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Open Access Highly Accessed Research article

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

Simon van Vliet123*, Felix JH Hol1, Tim Weenink16, Peter Galajda4 and Juan E Keymer15*

Author Affiliations

1 Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Lorentzweg 1, Delft, CJ 2628, The Netherlands

2 Department of Environmental Systems Science, ETH Zurich, Universitätsstrasse 16, 8092 Zürich, Switzerland

3 Department of Environmental Microbiology, Eawag, Überlandstrasse 133, Dübendorf 8600, Switzerland

4 Institute of Biophysics, Biological Research Centre of the Hungarian Academy of Sciences, Temesvari krt. 62, Szeged H-6726, Hungary

5 Instituto de Ecología y Biodiversidad (IEB), Las Palmeras 3425 Ñuñoa, Santiago, Casilla 653, Chile

6 Current address: Department of Bioengineering, Imperial College London, London, UK

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BMC Microbiology 2014, 14:116  doi:10.1186/1471-2180-14-116

Published: 7 May 2014

Abstract

Background

Bacterial 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.

Results

The 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.

Conclusions

We 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.

Keywords:
Habitat colonization; Spatially structured habitats; Microbes; Collective behavior; Bacterial competition; Microfluidics