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Phenotypically heterogeneous microenvironments emerge as biofilms mature across different environments. Phenotypic heterogeneity in biofilm sub-populations not obeying quorum sensing-dictated, collective group behavior may be considered as a strategy allowing non-conformists to survive hostile conditions. Heterogeneous phenotype development has been amply studied with respect to gene expression and genotypic changes, but 'biofilm genes' responsible for preprogrammed development of heterogeneous microenvironments in biofilms have never been discovered. Moreover, the question of what triggers the development of phenotypically heterogeneous microenvironments has never been addressed. The definition of biofilms as 'surface-adhering and surface-adapted' microbial communities contains the word 'surface' twice. This leads us to hypothesize that phenotypically heterogeneous microenvironments in biofilms develop as an adaptive response of initial colonizers to their adhering state, governed by the forces through which they adhere to a substratum surface. No surface is entirely homogeneous, while adhering bacteria can substantially contribute to stochastically occurring surface heterogeneity. Accordingly, bacterial adhesion forces sensed by initial colonizers differ across a substratum surface, leading to differential mechanical deformation of the cell wall and membrane, where many environmental sensors are located. Bacteria directly adhering to heterogeneous substratum domains therewith formulate their own local responses to their adhering state and command non-conformist behavior, leading to phenotypically heterogeneous microenvironments in biofilms.

Emergent heterogeneous microenvironments in biofilms: substratum surface heterogeneity and bacterial adhesion force-sensing