Cell Signals, Cell Contacts, and the Organization of Yeast Communities

Abstract

Even relatively simple species have evolved mechanisms to organize individual organisms into communities, such that the fitness of the group is greater than the fitness of isolated individuals. Within the fungal kingdom, the ability of many yeast species to organize into communities is crucial for their growth and survival, and this property has important impacts both on the economy and on human health. Over the last few years, studies of Saccharomyces cerevisiae have revealed several fundamental properties of yeast communities. First, strainto-strain variation in the structures of these groups is attributable in part to variability in the expression and functions of adhesin proteins. Second, the extracellular matrix surrounding these communities can protect them from environmental stress and may also be important in cell signaling. Finally, diffusible signals between cells contribute to community organization so that different regions of a community express different genes and adopt different cell fates. These findings provide an arena in which to view fundamental mechanisms by which contacts and signals between individual organisms allow them to assemble into functional communities.In many species, including our own, individual organisms assemble into communities to increase their overall fitness. Even in unicellular organisms like Saccharomyces cerevisiae, individual cells can organize themselves into a variety of types of multicellular aggregates. These biotic communities likely provide overall benefit to these yeast populations, for example by protecting organisms in the core of the structure from environmental stresses or by specializing functions to subpopulations within the community. Yeast communities also have broad relevance to human health and to industry. For example, biofilms formed by pathogenic yeasts on medical devices, such as catheters, are a major cause of the very high mortality rates of hospital-acquired fungal infections (reviewed in references 11, 43, and 44). Furthermore, surface film communities formed on food by spoilage yeasts may result in losses of billions of dollars annually (reviewed in reference 58). Yet the mechanisms underlying the organization of these communities are still poorly understood.In the first section of this paper, I review types of yeast communities, focusing on the model yeast Saccharomyces cerevisiae, and briefly discuss broader aspects of two processes fundamental to yeast communities: cell-cell signaling and cell adhesion. In the second section, I discuss four aspects of yeast community organization highlighted by recent publications: boundary formation, cell adhesion, the extracellular matrix (ECM), and diffusible cell-cell signals. Much of this recent progress has focused on the cytological structures of these communities and on the identification of several genetic pathways required for this organization. BACKGROUND. (I) THE MULTIFARIOUSYEAST COMMUNITY

Resolving Conflicts During the Evolutionary Transition to Multicellular Life

“…Pre-existing genetic history and development within the context of single cells provide possibilities for innovations to arise from minor genetic changes that can cause existing life-history variation to be remolded in collective settings (Michod & Herron 2006). Similarly, the recruitment of genes, regulatory networks (Newman & Bhat 2008), and functional modules (Niklas 2014, Niklas & Newman 2013) that evolved for cell-level purposes can often provide unanticipated collective-level benefits (Honigberg 2011, Sebe-Pedros et al 2013, Smukalla et al 2008, Sole & Valverde 2013, Umen & Olson 2012. From such bases, rudimentary life cycles can emerge.…”

“…This mechanism was likely common among primordial multicellular collectives and is encountered in many extant minor multicellular taxa, such as the social amoeba (Herron et al 2013, Pepper & Herron 2008. Indeed, there are numerous examples where multicellular collectives appear to be maintained in the face of frequent mixing that is expected to promote the emergence of conflicts (Herron et al 2013, Honigberg 2011, Sebe-Pedros et al 2013.…”

Cell Differentiation and Spatial Organization in Yeast Colonies: Role of Cell-Wall Integrity Pathway

“…Intriguingly, even unicellular microbial species form communities in which different cell types are organized into patterns [reviewed in Kaiser et al (2010), Honigberg (2011, and Loomis (2014)]. For example, colonies of the budding yeast Saccharomyces cerevisiae form an upper layer of larger cells (U cells) overlying a layer of smaller cells (L cells).…”

“…Colony sporulation patterns may reflect differences in nutrient environment across the community as well as cell-to-cell signals within communities [reviewed in Honigberg (2011)]. One function of sporulation patterning may be to localize sporulated cells to the surfaces of colonies to maximize their dispersal; spores are resistant to environmental stress and may be largely dispersed by insect vectors that feed at the surfaces of these microbial communities [reviewed in Neiman (2011)].…”

The Genetic Architecture of Biofilm Formation in a Clinical Isolate of Saccharomyces cerevisiae

“…Recent studies have demonstrated that the budding yeast Saccharomyces forms microbial communities that have these biofilm characteristics (Kuthan et al 2003;Váchová et al 2011). These characteristics are present in mats that form on soft agar (Reynolds and Fink 2001) and in complex colony biofilms (sometimes referred to as "fluffy colonies") that are distinguished from nonbiofilm colonies (also described as simple or smooth colonies) by intricate, organized, and strain-specific architecture (Supporting Information, Figure S1) (Palková and Váchová 2006;Granek and Magwene 2010;Honigberg 2011). These complex colony biofilms are also formed by the more prevalent fungal pathogens Candida albicans (Hall et al 2010) and Cryptococcus neoformans (Goldman et al 1998), where they are associated with pathogenicity.…”