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Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

View ORCID ProfileFrancisco Díaz-Pascual, Martin Lempp, View ORCID ProfileKazuki Nosho, View ORCID ProfileHannah Jeckel, View ORCID ProfileJeanyoung K. Jo, Konstantin Neuhaus, View ORCID ProfileRaimo Hartmann, Eric Jelli, Mads Frederik Hansen, Alexa Price-Whelan, View ORCID ProfileLars E.P. Dietrich, View ORCID ProfileHannes Link, View ORCID ProfileKnut Drescher
doi: https://doi.org/10.1101/2021.02.28.433255
Francisco Díaz-Pascual
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Martin Lempp
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Kazuki Nosho
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Hannah Jeckel
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Marburg, Germany
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Jeanyoung K. Jo
3Department of Biological Sciences, Columbia University, New York, NY, USA
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Konstantin Neuhaus
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Marburg, Germany
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Raimo Hartmann
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Eric Jelli
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Marburg, Germany
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Mads Frederik Hansen
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
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Alexa Price-Whelan
3Department of Biological Sciences, Columbia University, New York, NY, USA
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Lars E.P. Dietrich
3Department of Biological Sciences, Columbia University, New York, NY, USA
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Hannes Link
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
4Interfaculty Institute for Microbiology and Infection Medicine, University of Tübingen, Tübingen, Germany
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Knut Drescher
1Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Marburg, Germany
5Biozentrum, University of Basel, Basel, Switzerland
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  • For correspondence: knut.drescher@unibas.ch
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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.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 07, 2021.
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Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
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 E.P. Dietrich, Hannes Link, Knut Drescher
bioRxiv 2021.02.28.433255; doi: https://doi.org/10.1101/2021.02.28.433255
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Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies
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 E.P. Dietrich, Hannes Link, Knut Drescher
bioRxiv 2021.02.28.433255; doi: https://doi.org/10.1101/2021.02.28.433255

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