Clonal yeast biofilms can reap competitive advantages through cell differentiation without being obligatorily multicellular.
How differentiation between cell types evolved is a fundamental question in biology, but few studies have explored single-gene phenotypes that mediate first steps towards division of labour with selective advantage for groups of cells. Here, we show that differential expression of the FLO11 gene produces stable fractions of Flo11+and Flo11-cells in clonal Saccharomyces cerevisiae biofilm colonies on medium with intermediate viscosity. Differentiated Flo11+/-colonies, consisting of adhesive and non-adhesive cells, obtain a fourfold growth advantage over undifferentiated colonies by overgrowing glucose resources before depleting them, rather than depleting them while they grow as undifferentiated Flo11-colonies do. Flo11+/-colonies maintain their structure and differentiated state by switching non-adhesive cells to adhesive cells with predictable probability. Mixtures of Flo11+and Flo11-cells from mutant strains that are unable to use this epigenetic switch mechanism produced neither integrated colonies nor growth advantages, so the condition-dependent selective advantages of differentiated FLO11 expression can only be reaped by clone-mate cells. Our results show that selection for cell differentiation in clonal eukaryotes can evolve before the establishment of obligate undifferentiated multicellularity, and without necessarily leading to more advanced organizational complexity.
Cell Biology and Physiology, Department of Biology, Universitetsparken 15, 2100 Copenhagen, Denmark bregenberg@bio.ku.dk.
Birgitte
0000-0003-4996-7012
B
Regenberg
Cell Biology and Physiology, Department of Biology, Universitetsparken 15, 2100 Copenhagen, Denmark.
Kristian Ebbesen
KE
Hanghøj
Cell Biology and Physiology, Department of Biology, Universitetsparken 15, 2100 Copenhagen, Denmark.
Kaj Scherz
KS
Andersen
Centre for Social Evolution, Department of Biology, Universitetsparken 15, 2100 Copenhagen, Denmark.
Jacobus J
JJ
Boomsma
D018441:Biofilms; D002454:Cell Differentiation; D008562:Membrane Glycoproteins / Q000502:physiology*; D012441:Saccharomyces cerevisiae / Q000166:cytology* / Q000254:growth & development; D029701:Saccharomyces cerevisiae Proteins / Q000502:physiology*
C110690:FLO11 protein, S cerevisiae; D008562:Membrane Glycoproteins; D029701:Saccharomyces cerevisiae Proteins
cooperation; differentiation; division of labour; multicellularity