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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    • "Nivel/Organismo Microorganismos Plantas Invertebrados Vertebrados Ecosistemas Swenson et al. 2000a, b Comunidades Brookfield 1998; Xavier y Foster 2007; Nadell et al. 2008, 2009, 2015; Xavier et al. 2009; Mitri et al. 2011; Cornforth y Foster 2013 Pfister y Hay 1988; Hjältén et al. 1993; Campbell et al. 1997; Danell et al. 1999 Goodnight 1990a, b Vedder et al. 2014; Campobello et al. 2015 Meta-Poblaciones Acosta et al. 1993; Solis et al. 2002; McIntre y Fajardo 2011; Driscoll et al. 2013 Korb y Foster 2010 Demes, grupos De Vargas Roditi et al. 2013 Goodnight 1985; Stevens et al. 1995; Kelly 1996; McCauley y Taylor 1997; McCauley et al. 2000; Aspi et al. 2003; Donohue 2003, 2004; Weinig et al. 2007; Weiner et al. 2010; López Bernal et al. 2012; Marín y Weiner 2014 Wade 1976, 1977, 1980, 1982, 1987; Wade y McCauley 1980; McCauley y Wade 1980; Craig 1982; Breden y Wade 1989; Wade y Goonight 1991; Tsuji 1995; Banschbach y Herbers 1996, 1999; Schamber y Muir 2001; Eldakar et al. 2010; Formica et al. 2011; Pruitt y Goodnight 2014 McClintock 1984; Muir 1996; Craig y Muir 1996a, b; Hester et al. 1996a, b, c; Cheng et al. 2001a, b; Foster y Ratnieks 2005; Laiolo y Obseo 2012; Moorad 2013a, b; Muir et al. 2013; Searcy et al. 2014 Organismos, clones Alpert 1991, 1996, 1999; Cheplick 1997; Holzapfel y Alpert 2003 Células Foster et al. 2002; Queller et al. 2003; Castillo et al. 2005; Gilbert et al. 2007, 2009; Kuzdzal-Fick et al. 2007; Koschwanez et al. 2011, 2013; Ratcliff et al. 2012, 2013a, b Nedelcu y Michod 2006; Michod 2007; Herron y Michod 2008; Herron et al. 2009 "
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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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