Nonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates.

TitleNonuniform growth and surface friction determine bacterial biofilm morphology on soft substrates.
Publication TypeJournal Article
Year of Publication2020
AuthorsFei, C, Mao, S, Yan, J, Alert, R, Stone, HA, Bassler, BL, Wingreen, NS, Košmrlj, A
JournalProc Natl Acad Sci U S A
Volume117
Issue14
Pagination7622-7632
Date Published2020 04 07
ISSN1091-6490
KeywordsAgar, Anisotropy, Biofilms, Biomechanical Phenomena, Friction, Stress, Mechanical, Surface Properties, Vibrio cholerae
Abstract

<p>During development, organisms acquire three-dimensional (3D) shapes with important physiological consequences. While basic mechanisms underlying morphogenesis are known in eukaryotes, it is often difficult to manipulate them in vivo. To circumvent this issue, here we present a study of developing biofilms grown on agar substrates in which the spatiotemporal morphological patterns were altered by varying the agar concentration. Expanding biofilms are initially flat but later undergo a mechanical instability and become wrinkled. To gain mechanistic insights into this dynamic pattern-formation process, we developed a model that considers diffusion of nutrients and their uptake by bacteria, bacterial growth/biofilm matrix production, mechanical deformation of both the biofilm and the substrate, and the friction between them. Our model shows quantitative agreement with experimental measurements of biofilm expansion dynamics, and it accurately predicts two distinct spatiotemporal patterns observed in the experiments-the wrinkles initially appear either in the peripheral region and propagate inward (soft substrate/low friction) or in the central region and propagate outward (stiff substrate/high friction). Our results, which establish that nonuniform growth and friction are fundamental determinants of stress anisotropy and hence biofilm morphology, are broadly applicable to bacterial biofilms with similar morphologies and also provide insight into how other bacterial biofilms form distinct wrinkle patterns. We discuss the implications of forming undulated biofilm morphologies, which may enhance the availability of nutrients and signaling molecules and serve as a "bet hedging" strategy.</p>

DOI10.1073/pnas.1919607117
Alternate JournalProc Natl Acad Sci U S A
PubMed ID32193350
PubMed Central IDPMC7148565
Grant ListR01 GM082938 / GM / NIGMS NIH HHS / United States
R21 AI146223 / AI / NIAID NIH HHS / United States
R37 GM065859 / GM / NIGMS NIH HHS / United States
/ HHMI / Howard Hughes Medical Institute / United States
R21 AI114223 / AI / NIAID NIH HHS / United States