Flo11p adhesin required for meiotic differentiation in Saccharomyces cerevisiae minicolonies grown on plastic surfaces

White, Melissa G.; Piccirillo, Sarah; Dusevich, Vladimir; Law, Douglas; Kapros, Tamás; Honigberg, Saul M.

doi:10.1111/j.1567-1364.2010.00712.x

Cited by 11 publications

(20 citation statements)

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“…A different type of colony sporulation pattern forms in structures termed "minicolonies" (69). Minicolonies are related to biofilms in that they grow on a plastic surface submerged in liquid; however, unlike biofilms, minicolonies form limited structures rather than expanding to cover the entire surface.…”

Section: (I) Community Boundariesmentioning

confidence: 99%

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

Honigberg

2011

Eukaryot Cell

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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

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Section: (I) Community Boundariesmentioning

confidence: 99%

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

Honigberg

2011

Eukaryot Cell

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“…U and L cells differ in their metabolism, gene expression, and resistance to stress, and U and L layers are separated by a strikingly sharp boundary Vachova et al 2013). Patterns are also observed in yeast biofilms, where cells closest to the plastic surface grow as ovoid cells, whereas cells further from the surface differentiate into hyphae for Candida species [reviewed in Finkel and Mitchell (2011)] or pseudohyphae and eventually asci for S. cerevisiae (White et al 2011).…”

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confidence: 99%

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

Piccirillo¹,

Morales²,

White³

et al. 2015

Genetics

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Many microbial communities contain organized patterns of cell types, yet relatively little is known about the mechanism or function of this organization. In colonies of the budding yeast Saccharomyces cerevisiae, sporulation occurs in a highly organized pattern, with a top layer of sporulating cells sharply separated from an underlying layer of nonsporulating cells. A mutant screen identified the Mpk1 and Bck1 kinases of the cell-wall integrity (CWI) pathway as specifically required for sporulation in colonies. The CWI pathway was induced as colonies matured, and a target of this pathway, the Rlm1 transcription factor, was activated specifically in the nonsporulating cell layer, here termed feeder cells. Rlm1 stimulates permeabilization of feeder cells and promotes sporulation in an overlying cell layer through a cell-nonautonomous mechanism. The relative fraction of the colony apportioned to feeder cells depends on nutrient environment, potentially buffering sexual reproduction against suboptimal environments.KEYWORDS cell-wall integrity; cell permeability; cell-cell signaling; Saccharomyces cerevisiae; sporulation A S embryos develop, cells of different fates organize into patterns [reviewed in Kicheva et al. (2012) and Perrimon et al. (2012)] . 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). U and L cells differ in their metabolism, gene expression, and resistance to stress, and U and L layers are separated by a strikingly sharp boundary Vachova et al. 2013). Patterns are also observed in yeast biofilms, where cells closest to the plastic surface grow as ovoid cells, whereas cells further from the surface differentiate into hyphae for Candida species [reviewed in Finkel and Mitchell (2011)] or pseudohyphae and eventually asci for S. cerevisiae (White et al. 2011).Sporulation also occurs in patterns within yeast colonies. Specifically, a narrow horizontal layer of sporulated cells forms through the center of the colony early during colony development. As colonies continue to mature, this layer progressively expands upward to include the top of the colony; this wave is driven by progressive alkalization and activation of the Rim101 signaling pathway . In contrast, cells at the bottom of the colony, i.e., directly contacting the agar substrate, also sporulate at early stages of colony development, but this narrow cell layer does not expand as the colony matures . The same colony sporulation pattern is observed in a range of laboratory yeasts as well as in S. cerevisiae and S. paradoxus isolated from the wild. Indeed, in these wild yeasts, the same colony sporulation pattern forms on a range of fermentable and nonfermentable carbon sources .The mechanism of sporulation patterning and its function remai...

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“…Ʃ1278b) phg occurs most efficiently in medium containing glucose, whereas in other strain backgrounds (e.g. SK1), phg occurs most efficiently in NFCs 56575859. Finally, as with phg and sporulation, the rate of ageing in quiescent cells varies significantly between different laboratory strains 60.…”

Section: Lessons From the Wildmentioning

confidence: 96%

“…The diversity of flocculin-dependent phenotypes reflects the variety of communities that can form in this species. For example, the FLO11 flocculin is required to form "structured colonies", which have with a distinctive lacey appearance 130131, "mats", which are large thin colonies formed on low agar (high moisture) plates 132, "flors", which are thin colonies of yeast that form on the top of liquid cultures 133, "flocs", which are large clumps of cells that form suspended in cultures 58134, and "minicolonies" which are biofilm like structures that adhere to plastic surfaces submerged in medium 56133. Both lab and natural yeast isolates vary considerably in their ability to undergo these phg-spectrum phenotypes 20131.…”

Section: Varying Fates Varying Functionsmentioning

confidence: 99%

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Similar environments but diverse fates: Responses of budding yeast to nutrient deprivation

Honigberg¹

2016

Microbial Cell

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Diploid budding yeast (Saccharomyces cerevisiae) can adopt one of several alternative differentiation fates in response to nutrient limitation, and each of these fates provides distinct biological functions. When different strain backgrounds are taken into account, these various fates occur in response to similar environmental cues, are regulated by the same signal transduction pathways, and share many of the same master regulators. I propose that the relationships between fate choice, environmental cues and signaling pathways are not Boolean, but involve graded levels of signals, pathway activation and master-regulator activity. In the absence of large differences between environmental cues, small differences in the concentration of cues may be reinforced by cell-to-cell signals. These signals are particularly essential for fate determination within communities, such as colonies and biofilms, where fate choice varies dramatically from one region of the community to another. The lack of Boolean relationships between cues, signaling pathways, master regulators and cell fates may allow yeast communities to respond appropriately to the wide range of environments they encounter in nature.

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Flo11p adhesin required for meiotic differentiation in Saccharomyces cerevisiae minicolonies grown on plastic surfaces

Cited by 11 publications

References 44 publications

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

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

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

Similar environments but diverse fates: Responses of budding yeast to nutrient deprivation

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