The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations

Abstract

BackgroundBacterial habitats, such as soil and the gut, are structured at the micrometer scale. Important aspects of microbial life in such spatial ecosystems are migration and colonization. Here we explore the colonization of a structured ecosystem by two neutrally labeled strains of Escherichia coli. Using time-lapse microscopy we studied the colonization of one-dimensional arrays of habitat patches linked by connectors, which were invaded by the two E. coli strains from opposite sides.ResultsThe two strains colonize a habitat from opposite sides by a series of traveling waves followed by an expansion front. When population waves collide, they branch into a continuing traveling wave, a reflected wave and a stationary population. When the two strains invade the landscape from opposite sides, they remain segregated in space and often one population will displace the other from most of the habitat. However, when the strains are co-cultured before entering the habitats, they colonize the habitat together and do not separate spatially. Using physically separated, but diffusionally coupled, habitats we show that colonization waves and expansion fronts interact trough diffusible molecules, and not by direct competition for space. Furthermore, we found that colonization outcome is influenced by a culture’s history, as the culture with the longest doubling time in bulk conditions tends to take over the largest fraction of the habitat. Finally, we observed that population distributions in parallel habitats located on the same device and inoculated with cells from the same overnight culture are significantly more similar to each other than to patterns in identical habitats located on different devices inoculated with cells from different overnight cultures, even tough all cultures were started from the same −80°C frozen stock.ConclusionsWe found that the colonization of spatially structure habitats by two interacting populations can lead to the formation of complex, but reproducible, spatiotemporal patterns. Furthermore, we showed that chemical interactions between two populations cause them to remain spatially segregated while they compete for habitat space. Finally, we observed that growth properties in bulk conditions correlate with the outcome of habitat colonization. Together, our data show the crucial roles of chemical interactions between populations and a culture’s history in determining the outcome of habitat colonization.

Zooming in to see the bigger picture: Microfluidic and nanofabrication tools to study bacteria

“…In the absence of external mixing (which occurs in shaken flasks), dispersal, chemotaxis, and aggregation become key drivers of bacterial community dynamics. As a result of these factors, the population expansion of bacteria that colonize a structured habitat does not obey the statistics of an ideal gas; instead, high-density demographic clusters form in close proximity to unoccupied territory (7,(85)(86)(87)(88). Keymer et al demonstrated that these processes allow E. coli to organize into a structured metapopulation (a population of populations) when colonizing an array of coupled habitat patches (7).…”

“…Approaches that allow several species to collectively define the chemical complexity of the medium while retaining the contributing cells in pure culture could, for instance, be implemented by using the on-chip ecosystems or 3D-printing technique described above. Other techniques that establish the physical segregation of populations while allowing chemical interactions rely on coupling separate culturing wells through a porous membrane (8) or hydrogel (108) or use shallow slits that prevent cellular migration from one compartment to the other (87,109). We expect that these and other (110) approaches will prove to be valuable tools to unravel the complexity of natural bacterial communities.…”

Bacteria‐in‐paper, a versatile platform to study bacterial ecology

“…; Van Vliet et al . ). A challenge to confining bacteria to liquid‐saturated paper is the liquid film that forms when wet paper comes in contact with a surface (e.g.…”

“…As both landscapes are colonised from the same inoculation zone, and thus by the same initial community, the effect of branching on the range expansions can be assessed by comparing the community composition at the extremities of both landscapes. Paper scaffolds were saturated with rich growth medium (LB) and inoculated in the centre with a 1:1 mixture of neutrally labelled E. coli, isogenic except for a green fluorescent protein (GFP) versus red fluorescent protein (RFP) insertion in the Lac operon (Keymer et al 2008;Hol et al 2013;Van Vliet et al 2014). A challenge to confining bacteria to liquid-saturated paper is the liquid film that forms when wet paper comes in contact with a surface (e.g.…”

Bacterial predator–prey dynamics in microscale patchy landscapes

“…During phase (i), the majority of E. coli bacteria are planktonic, motile, and migrate between patches rapidly, whereas in phase (ii), the majority of E. coli become sessile and show an increase in surface-associated growth [16]. Without predator (figure 1b,c), one observes phases (i) and (ii) only (see [38] for a detailed analysis of the colonization process). When prey and predator are both (simultaneously) inoculated, predation starts to dominate in phases (ii) and (iii) and the population density of E. coli starts to decline approximately 10-20 h after inoculation.…”