TEMPO AND MODE OF MULTICELLULAR ADAPTATION IN EXPERIMENTALLY EVOLVED<i>SACCHAROMYCES CEREVISIAE</i>

Ratcliff, William C.; Pentz, Jennifer; Travisano, Michael

doi:10.1111/evo.12101

Cited by 49 publications

(80 citation statements)

References 56 publications

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“…Where previous reports studied evolution of S. cerevisiae in serial shake flask cultures (29-33), we reproducibly observed the occurrence of large multicellular clusters during prolonged anaerobic cultivation of the haploid S. cerevisiae strain CEN.PK113-7D (34) in sequential bioreactor batch cultures. The phenotype of these clusters was similar to the "snowflake yeast" previously described by Ratcliff and coworkers (21,35). The design of the "fill and draw" system used in our bioreactors provided an unintended selective advantage to fast-sedimenting cell lines.…”

Section: Selection Of Multicellular Clusters In Sequential Bioreactorsupporting

confidence: 56%

Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae

Oud

Guadalupe-Medina

Nijkamp

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

101

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Significance The shift from unicellular to multicellular life forms represents a key innovation step in the evolution of life on Earth. However, knowledge on the evolutionary pressures resulting in the selection of multicellular life forms and the underlying molecular mechanisms is far from complete. Our study provides a complete identification of the specific genetic changes by which the unicellular eukaryote S. cerevisiae can acquire a multicellular, fast-sedimenting phenotype. We demonstrated that a minimal evolutionary mechanism encompassed a deregulation of the late step of the cell cycle through mutation in ACE2 followed by whole genome duplication.

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Section: Selection Of Multicellular Clusters In Sequential Bioreactorsupporting

confidence: 56%

Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae

Oud

Guadalupe-Medina

Nijkamp

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

101

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“…Using complementation with the wild-type allele, we verified that the ACE2 mutations were causative of the separation defect aggregation phenotype in these two clones (Table 1), with subtle modification to the cell morphology by BEM2-a gene involved in bud emergence that is also mutated in both clones ( Figure S2B in File S1) (Bender and Pringle 1991;Kim et al 1994). This type of separation defect in yeast is considered a type of multicellularity, and can be an adaptive trait when cells are challenged with local dispersal of nutrients (Koschwanez et al 2011(Koschwanez et al , 2013, settling (Ratcliff et al 2012(Ratcliff et al , 2013, or, as we show here, residence time in chemostats (Oud et al 2013). We would predict that floc formation could also be an adaptive strategy for cultures evolved under certain stress treatments.…”

Section: Majority Of Aggregating Clones Demonstrate Characteristics Osupporting

confidence: 54%

Experimental evolution reveals favored adaptive routes to cell aggregation in yeast

Hope

Amorosi

Miller

et al. 2016

Preprint

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Yeast flocculation is a community-building cell aggregation trait that is an important mechanism of stress resistance and a useful phenotype for brewers; however, it is also a nuisance in many industrial processes, in clinical settings, and in the laboratory. Chemostat-based evolution experiments are impaired by inadvertent selection for aggregation, which we observe in 35% of populations. These populations provide a testing ground for understanding the breadth of genetic mechanisms Saccharomyces cerevisiae uses to flocculate, and which of those mechanisms provide the biggest adaptive advantages. In this study, we employed experimental evolution as a tool to ask whether one or many routes to flocculation are favored, and to engineer a strain with reduced flocculation potential. Using a combination of whole genome sequencing and bulk segregant analysis, we identified causal mutations in 23 independent clones that had evolved cell aggregation during hundreds of generations of chemostat growth. In 12 of those clones, we identified a transposable element insertion in the promoter region of known flocculation gene FLO1, and, in an additional five clones, we recovered loss-of-function mutations in transcriptional repressor TUP1, which regulates FLO1 and other related genes. Other causal mutations were found in genes that have not been previously connected to flocculation. Evolving a flo1 deletion strain revealed that this single deletion reduces flocculation occurrences to 3%, and demonstrated the efficacy of using experimental evolution as a tool to identify and eliminate the primary adaptive routes for undesirable traits.

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“…Recently, however, this constraint has been circumvented through experimental evolution of novel multicellular organisms [6][7][8]11 , genetic reconstruction of early events 12 and experiments comparing extant multicellular taxa with their unicellular relatives 13,14 . To examine the biophysical basis of the evolution of increased size in a nascent multicellular organism, we employed the tractable 'snowflake' yeast model system [6][7][8] . Multicellular snowflake clusters evolved from the unicellular baker's yeast Saccharomyces cerevisiae under daily selection for rapid settling speed in liquid media 6 .…”

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confidence: 99%

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confidence: 99%

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Cellular packing, mechanical stress and the evolution of multicellularity

et al. 2017

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The evolution of multicellularity set the stage for sustained increases in organismal complexity [1][2][3][4][5] . However, a fundamental aspect of this transition remains largely unknown: how do simple clusters of cells evolve increased size when confronted by forces capable of breaking intracellular bonds? Here we show that multicellular snowflake yeast clusters 6-8 fracture due to crowding-induced mechanical stress. Over seven weeks (~291 generations) of daily selection for large size, snowflake clusters evolve to increase their radius 1.7-fold by reducing the accumulation of internal stress. During this period, cells within the clusters evolve to be more elongated, concomitant with a decrease in the cellular volume fraction of the clusters. The associated increase in free space reduces the internal stress caused by cellular growth, thus delaying fracture and increasing cluster size. This work demonstrates how readily natural selection finds simple, physical solutions to spatial constraints that limit the evolution of group size-a fundamental step in the evolution of multicellularity.The first step in the transition to multicellularity-prior to the origin of cellular division of labour, genetically regulated development and complex multicellular forms-was the evolution of simple multicellular clusters [1][2][3][4][5] . Long before simple clusters of cells can evolve traits characteristic of complex multicellularity, they must contend with physical forces-both internal and external-that are capable of breaking cell-cell bonds and thus limit cluster size. This physical challenge is critical for several reasons. First, large size is a likely prerequisite to the evolution of complex multicellularity 2,3 . Second, these forces act on long length scales that were probably irrelevant to a single-cell ancestor, and are thus evolutionarily novel. Finally, it is unclear how simple multicellular clusters that do not yet possess genetically regulated developmental systems can evolve novel multicellular morphology.Direct experimental investigation of the early steps in the transition to multicellularity has been challenging, largely because these transitions occurred long ago, and the evolutionary path to multicellularity has been obscured by extinction in most extant lineages 9,10 . Recently, however, this constraint has been circumvented through experimental evolution of novel multicellular organisms [6][7][8]11 , genetic reconstruction of early events 12 and experiments comparing extant multicellular taxa with their unicellular relatives 13,14 . To examine the biophysical basis of the evolution of increased size in a nascent multicellular organism, we employed the tractable 'snowflake' yeast model system [6][7][8] . Multicellular snowflake clusters evolved from the unicellular baker's yeast Saccharomyces cerevisiae under daily selection for rapid settling speed in liquid media 6 . The resulting snowflake growth form is the consequence of a single mutation in the ACE2 gene . This mutation prevents cell separation after ...

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TEMPO AND MODE OF MULTICELLULAR ADAPTATION IN EXPERIMENTALLY EVOLVEDSACCHAROMYCES CEREVISIAE

Cited by 49 publications

References 56 publications

Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae

Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae

Experimental evolution reveals favored adaptive routes to cell aggregation in yeast

Cellular packing, mechanical stress and the evolution of multicellularity

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