Role of Multicellular Aggregates in Biofilm Formation

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....

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Autores principales:	Kasper N. Kragh, Jaime B. Hutchison, Gavin Melaugh, Chris Rodesney, Aled E. L. Roberts, Yasuhiko Irie, Peter Ø. Jensen, Stephen P. Diggle, Rosalind J. Allen, Vernita Gordon, Thomas Bjarnsholt
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1d21e62cdd1b4aa5ba945473f4bc6263
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spelling	oai:doaj.org-article:1d21e62cdd1b4aa5ba945473f4bc62632021-11-15T15:41:42ZRole of Multicellular Aggregates in Biofilm Formation10.1128/mBio.00237-162150-7511https://doaj.org/article/1d21e62cdd1b4aa5ba945473f4bc62632016-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00237-16https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE During the past decades, there has been a consensus around the model of development of a biofilm, involving attachment of single planktonic bacterial cells to a surface and the subsequent development of a mature biofilm. This study presents results that call for a modification of this rigorous model. We show how free floating biofilm aggregates can have a profound local effect on biofilm development when attaching to a surface. Our findings show that an aggregate landing on a surface will eventually outcompete the biofilm population arising from single cells attached around the aggregate and dominate the local biofilm development. These results point to a regime where preformed biofilm aggregates may have a fitness advantage over planktonic cells when it comes to accessing nutrients. Our findings add to the increasingly prominent comprehension that biofilm lifestyle is the default for bacteria and that planktonic single cells may be only a transition state at the most.Kasper N. KraghJaime B. HutchisonGavin MelaughChris RodesneyAled E. L. RobertsYasuhiko IriePeter Ø. JensenStephen P. DiggleRosalind J. AllenVernita GordonThomas BjarnsholtAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 2 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kasper N. Kragh Jaime B. Hutchison Gavin Melaugh Chris Rodesney Aled E. L. Roberts Yasuhiko Irie Peter Ø. Jensen Stephen P. Diggle Rosalind J. Allen Vernita Gordon Thomas Bjarnsholt Role of Multicellular Aggregates in Biofilm Formation
description	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. IMPORTANCE During the past decades, there has been a consensus around the model of development of a biofilm, involving attachment of single planktonic bacterial cells to a surface and the subsequent development of a mature biofilm. This study presents results that call for a modification of this rigorous model. We show how free floating biofilm aggregates can have a profound local effect on biofilm development when attaching to a surface. Our findings show that an aggregate landing on a surface will eventually outcompete the biofilm population arising from single cells attached around the aggregate and dominate the local biofilm development. These results point to a regime where preformed biofilm aggregates may have a fitness advantage over planktonic cells when it comes to accessing nutrients. Our findings add to the increasingly prominent comprehension that biofilm lifestyle is the default for bacteria and that planktonic single cells may be only a transition state at the most.
format	article
author	Kasper N. Kragh Jaime B. Hutchison Gavin Melaugh Chris Rodesney Aled E. L. Roberts Yasuhiko Irie Peter Ø. Jensen Stephen P. Diggle Rosalind J. Allen Vernita Gordon Thomas Bjarnsholt
author_facet	Kasper N. Kragh Jaime B. Hutchison Gavin Melaugh Chris Rodesney Aled E. L. Roberts Yasuhiko Irie Peter Ø. Jensen Stephen P. Diggle Rosalind J. Allen Vernita Gordon Thomas Bjarnsholt
author_sort	Kasper N. Kragh
title	Role of Multicellular Aggregates in Biofilm Formation
title_short	Role of Multicellular Aggregates in Biofilm Formation
title_full	Role of Multicellular Aggregates in Biofilm Formation
title_fullStr	Role of Multicellular Aggregates in Biofilm Formation
title_full_unstemmed	Role of Multicellular Aggregates in Biofilm Formation
title_sort	role of multicellular aggregates in biofilm formation
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/1d21e62cdd1b4aa5ba945473f4bc6263
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_version_	1718427629510459392

Role of Multicellular Aggregates in Biofilm Formation

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