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Role of multicellular aggregates in biofilm formation

Kragh, Kasper; Hutchison, Jaime B.; Melaugh, Gavin; Rodesney, Chris; Roberts, Aled; Irie, Yasuhiko; Jensen, Peter �.; Diggle, Stephen P.; Allen, Rosalind J.; Gordon, Vernita; Bjarnsholt, Thomas

Authors

Kasper Kragh

Jaime B. Hutchison

Gavin Melaugh

Chris Rodesney

Aled Roberts

Yasuhiko Irie

Peter �. Jensen

Stephen P. Diggle

Rosalind J. Allen

Vernita Gordon

Thomas Bjarnsholt



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.

Citation

Kragh, K., Hutchison, J. B., Melaugh, G., Rodesney, C., Roberts, A., Irie, Y., …Bjarnsholt, T. (2016). Role of multicellular aggregates in biofilm formation. mBio, 7(2), Article e00237-16. https://doi.org/10.1128/mBio.00237-16

Journal Article Type Article
Acceptance Date Feb 22, 2016
Publication Date Mar 22, 2016
Deposit Date Aug 23, 2016
Publicly Available Date Mar 28, 2024
Journal mBio
Print ISSN 2161-2129
Electronic ISSN 2150-7511
Publisher American Society for Microbiology
Peer Reviewed Peer Reviewed
Volume 7
Issue 2
Article Number e00237-16
DOI https://doi.org/10.1128/mBio.00237-16
Public URL https://nottingham-repository.worktribe.com/output/779659
Publisher URL http://mbio.asm.org/content/7/2/e00237-16

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