Abstract
Biofilms develop from bacteria bound on surfaces that grow into structured communities (microcolonies). Although surface topography is known to affect bacterial colonization, how multiple individual settlers develop into microcolonies simultaneously remains underexplored. Here, we use multiscale population-growth and 3D-morphometric analyses to assess the spatiotemporal development of hundreds of bacterial colonizers towards submillimeter-scale microcolony communities. Using an oral bacterium (Streptococcus mutans), we find that microbial cells settle on the surface randomly under sucrose-rich conditions, regardless of surface topography. However, only a subset of colonizers display clustering behavior and growth following a power law. These active colonizers expand three-dimensionally by amalgamating neighboring bacteria into densely populated microcolonies. Clustering and microcolony assembly are dependent on exopolysaccharides, while population growth dynamics and spatial structure are affected by cooperative or antagonistic microbes. Our work suggests that biofilm assembly resembles certain spatial-structural features of urbanization, where population growth and expansion can be influenced by type of settlers, neighboring cells, and further community merging and scaffolding occurring at various scales.
Highlights
Biofilms develop from bacteria bound on surfaces that grow into structured communities
The evolution of a biofilm community from single-cell to multicellular level was assessed by employing an analytical tool, designed for spatiotemporal analysis at multi-length scale across three dimensions, to track multiple cells and clusters regarding growth dynamics, morphology, and surface topography simultaneously
Several analyses can be performed, including (i) identification of spatial patterns of bacterial binding according to surface topographies; (ii) assessment of the growth of the entire population of colonizing microorganisms on a given surface; (iii) visualization of how they organize themselves into structured communities; and (iv) evaluation of symbiotic/ competition behavior among the population
Summary
Biofilms develop from bacteria bound on surfaces that grow into structured communities (microcolonies). The growth dynamics display spatial and structural patterns similar to urbanization, whereby some settlers stayed static while others grow into aggregates (villages) that further expand into densely populated microcolonies enclosed to welldefined boundaries (cities), which in turn merge to each other resulting in a larger biofilm superstructure (megacity). This conceptual framework may lead to alternative ways of studying the biofilm-assembly mechanisms and assessing therapeutic strategies that include events at large scale
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