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.
Highlights
It is broadly accepted that bacteria principally exist as surface-associated communities called biofilms[1,2]
Tfp are retractile bacterial appendages whose cycles of elongation and retraction enable bacteria to exert forces on their surroundings[23,26]. These polymers have a diameter of molecular size and length exceeding the size of the bacteria body[23]
We took advantage of the fact that the merger of microcolonies necessitates a complex rearrangement of cells and will inform us on the internal dynamics of bacterial microcolonies
Summary
It is broadly accepted that bacteria principally exist as surface-associated communities called biofilms[1,2]. Microcolonies represent the first stage of a usually complex development into mature differentiated multicellular biofilms[1]. The unique reliance on Tfp makes Ng an ideal model system to fully understand the dynamics of formation of bacterial microcolonies. We look experimentally at the dynamics of formation of Ng microcolonies and highlight the crucial role of the mechanical forces generated by retractile Tfp in this process. We observe a sharp gradient of bacterial motility from mobile surface layer towards nearly immobile bulk of the microcolony. These results are corroborated by experiments with bacteria incapable of Tfp retraction and comparison with the predictions of the in silico model we recently developed[25]. We see that heterogeneous gene expression follows the heterogeneous motile behavior
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