Bend or break: how biochemically versatile molecules enable metabolic division of labor in clonal microbial communities.
cross-feeding systems
division of labor
gluconeogenesis
glycolysis
metabolic specialization
phenotypic heterogeneity
Journal
Genetics
ISSN: 1943-2631
Titre abrégé: Genetics
Pays: United States
ID NLM: 0374636
Informations de publication
Date de publication:
02 10 2021
02 10 2021
Historique:
accepted:
29
06
2021
received:
17
02
2021
entrez:
1
12
2021
pubmed:
2
12
2021
medline:
25
3
2022
Statut:
ppublish
Résumé
In fluctuating nutrient environments, isogenic microbial cells transition into "multicellular" communities composed of phenotypically heterogeneous cells, showing functional specialization. In fungi (such as budding yeast), phenotypic heterogeneity is often described in the context of cells switching between different morphotypes (e.g., yeast to hyphae/pseudohyphae or white/opaque transitions in Candida albicans). However, more fundamental forms of metabolic heterogeneity are seen in clonal Saccharomyces cerevisiae communities growing in nutrient-limited conditions. Cells within such communities exhibit contrasting, specialized metabolic states, and are arranged in distinct, spatially organized groups. In this study, we explain how such an organization can stem from self-organizing biochemical reactions that depend on special metabolites. These metabolites exhibit plasticity in function, wherein the same metabolites are metabolized and utilized for distinct purposes by different cells. This in turn allows cell groups to function as specialized, interdependent cross-feeding systems which support distinct metabolic processes. Exemplifying a system where cells exhibit either gluconeogenic or glycolytic states, we highlight how available metabolites can drive favored biochemical pathways to produce new, limiting resources. These new resources can themselves be consumed or utilized distinctly by cells in different metabolic states. This thereby enables cell groups to sustain contrasting, even apparently impossible metabolic states with stable transcriptional and metabolic signatures for a given environment, and divide labor in order to increase community fitness or survival. We speculate on possible evolutionary implications of such metabolic specialization and division of labor in isogenic microbial communities.
Identifiants
pubmed: 34849891
pii: 6380408
doi: 10.1093/genetics/iyab109
pmc: PMC8633146
pii:
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : DBT-Wellcome Trust India Alliance
ID : IA/E/16/1/502996
Pays : India
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America.
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