Cell adhesion and fluid flow jointly initiate genotype spatial distribution in biofilms.

Ricardo Martínez-García,Juan A Bonachela,Carey D Nadell,Knut Drescher,Raimo Hartmann,Oleg A Igoshin

doi:10.1371/journal.pcbi.1006094

Abstract

Biofilms are microbial collectives that occupy a diverse array of surfaces. It is well known that the function and evolution of biofilms are strongly influenced by the spatial arrangement of different strains and species within them, but how spatiotemporal distributions of different genotypes in biofilm populations originate is still underexplored. Here, we study the origins of biofilm genetic structure by combining model development, numerical simulations, and microfluidic experiments using the human pathogen Vibrio cholerae. Using spatial correlation functions to quantify the differences between emergent cell lineage segregation patterns, we find that strong adhesion often, but not always, maximizes the size of clonal cell clusters on flat surfaces. Counterintuitively, our model predicts that, under some conditions, investing in adhesion can reduce rather than increase clonal group size. Our results emphasize that a complex interaction between fluid flow and cell adhesiveness can underlie emergent patterns of biofilm genetic structure. This structure, in turn, has an outsize influence on how biofilm-dwelling populations function and evolve.

Highlights

In addition to living as planktonic cells in liquid environments, bacteria often form dense conglomerates attached to surfaces, termed biofilms
Combining experiments on V. cholerae and simulations of a cellular automaton, we show that the complex interaction between bacterial traits and environmental factors strongly influences the early origins of biofilm spatial structure
As V. cholerae does not use gliding or twitching motility to roam on glass surfaces after attachment [39], differences in surface occupation by our strains was attributed to their difference in matrix production

Summary

Introduction

In addition to living as planktonic cells in liquid environments, bacteria often form dense conglomerates attached to surfaces, termed biofilms. Biofilms are one of the most widespread forms of life on Earth, and they are deeply embedded into global scale processes such as biogeochemical cycling [1]. They play a central role in the interaction between bacteria and multicellular organisms, including humans, as biofilm production enhances antibiotic tolerance [2] and influences bacterial pathogenesis and microbiome functioning [3]. Intra-strain cooperative behaviors are more likely to be evolutionarily stable when different cell lineages are segregated in space, with typical interaction distances between cells being strongly influenced by the diffusivity of secreted products, biofilm architecture, and environmental flow conditions [16,17,18,19]. The means by which biofilm strain and species structure originates in the first place, are less well understood

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