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Self-establishing communities enable cooperative metabolite exchange in a eukaryote

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Campbell, Kate, Vowinckel, Jakob, Mülleder, Michael, Malmsheimer, Silke, Lawrence, Nicola, Calvani, Enrica, Miller-Fleming, Leonor, Alam, Mohammad T., Christen, Stefan, Keller, Markus A. and Ralser, Markus (2015) Self-establishing communities enable cooperative metabolite exchange in a eukaryote. eLife, 4 . e09943. ISSN 2050-084X.

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Official URL: http://dx.doi.org/10.7554/eLife.09943.001

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Abstract

Metabolite exchange among co-growing cells is frequent by nature, however, is not necessarily occurring at growth-relevant quantities indicative of non-cell-autonomous metabolic function. Complementary auxotrophs of Saccharomyces cerevisiae amino acid and nucleotide metabolism regularly fail to compensate for each other's deficiencies upon co-culturing, a situation which implied the absence of growth-relevant metabolite exchange interactions. Contrastingly, we find that yeast colonies maintain a rich exometabolome and that cells prefer the uptake of extracellular metabolites over self-synthesis, indicators of ongoing metabolite exchange. We conceived a system that circumvents co-culturing and begins with a self-supporting cell that grows autonomously into a heterogeneous community, only able to survive by exchanging histidine, leucine, uracil, and methionine. Compensating for the progressive loss of prototrophy, self-establishing communities successfully obtained an auxotrophic composition in a nutrition-dependent manner, maintaining a wild-type like exometabolome, growth parameters, and cell viability. Yeast, as a eukaryotic model, thus possesses extensive capacity for growth-relevant metabolite exchange and readily cooperates in metabolism within progressively establishing communities.

Item Type: Journal Article
Subjects: Q Science > QK Botany
Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences > Cell & Developmental Biology
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): Metabolites, Saccharomyces cerevisiae, Yeast, Eukaryotic cells
Journal or Publication Title: eLife
Publisher: eLife Sciences Publications Ltd.
ISSN: 2050-084X
Official Date: 26 October 2015
Dates:
DateEvent
26 October 2015Published
20 October 2015Accepted
8 July 2015Submitted
Volume: 4
Article Number: e09943
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 8 March 2017
Date of first compliant Open Access: 8 March 2017
Funder: Wellcome Trust (London, England), European Research Council (ERC), Isaac Newton Trust, Fonds zur Förderung der Wissenschaftlichen Forschung (Austria) (FWF)
Grant number: RG 093735/Z/10/Z (Wellcome Trust), StG 260809 (ERC), RG 68998 (Isaac Newton Trust), J3341 (FWF)

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