Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

Bacteria commonly live in spatially structured biofilm assemblages, which are encased by an extracellular matrix. Metabolic activity of the cells inside biofilms causes gradients in local environmental conditions, which leads to the emergence of physiologically differentiated subpopulations. Informa...

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Autores principales:	Francisco Díaz-Pascual, Martin Lempp, Kazuki Nosho, Hannah Jeckel, Jeanyoung K Jo, Konstantin Neuhaus, Raimo Hartmann, Eric Jelli, Mads Frederik Hansen, Alexa Price-Whelan, Lars EP Dietrich, Hannes Link, Knut Drescher
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	biofilms colonies metabolism cross-feeding phenotypic heterogeneity Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/c7189e6f7875449c8818c4fcab0a0457
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spelling	oai:doaj.org-article:c7189e6f7875449c8818c4fcab0a04572021-11-09T11:53:43ZSpatial alanine metabolism determines local growth dynamics of Escherichia coli colonies10.7554/eLife.707942050-084Xe70794https://doaj.org/article/c7189e6f7875449c8818c4fcab0a04572021-11-01T00:00:00Zhttps://elifesciences.org/articles/70794https://doaj.org/toc/2050-084XBacteria commonly live in spatially structured biofilm assemblages, which are encased by an extracellular matrix. Metabolic activity of the cells inside biofilms causes gradients in local environmental conditions, which leads to the emergence of physiologically differentiated subpopulations. Information about the properties and spatial arrangement of such metabolic subpopulations, as well as their interaction strength and interaction length scales are lacking, even for model systems like Escherichia coli colony biofilms grown on agar-solidified media. Here, we use an unbiased approach, based on temporal and spatial transcriptome and metabolome data acquired during E. coli colony biofilm growth, to study the spatial organization of metabolism. We discovered that alanine displays a unique pattern among amino acids and that alanine metabolism is spatially and temporally heterogeneous. At the anoxic base of the colony, where carbon and nitrogen sources are abundant, cells secrete alanine via the transporter AlaE. In contrast, cells utilize alanine as a carbon and nitrogen source in the oxic nutrient-deprived region at the colony mid-height, via the enzymes DadA and DadX. This spatially structured alanine cross-feeding influences cellular viability and growth in the cross-feeding-dependent region, which shapes the overall colony morphology. More generally, our results on this precisely controllable biofilm model system demonstrate a remarkable spatiotemporal complexity of metabolism in biofilms. A better characterization of the spatiotemporal metabolic heterogeneities and dependencies is essential for understanding the physiology, architecture, and function of biofilms.Francisco Díaz-PascualMartin LemppKazuki NoshoHannah JeckelJeanyoung K JoKonstantin NeuhausRaimo HartmannEric JelliMads Frederik HansenAlexa Price-WhelanLars EP DietrichHannes LinkKnut DreschereLife Sciences Publications Ltdarticlebiofilmscoloniesmetabolismcross-feedingphenotypic heterogeneityMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilms colonies metabolism cross-feeding phenotypic heterogeneity Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	biofilms colonies metabolism cross-feeding phenotypic heterogeneity Medicine R Science Q Biology (General) QH301-705.5 Francisco Díaz-Pascual Martin Lempp Kazuki Nosho Hannah Jeckel Jeanyoung K Jo Konstantin Neuhaus Raimo Hartmann Eric Jelli Mads Frederik Hansen Alexa Price-Whelan Lars EP Dietrich Hannes Link Knut Drescher Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
description	Bacteria commonly live in spatially structured biofilm assemblages, which are encased by an extracellular matrix. Metabolic activity of the cells inside biofilms causes gradients in local environmental conditions, which leads to the emergence of physiologically differentiated subpopulations. Information about the properties and spatial arrangement of such metabolic subpopulations, as well as their interaction strength and interaction length scales are lacking, even for model systems like Escherichia coli colony biofilms grown on agar-solidified media. Here, we use an unbiased approach, based on temporal and spatial transcriptome and metabolome data acquired during E. coli colony biofilm growth, to study the spatial organization of metabolism. We discovered that alanine displays a unique pattern among amino acids and that alanine metabolism is spatially and temporally heterogeneous. At the anoxic base of the colony, where carbon and nitrogen sources are abundant, cells secrete alanine via the transporter AlaE. In contrast, cells utilize alanine as a carbon and nitrogen source in the oxic nutrient-deprived region at the colony mid-height, via the enzymes DadA and DadX. This spatially structured alanine cross-feeding influences cellular viability and growth in the cross-feeding-dependent region, which shapes the overall colony morphology. More generally, our results on this precisely controllable biofilm model system demonstrate a remarkable spatiotemporal complexity of metabolism in biofilms. A better characterization of the spatiotemporal metabolic heterogeneities and dependencies is essential for understanding the physiology, architecture, and function of biofilms.
format	article
author	Francisco Díaz-Pascual Martin Lempp Kazuki Nosho Hannah Jeckel Jeanyoung K Jo Konstantin Neuhaus Raimo Hartmann Eric Jelli Mads Frederik Hansen Alexa Price-Whelan Lars EP Dietrich Hannes Link Knut Drescher
author_facet	Francisco Díaz-Pascual Martin Lempp Kazuki Nosho Hannah Jeckel Jeanyoung K Jo Konstantin Neuhaus Raimo Hartmann Eric Jelli Mads Frederik Hansen Alexa Price-Whelan Lars EP Dietrich Hannes Link Knut Drescher
author_sort	Francisco Díaz-Pascual
title	Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
title_short	Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
title_full	Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
title_fullStr	Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
title_full_unstemmed	Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
title_sort	spatial alanine metabolism determines local growth dynamics of escherichia coli colonies
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/c7189e6f7875449c8818c4fcab0a0457
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_version_	1718441054508679168

Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

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