Role of multicellular aggregates in biofilm formation

Kragh, Kasper, Hutchison, Jaime B., Melaugh, Gavin, Rodesney, Chris, Roberts, Aled, Irie, Yasuhiko, Jensen, Peter Ø., Diggle, Stephen P., Allen, Rosalind J., Gordon, Vernita and Bjarnsholt, Thomas (2016) Role of multicellular aggregates in biofilm formation. mBio, 7 (2). e00237-16/1-e00237-16/11. ISSN 2150-7511

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Abstract

In traditional models of in vitro biofilm development, individual bacterial cells seed a surface, multiply, and mature into multicellular, three-dimensional structures. Much research has been devoted to elucidating the mechanisms governing the initial attachment of single cells to surfaces. However, in natural environments and during infection, bacterial cells tend to clump as multicellular aggregates, and biofilms can also slough off aggregates as a part of the dispersal process. This makes it likely that biofilms are often seeded by aggregates and single cells, yet how these aggregates impact biofilm initiation and development is not known. Here we use a combination of experimental and computational approaches to determine the relative fitness of single cells and preformed aggregates during early development of Pseudomonas aeruginosa biofilms. We find that the relative fitness of aggregates depends markedly on the density of surrounding single cells, i.e., the level of competition for growth resources. When competition between aggregates and single cells is low, an aggregate has a growth disadvantage because the aggregate interior has poor access to growth resources. However, if competition is high, aggregates exhibit higher fitness, because extending vertically above the surface gives cells at the top of aggregates better access to growth resources. Other advantages of seeding by aggregates, such as earlier switching to a biofilm-like phenotype and enhanced resilience toward antibiotics and immune response, may add to this ecological benefit. Our findings suggest that current models of biofilm formation should be reconsidered to incorporate the role of aggregates in biofilm initiation.

Item Type: Article
RIS ID: https://nottingham-repository.worktribe.com/output/779659
Schools/Departments: University of Nottingham, UK > Faculty of Medicine and Health Sciences > School of Life Sciences
Identification Number: 10.1128/mBio.00237-16
Depositing User: Diggle, Dr Stephen
Date Deposited: 23 Aug 2016 08:15
Last Modified: 04 May 2020 17:41
URI: https://eprints.nottingham.ac.uk/id/eprint/35960

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