Metabolic constraints drive self-organization of specialized cell groups

How phenotypically distinct states in isogenic cell populations appear and stably co-exist remains unresolved. We find that within a mature, clonal yeast colony developing in low glucose, cells arrange into metabolically disparate cell groups. Using this system, we model and experimentally identify...

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Bibliographic Details
Published in:eLife 2019-06, Vol.8
Main Authors: Varahan, Sriram, Walvekar, Adhish, Sinha, Vaibhhav, Krishna, Sandeep, Laxman, Sunil
Format: Article
Language:English
Subjects:
Amino acids
Cell Biology
cell states
Colonies
Gene expression
gluconeogenesis
Glucose
Growth rate
Light
Metabolism
Metabolites
Models, Biological
Morphology
Pentose phosphate pathway
Physics of Living Systems
Saccharomyces cerevisiae - cytology
Saccharomyces cerevisiae - growth & development
Saccharomyces cerevisiae - metabolism
Self-assembly
self-organization
Trehalose
Trehalose - metabolism
yeast
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Summary:How phenotypically distinct states in isogenic cell populations appear and stably co-exist remains unresolved. We find that within a mature, clonal yeast colony developing in low glucose, cells arrange into metabolically disparate cell groups. Using this system, we model and experimentally identify metabolic constraints sufficient to drive such self-assembly. Beginning in a uniformly gluconeogenic state, cells exhibiting a contrary, high pentose phosphate pathway activity state, spontaneously appear and proliferate, in a spatially constrained manner. Gluconeogenic cells in the colony produce and provide a resource, which we identify as trehalose. Above threshold concentrations of external trehalose, cells switch to the new metabolic state and proliferate. A self-organized system establishes, where cells in this new state are sustained by trehalose consumption, which thereby restrains other cells in the trehalose producing, gluconeogenic state. Our work suggests simple physico-chemical principles that determine how isogenic cells spontaneously self-organize into structured assemblies in complimentary, specialized states.
ISSN:2050-084X
2050-084X
DOI:10.7554/eLife.46735