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

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.

SUBMITTER: Martinez-Garcia R

PROVIDER: S-EPMC5901778 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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

Martínez-García Ricardo R Nadell Carey D CD Hartmann Raimo R Drescher Knut K Bonachela Juan A JA

PLoS computational biology 20180416 4

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 ...[more]

PMID: 29659578

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Project description:Most microorganisms live in complex communities, where they interact both synergistically and competitively. To explore the relationship between environmental heterogeneity and the spatial structure of well-defined biofilms, single- and mixed-species biofilms of Pseudomonas aeruginosa PAO1 and Flavobacterium sp. CDC-65 was grown in a planar flow cell under highly controlled flow gradients. Both organisms behaved differently in mixed cultures than in single-species cultures due to inter-species interactions, and these interactions were significantly affected by external flow conditions. Pseudomonas and Flavobacterium showed a competitive relationship under slow inflow conditions, where the supply of growth medium was limited. Under such competitive conditions, the faster- specific growth rate of Flavobacterium allowed it to secure access to favorable regions of the biofilm by overgrowing Pseudomonas. In contrast, Pseudomonas was restricted to nutritionally depleted habitat near the base of the biofilm, and its growth was significantly inhibited. Conversely, under higher inflow conditions providing greater influx of growth medium, both organisms accumulated greater biomass in mixed biofilms than in single-species biofilms. Spatial segregation of the two organisms within the biofilms contributed to enhanced overall exploitation of available nutrients and substrates, while morphological changes favored better adherence to the surface under high hydrodynamic shear. These results indicate that synergy and competition in biofilms vary with flow conditions. Limited resource replenishment favors competition under low-flow conditions, while high flow reduces competition and favors synergy by providing greater resources and simultaneously imposing increased hydrodynamic shear that makes it more difficult to accumulate biomass on the surface. Ecological interactions that produce mechanically stronger and more robust biofilms will support more extensive growth on surfaces subject to high hydrodynamic shear, but these interactions are difficult to predict from observations of the behavior of individual organisms.

Dataset Information

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

Publications

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

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