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Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility

Bacteria often live in complex communities in which they interact with other organisms. Consideration of the social environment of bacteria can reveal emergent traits and behaviors that would be overlooked by studying bacteria in isolation. Here we characterize a social trait which emerges upon inte...

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Autores principales: McCully, Lucy M., Bitzer, Adam S., Seaton, Sarah C., Smith, Leah M., Silby, Mark W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354810/
https://www.ncbi.nlm.nih.gov/pubmed/30700513
http://dx.doi.org/10.1128/mSphere.00696-18
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author McCully, Lucy M.
Bitzer, Adam S.
Seaton, Sarah C.
Smith, Leah M.
Silby, Mark W.
author_facet McCully, Lucy M.
Bitzer, Adam S.
Seaton, Sarah C.
Smith, Leah M.
Silby, Mark W.
author_sort McCully, Lucy M.
collection PubMed
description Bacteria often live in complex communities in which they interact with other organisms. Consideration of the social environment of bacteria can reveal emergent traits and behaviors that would be overlooked by studying bacteria in isolation. Here we characterize a social trait which emerges upon interaction between the distantly related soil bacteria Pseudomonas fluorescens Pf0-1 and Pedobacter sp. strain V48. On hard agar, which is not permissive for motility of the monoculture of either species, coculture reveals an emergent phenotype that we term “interspecies social spreading,” where the mixed colony spreads across the hard surface. We show that initiation of social spreading requires close association between the two species of bacteria. Both species remain associated throughout the spreading colony, with reproducible and nonhomogenous patterns of distribution. The nutritional environment influences social spreading: no social behavior is observed under high-nutrient conditions, but low-nutrient conditions are insufficient to promote social spreading without high salt concentrations. This simple two-species consortium is a tractable model system that will facilitate mechanistic investigations of interspecies interactions and provide insight into emergent properties of interacting species. These studies will contribute to the broader knowledge of how bacterial interactions influence the functions of communities they inhabit. IMPORTANCE The wealth of studies on microbial communities has revealed the complexity and dynamics of the composition of communities in many ecological settings. Fewer studies probe the functional interactions of the community members. Function of the community as a whole may not be fully revealed by characterizing the individuals. In our two-species model community, we find an emergent trait resulting from the interaction of the soil bacteria Pseudomonas fluorescens Pf0-1 and Pedobacter sp. V48. Observation of emergent traits suggests there may be many functions of a community that are not predicted based on a priori knowledge of the community members. These types of studies will provide a more holistic understanding of microbial communities, allowing us to connect information about community composition with behaviors determined by interspecific interactions. These studies increase our ability to understand communities, such as the soil microbiome, plant-root microbiome, and human gut microbiome, with the final goal of being able to manipulate and rationally improve these communities.
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spelling pubmed-63548102019-02-01 Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility McCully, Lucy M. Bitzer, Adam S. Seaton, Sarah C. Smith, Leah M. Silby, Mark W. mSphere Research Article Bacteria often live in complex communities in which they interact with other organisms. Consideration of the social environment of bacteria can reveal emergent traits and behaviors that would be overlooked by studying bacteria in isolation. Here we characterize a social trait which emerges upon interaction between the distantly related soil bacteria Pseudomonas fluorescens Pf0-1 and Pedobacter sp. strain V48. On hard agar, which is not permissive for motility of the monoculture of either species, coculture reveals an emergent phenotype that we term “interspecies social spreading,” where the mixed colony spreads across the hard surface. We show that initiation of social spreading requires close association between the two species of bacteria. Both species remain associated throughout the spreading colony, with reproducible and nonhomogenous patterns of distribution. The nutritional environment influences social spreading: no social behavior is observed under high-nutrient conditions, but low-nutrient conditions are insufficient to promote social spreading without high salt concentrations. This simple two-species consortium is a tractable model system that will facilitate mechanistic investigations of interspecies interactions and provide insight into emergent properties of interacting species. These studies will contribute to the broader knowledge of how bacterial interactions influence the functions of communities they inhabit. IMPORTANCE The wealth of studies on microbial communities has revealed the complexity and dynamics of the composition of communities in many ecological settings. Fewer studies probe the functional interactions of the community members. Function of the community as a whole may not be fully revealed by characterizing the individuals. In our two-species model community, we find an emergent trait resulting from the interaction of the soil bacteria Pseudomonas fluorescens Pf0-1 and Pedobacter sp. V48. Observation of emergent traits suggests there may be many functions of a community that are not predicted based on a priori knowledge of the community members. These types of studies will provide a more holistic understanding of microbial communities, allowing us to connect information about community composition with behaviors determined by interspecific interactions. These studies increase our ability to understand communities, such as the soil microbiome, plant-root microbiome, and human gut microbiome, with the final goal of being able to manipulate and rationally improve these communities. American Society for Microbiology 2019-01-30 /pmc/articles/PMC6354810/ /pubmed/30700513 http://dx.doi.org/10.1128/mSphere.00696-18 Text en Copyright © 2019 McCully et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
McCully, Lucy M.
Bitzer, Adam S.
Seaton, Sarah C.
Smith, Leah M.
Silby, Mark W.
Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title_full Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title_fullStr Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title_full_unstemmed Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title_short Interspecies Social Spreading: Interaction between Two Sessile Soil Bacteria Leads to Emergence of Surface Motility
title_sort interspecies social spreading: interaction between two sessile soil bacteria leads to emergence of surface motility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6354810/
https://www.ncbi.nlm.nih.gov/pubmed/30700513
http://dx.doi.org/10.1128/mSphere.00696-18
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