Pili mediated intercellular forces shape heterogeneous bacterial microcolonies prior to multicellular differentiation

Abstract

Microcolonies are aggregates of a few dozen to a few thousand cells exhibited by many bacteria. The formation of microcolonies is a crucial step towards the formation of more mature bacterial communities known as biofilms, but also marks a significant change in bacterial physiology. Within a microcolony, bacteria forgo a single cell lifestyle for a communal lifestyle hallmarked by high cell density and physical interactions between cells potentially altering their behaviour. It is thus crucial to understand how initially identical single cells start to behave differently while assembling in these tight communities. Here we show that cells in the microcolonies formed by the human pathogen Neisseria gonorrhoeae (Ng) present differential motility behaviors within an hour upon colony formation. Observation of merging microcolonies and tracking of single cells within microcolonies reveal a heterogeneous motility behavior: cells close to the surface of the microcolony exhibit a much higher motility compared to cells towards the center. Numerical simulations of a biophysical model for the microcolonies at the single cell level suggest that the emergence of differential behavior within a multicellular microcolony of otherwise identical cells is of mechanical origin. It could suggest a route toward further bacterial differentiation and ultimately mature biofilms.

Phenol Removal Capacity of the Common Duckweed (Lemna minor L.) and Six Phenol-Resistant Bacterial Strains From Its Rhizosphere: In Vitro Evaluation at High Phenol Concentrations

“…Moreover, in the recent bioremediation studies, it is becoming increasingly clear that the biological "platforms" are advantageous to the inorganic surfaces as a source of nutrients and a physical barrier, which simultaneously enhances the PGP properties of the bacteria [34]. In this study, we observed bacterial microcolonies in the intercellular crevices between epidermal root cells, which is a form of bacterial organization known to correspond to the early stages of biofilm formation [35]. The root exudates tend to leak from these intercellular spaces, therefore attracting the bacteria, which subsequently tend to organize into microcolonies and fully-formed biofilms [21,28,35].…”

“…In this study, we observed bacterial microcolonies in the intercellular crevices between epidermal root cells, which is a form of bacterial organization known to correspond to the early stages of biofilm formation [35]. The root exudates tend to leak from these intercellular spaces, therefore attracting the bacteria, which subsequently tend to organize into microcolonies and fully-formed biofilms [21,28,35]. This is a property that is reported to be useful in very different bioremediation strategies [25,35].…”

Continuum theory of active phase separation in cellular aggregates

“…Pili-mediated intercellular interactions of the bacteria are well studied and may serve as an important example to construct a microscopic model for active cellular force generation. N. gonorrhoeae bacteria have multiple (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20) pili isotropically distributed over the cell body (see fig. 1 (c)) [27][28][29].…”

“…Multi-scale computer simulations have played an important role in the study of the physics of the formation of N. gonorrhoeae colonies [16][17][18]. Continuum approaches such as theories of active gels [19][20][21][22][23][24][25][26] so far do not capture important features of dense cellular aggregates.…”

Clustering of bacteria with heterogeneous motility

“…For example, motility can either favor bacterial aggregation by enabling cell-cell encounters [15] but also prevent localized aggregates by enhancing dispersion [18]. Moreover, it is well-known that bacteria develop several subpopulations in order to adapt to evolving environmental conditions [19], so that heterogeneous behaviours can be found inside colonies [20,21]. But how heterogeneity influences clustering in such real systems is presently unknown.…”