Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community
Journal article, 2021
Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures or synthetic assemblies. Here, we show how kefir, a natural milk-fermenting community of prokaryotes (predominantly lactic and acetic acid bacteria) and yeasts (family Saccharomycetaceae), realizes stable coexistence through spatiotemporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microorganisms) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a sequential manner in which early members open the niche for the followers by making available metabolites such as amino acids and lactate. Through metabolomics, transcriptomics and large-scale mapping of inter-species interactions, we show how microorganisms poorly suited for milk survive in—and even dominate—the community, through metabolic cooperation and uneven partitioning between grain and milk. Overall, our findings reveal how inter-species interactions partitioned in space and time lead to stable coexistence.
Author
Sonja Blasche
European Molecular Biology Laboratory
Yongkyu Kim
European Molecular Biology Laboratory
Ruben A.T. Mars
Swiss Federal Institute of Technology in Zürich (ETH)
Daniel Machado
European Molecular Biology Laboratory
Maria Maansson
Chr. Hansen
Eleni Kafkia
University of Cambridge
European Molecular Biology Laboratory
Alessio Milanese
European Molecular Biology Laboratory
Georg Zeller
European Molecular Biology Laboratory
B. Teusink
Vrije Universiteit Amsterdam
Jens B Nielsen
Chalmers, Biology and Biological Engineering, Systems and Synthetic Biology
Vladimir Benes
European Molecular Biology Laboratory
Rute Neves
Chr. Hansen
Uwe H. Sauer
Swiss Federal Institute of Technology in Zürich (ETH)
Kiran Raosaheb Patil
University of Cambridge
European Molecular Biology Laboratory
Nature Microbiology
2058-5276 (eISSN)
Vol. 6 2 196-208Subject Categories
Botany
Ecology
Microbiology
DOI
10.1038/s41564-020-00816-5
PubMed
33398099