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  Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies

Diaz-Pascual, F., Lempp, M., Nosho, K., Jeckel, H., Jo, J. K., Neuhaus, K., et al. (2021). Spatial alanine metabolism determines local growth dynamics of Escherichia coli colonies. eLife, 10:e70794. doi:10.7554/elife.70794.

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https://doi.org/10.7554/elife.70794 (Verlagsversion)
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Diaz-Pascual, F.1, Autor           
Lempp, M.2, Autor           
Nosho, K.1, Autor
Jeckel, H.1, Autor           
Jo, J. K.3, Autor
Neuhaus, K.1, Autor           
Hartmann, R.1, Autor           
Jelli, E.1, Autor           
Hansen, M. F.3, Autor
Price-Whelan, A.3, Autor
Dietrich, L. E.3, Autor
Link, H.4, Autor           
Drescher, K.1, Autor           
Affiliations:
1Max Planck Research Group Bacterial Biofilms, Max Planck Institute for Terrestrial Microbiology, Max Planck Society, ou_3266298              
2Emmy Noether Research Group Dynamic Control of Metabolic Networks, Alumni, Max Planck Institute for Terrestrial Microbiology, Max Planck Society, ou_3266292              
3external, ou_persistent22              
4Emmy Noether Research Group Dynamic Control of Metabolic Networks, Max Planck Institute for Terrestrial Microbiology, Max Planck Society, ou_3266292              

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Schlagwörter: Alanine/*metabolism Biofilms/*growth & development Escherichia coli/growth & development/*physiology *Metabolome Spatial Analysis *Transcriptome *E. coli *biofilms *colonies *cross-feeding *infectious disease *metabolism *microbiology *phenotypic heterogeneity *physics of living systems declared
 Zusammenfassung: 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.

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Sprache(n): eng - English
 Datum: 2021
 Publikationsstatus: Erschienen
 Seiten: -
 Ort, Verlag, Ausgabe: -
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 Art der Begutachtung: Expertenbegutachtung
 Art des Abschluß: -

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Titel: eLife
Genre der Quelle: Zeitschrift
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Ort, Verlag, Ausgabe: Cambridge : eLife Sciences Publications
Seiten: - Band / Heft: - Artikelnummer: 10:e70794 Start- / Endseite: - Identifikator: Anderer: URL
ISSN: 2050-084X
CoNE: https://pure.mpg.de/cone/journals/resource/2050-084X