Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity

FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts, United States of America.
PLoS Biology (Impact Factor: 9.34). 08/2011; 9(8):e1001122. DOI: 10.1371/journal.pbio.1001122
Source: PubMed


Author Summary
The evolution of multicellularity is one of the major steps in the history of life and has occurred many times independently. Despite this, we do not understand how and why single-celled organisms first joined together to form multicellular clumps of cells. Here, we show that clumps of cells can cooperate, using secreted enzymes, to collect food from the environment. In nature, the budding yeast Saccharomyces cerevisiae grows as multicellular clumps and secretes invertase, an enzyme that breaks down sucrose into smaller sugars (glucose and fructose) that cells can import. We genetically manipulate both clumping and secretion to show that multicellular clumps of cells can grow when sucrose is scarce, whereas single cells cannot. In addition, we find that clumps of cells have an advantage when competing against “cheating” cells that import sugars but do not make invertase. Since the evolution of secreted enzymes predates the origin of multicellularity, we argue that the social benefits conferred by secreted enzymes were the driving force for the evolution of cell clumps that were the first, primitive form of multicellular life.

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    • "Consistent with this social theory model, laboratory experiments find that the relative fitness of nonproducers can be higher or lower than that of producers, depending on factors such as density (Greig & Travisano 2004), frequency (Gore et al. 2009; Damore & Gore Correspondence: Gonensin O. Bozdag, Fax: +49 4522 763-260; E-mail: 2012) and sucrose concentration (Koschwanez et al. 2011). However, a recent experiment found that mixed cultures of producers and nonproducers had higher mean fitness than monocultures of producers, inconsistent with the model of nonproducers as cheats (MacLean et al. 2010). "
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    ABSTRACT: The sharing of secreted invertase by yeast cells is a well established laboratory model for cooperation, but the only evidence that such cooperation occurs in nature is that the SUC loci, which encode invertase, vary in number and functionality. Genotypes that do not produce invertase can act as “cheats” in laboratory experiments, growing on the glucose that is released when invertase producers, or “cooperators”, digest sucrose. However, genetic variation for invertase production might instead be explained by adaptation of different populations to different local availabilities of sucrose, the substrate for invertase. Here we find that, 110 wild yeast strains isolated from natural habitats, all contained a single SUC locus and produced invertase; none were “cheats”. The only genetic variants we found were three strains isolated instead from sucrose-rich nectar, which produced higher levels of invertase from three additional SUC loci at their sub-telomeres. We argue that the pattern of SUC gene variation is better explained by local adaptation than by social conflict.This article is protected by copyright. All rights reserved.
    Molecular Ecology 08/2014; 23(20). DOI:10.1111/mec.12904 · 6.49 Impact Factor
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    • "For example, cells that have divided can remain attached to each other forming multi-cellular filaments or aggregates. ST in the context of cellular division can therefore lead to the evolution of multi-cellularity, which is a major topic of investigation (Bell and Mooers, 1997; Bonner, 1998, 2008; Maynard Smith and Szathmary, 1998; Michod, 1999, 2007; Furusawa and Kaneko, 2000; Carroll, 2001; Pfeiffer and Bonhoeffer, 2003; Kirk, 2003, 2005; King, 2004; Grosberg and Strathmann, 2007; Rainey, 2007; Willensdorfer, 2008; Kolter, 2010; Rossetti et al., 2010, 2011; Koschwanez et al., 2011; Ratcliff et al., 2012, 2013; Norman et al., 2013). Another example of ST is that the offspring of a social insect do not leave the nest but stay with their mother and participate in raising further offspring (Wilson, 1971; Gadagkar, 1994, 2001; Hunt, 2007; Hölldobler and Wilson, 2009). "
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    ABSTRACT: Staying together means that replicating units do not separate after reproduction, but remain attached to each other or in close proximity. Staying together is a driving force for evolution of complexity, including the evolution of multi-cellularity and eusociality. We analyze the fixation probability of a mutant that has the ability to stay together. We assume that the size of the complex affects the reproductive rate of its units and the probability of staying together. We examine the combined effect of natural selection and random drift on the emergence of staying together in a finite sized population. The number of states in the underlying stochastic process is an exponential function of population size. We develop a framework for any intensity of selection and give closed form solutions for special cases. We derive general results for the limit of weak selection.
    Journal of Theoretical Biology 06/2014; 360. DOI:10.1016/j.jtbi.2014.06.026 · 2.12 Impact Factor
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    • "Public goods produced in the interior of a cluster are less likely to escape if there are a greater number of cells in the cluster. Indeed, there is growing evidence that spatial clustering enhances cooperation in microbial populations where public goods are exchanged (Kummerli et al., 2009; Julou et al., 2013; Momeni et al., 2014; Allison, 2005; Misevic et al., 2012; Buckling et al., 2007; Koschwanez et al., 2011; Allen et al., 2014; Gore et al., 2009; Damore and Gore, 2012). We modify our fitnesses to incorporate the advantage of clustering. "
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    ABSTRACT: We study the coevolution of staying together and cooperation. Staying together means that replicating units do not separate after reproduction, but remain in proximity. For example, following cell division the two daughter cells may not fully separate but stay attached to each other. Repeated cell division thereby can lead to a simple multi-cellular complex. We assume that cooperators generate a diffusible public good, which can be absorbed by any cell in the system. The production of the public good entails a cost, while the absorption leads to a benefit. Defectors produce no public good. Defectors have a selective advantage unless a mechanism for evolution of cooperation is at work. Here we explore the idea that the public good produced by a cooperating cell is absorbed by cells of the same complex with a probability that depends on the size of the complex. Larger complexes are better at absorbing the public goods produced by their own individuals. We derive analytical conditions for the evolution of staying together, thereby studying the coevolution of clustering and cooperation. If cooperators and defectors differ in their intrinsic efficiency to absorb the public good, then we find multiple stable equilibria and the possibility for coexistence between cooperators and defectors. Finally we study the implications of disadvantages that might arise if complexes become too large.
    Journal of Theoretical Biology 06/2014; 360. DOI:10.1016/j.jtbi.2014.06.023 · 2.12 Impact Factor
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