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Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

Diaz-Pascual, Francisco and Lempp, Martin and Nosho, Kazuki and Jeckel, Hannah and Jo, Jeanyoung K. and Neuhaus, Konstantin and Hartmann, Raimo and Jelli, Eric and Hansen, Mads Frederik and Price-Whelan, Alexa and Dietrich, Lars E. P. and Link, Hannes and Drescher, Knut. (2021) Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies.

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Abstract

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.
Faculties and Departments:05 Faculty of Science > Departement Biozentrum > Infection Biology > Microbiology and Biophysics (Drescher)
UniBasel Contributors:Drescher, Knut
Item Type:Working Paper
Publisher:Cold Spring Harbor Laboratory
Number of Pages:32
Note:Publication type according to Uni Basel Research Database: Discussion paper / Internet publication
Language:English
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edoc DOI:
Last Modified:25 Jun 2021 10:39
Deposited On:25 Jun 2021 10:39

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