title: 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(+)], 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(+)]. [GAR(+)] 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 cross-kingdom 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(+)] presents a unique example of Lamarckian inheritance.
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Departments of Chemical and Systems Biology and of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.
authors.forename: Daniel F
authors.initials: DF
authors.lastname: Jarosz
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Jessica C S
authors.initials: JCS
authors.lastname: Brown
authors.affiliation: Department of Viticulture and Enology, University of California, Davis, Davis, CA 95616, USA.
authors.forename: Gordon A
authors.initials: GA
authors.lastname: Walker
authors.affiliation: Computational and Systems Biology Initiative, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Manoshi S
authors.initials: MS
authors.lastname: Datta
authors.affiliation: Department of Physics, Harvard University, Cambridge, MA 02138, USA.
authors.forename: W Lloyd
authors.initials: WL
authors.lastname: Ung
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Department of Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA; Center for Biomedical Informatics, Harvard Medical School, Boston, MA 02115, USA.
authors.forename: Alex K
authors.initials: AK
authors.lastname: Lancaster
authors.affiliation: Department of Physics, Harvard University, Cambridge, MA 02138, USA.
authors.forename: Assaf
authors.initials: A
authors.lastname: Rotem
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Amelia
authors.initials: A
authors.lastname: Chang
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Gregory A
authors.initials: GA
authors.lastname: Newby
authors.affiliation: Department of Physics, Harvard University, Cambridge, MA 02138, USA; School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA.
authors.forename: David A
authors.initials: DA
authors.lastname: Weitz
authors.affiliation: Department of Viticulture and Enology, University of California, Davis, Davis, CA 95616, USA. Electronic address: lfbisson@ucdavis.edu.
authors.forename: Linda F
authors.initials: LF
authors.lastname: Bisson
authors.affiliation: Whitehead Institute for Biomedical Research, Cambridge, MA 02142, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA; Howard Hughes Medical Institute, Chevy Chase, MD 20815, USA. Electronic address: lindquist_admin@wi.mit.edu.
authors.forename: Susan
authors.initials: S
authors.lastname: Lindquist
mesh_terms: D044127:Epigenesis, Genetic; D005285:Fermentation; D005947:Glucose / Q000378:metabolism; D011328:Prions / Q000378:metabolism*; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000378:metabolism*; D041181:Staphylococcus hominis / Q000235:genetics / Q000378:metabolism*; D014920:Wine / Q000382:microbiology; D015003:Yeasts / Q000235:genetics / Q000378:metabolism
chemical_list: D011328:Prions; D005947:Glucose