix components makes
producer cells susceptible to cheating by nonproducing individuals.
Despite detrimental effects of nonproducers, biofilms can be
heterogeneous, with isogenic nonproducers being a natural consequence of
phenotypic differentiation processes. For instance, in Bacillus subtilis
biofilm cells differ in production of the two major matrix components,
the amyloid fiber protein TasA and exopolysaccharides (EPS),
demonstrating different expression levels of corresponding matrix genes.
This raises questions regarding matrix gene expression dynamics during
biofilm development and the impact of phenotypic nonproducers on biofilm
robustness. Here, we show that biofilms are structurally heterogeneous
and can be separated into strongly and weakly associated clusters. We
reveal that spatiotemporal changes in structural heterogeneity correlate
with matrix gene expression, with TasA playing a key role in biofilm
integrity and timing of development. We show that the matrix remains
partially privatized by the producer subpopulation, where cells tightly
stick together even when exposed to shear stress. Our results support
previous findings on the existence of "weak points" in seemingly robust
biofilms as well as on the key role of linkage proteins in biofilm
formation. Furthermore, we provide a starting point for investigating
the privatization of common goods within isogenic populations.
IMPORTANCE Biofilms are communities of bacteria protected by a
self-produced extracellular matrix. The detrimental effects of
nonproducing individuals on biofilm development raise questions about
the dynamics between community members, especially when isogenic
nonproducers exist within wild-type populations. We asked ourselves
whether phenotypic nonproducers impact biofilm robustness, and where and
when this heterogeneity of matrix gene expression occurs. Based on our
results, we propose that the matrix remains partly privatized by the
producing subpopulation, since producing cells stick together when
exposed to shear stress. The important role of linkage proteins in
robustness and development of the structurally heterogeneous biofilm
provides an entry into studying the privatization of common goods within
isogenic populations.