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

Martínez-García, Ricardo and Nadell, Carey D. and Hartmann, Raimo and Drescher, Knut and Bonachela, Juan A. (2018) Cell adhesion and fluid flow jointly initiate genotype spatial distribution in biofilms. PLoS Computational Biology, 14 (4). e1006094. ISSN 1553-734X (https://doi.org/10.1371/journal.pcbi.1006094)

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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.