Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

eLife

Alexa Price-Whelan¹  Lars EP Dietrich¹  Jeanyoung K Jo¹  Martin Lempp²  Raimo Hartmann²  Mads Frederik Hansen²  Francisco Díaz-Pascual²  Kazuki Nosho²  Eric Jelli³  Hannah Jeckel⁴  Konstantin Neuhaus⁴  Knut Drescher⁴  Hannes Link⁵ 

[1] Department of Biological Sciences, Columbia University, New York, United States;Max Planck Institute for Terrestrial Microbiology, Marburg, Germany;Max Planck Institute for Terrestrial Microbiology, Marburg, Germany;Department of Physics, Philipps-Universität Marburg, Marburg, Germany;Max Planck Institute for Terrestrial Microbiology, Marburg, Germany;Department of Physics, Philipps-Universität Marburg, Marburg, Germany;Biozentrum, University of Basel, Basel, Switzerland;Max Planck Institute for Terrestrial Microbiology, Marburg, Germany;Interfaculty Institute for Microbiology and Infection Medicine, Eberhard Karls Universität Tübingen, Tübingen, Germany;

关键词: biofilms;    colonies;    metabolism;    cross-feeding;    phenotypic heterogeneity;    E. coli;   

DOI  :  10.7554/eLife.70794

来源: eLife Sciences Publications, Ltd

【 摘 要 】

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.

【 授权许可】

CC BY