Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies

ABSTRACT Bacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask why bacterial lineages invest simultaneously in both fast- and slow-grow...

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Autores principales:	Nick Vallespir Lowery, Luke McNally, William C. Ratcliff, Sam P. Brown
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	biofilms evolution microbial ecology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6249f3df0a324e19aaa3ff865c49a1b4
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spelling	oai:doaj.org-article:6249f3df0a324e19aaa3ff865c49a1b42021-11-15T15:51:44ZDivision of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies10.1128/mBio.00672-172150-7511https://doaj.org/article/6249f3df0a324e19aaa3ff865c49a1b42017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00672-17https://doaj.org/toc/2150-7511ABSTRACT Bacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask why bacterial lineages invest simultaneously in both fast- and slow-growing types. We develop a population dynamic model of lineage expansion across a patchy environment and find that mixed investment is favored across a broad range of environmental conditions, even when transmission is entirely via biofilm cells. This mixed strategy is favored because of a division of labor where exponentially dividing planktonic cells can act as an engine for the production of future biofilm cells, which grow more slowly. We use experimental evolution to test our predictions and show that phenotypic heterogeneity is persistent even under selection for purely planktonic or purely biofilm transmission. Furthermore, simulations suggest that maintenance of a biofilm subpopulation serves as a cost-effective hedge against environmental uncertainty, which is also consistent with our experimental findings. IMPORTANCE Cell types specialized for survival have been observed and described within clonal bacterial populations for decades, but why are these specialists continually produced under benign conditions when such investment comes at a high reproductive cost? Conversely, when survival becomes an imperative, does it ever benefit the population to maintain a pool of rapidly growing but vulnerable planktonic cells? Using a combination of mathematical modeling, simulations, and experiments, we find that mixed investment strategies are favored over a broad range of environmental conditions and rely on a division of labor between cell types, where reproductive specialists amplify survival specialists, which can be transmitted through the environment with a limited mortality rate. We also show that survival specialists benefit rapidly growing populations by serving as a hedge against unpredictable changes in the environment. These results help to clarify the general evolutionary and ecological forces that can generate and maintain diverse subtypes within clonal bacterial populations.Nick Vallespir LoweryLuke McNallyWilliam C. RatcliffSam P. BrownAmerican Society for Microbiologyarticlebiofilmsevolutionmicrobial ecologyMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilms evolution microbial ecology Microbiology QR1-502
spellingShingle	biofilms evolution microbial ecology Microbiology QR1-502 Nick Vallespir Lowery Luke McNally William C. Ratcliff Sam P. Brown Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
description	ABSTRACT Bacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask why bacterial lineages invest simultaneously in both fast- and slow-growing types. We develop a population dynamic model of lineage expansion across a patchy environment and find that mixed investment is favored across a broad range of environmental conditions, even when transmission is entirely via biofilm cells. This mixed strategy is favored because of a division of labor where exponentially dividing planktonic cells can act as an engine for the production of future biofilm cells, which grow more slowly. We use experimental evolution to test our predictions and show that phenotypic heterogeneity is persistent even under selection for purely planktonic or purely biofilm transmission. Furthermore, simulations suggest that maintenance of a biofilm subpopulation serves as a cost-effective hedge against environmental uncertainty, which is also consistent with our experimental findings. IMPORTANCE Cell types specialized for survival have been observed and described within clonal bacterial populations for decades, but why are these specialists continually produced under benign conditions when such investment comes at a high reproductive cost? Conversely, when survival becomes an imperative, does it ever benefit the population to maintain a pool of rapidly growing but vulnerable planktonic cells? Using a combination of mathematical modeling, simulations, and experiments, we find that mixed investment strategies are favored over a broad range of environmental conditions and rely on a division of labor between cell types, where reproductive specialists amplify survival specialists, which can be transmitted through the environment with a limited mortality rate. We also show that survival specialists benefit rapidly growing populations by serving as a hedge against unpredictable changes in the environment. These results help to clarify the general evolutionary and ecological forces that can generate and maintain diverse subtypes within clonal bacterial populations.
format	article
author	Nick Vallespir Lowery Luke McNally William C. Ratcliff Sam P. Brown
author_facet	Nick Vallespir Lowery Luke McNally William C. Ratcliff Sam P. Brown
author_sort	Nick Vallespir Lowery
title	Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
title_short	Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
title_full	Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
title_fullStr	Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
title_full_unstemmed	Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
title_sort	division of labor, bet hedging, and the evolution of mixed biofilm investment strategies
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/6249f3df0a324e19aaa3ff865c49a1b4
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Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies

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