Cross-Kingdom Chemical Communication Drives a Heritable, Mutually Beneficial Prion-Based Transformation of Metabolism

Abstract

In experimental science, organisms are usually studied in isolation, but in the wild they compete and cooperate in complex communities. We report a system for cross-kingdom communication by which bacteria heritably transform yeast metabolism. An ancient biological circuit blocks yeast from using other carbon sources in the presence of glucose. [GAR[superscript +]], a protein-based epigenetic element, allows yeast to circumvent this glucose repression and use multiple carbon sources in the presence of glucose. Some bacteria secrete a chemical factor that induces [GAR[superscript +]]. [GAR[superscript +]] is advantageous to bacteria because yeast cells make less ethanol, and is advantageous to yeast because their growth and long-term viability is improved in complex carbon sources. This crosskingdom communication is broadly conserved, providing a compelling argument for its adaptive value. By heritably transforming growth and survival strategies in response to the selective pressures of life in a biological community, [GAR[superscript +]] presents a unique example of Lamarckian inheritance.