Yeasts create multicellular structures of varying complexity, such as more complex colonies and biofilms and less complex flocs, each of which develops via different mechanisms. Colony biofilms originate from one or more cells that, through growth and division, develop a complicated three-dimensional structure consisting of aerial parts, agar-embedded invasive parts and a central cavity, filled with extracellular matrix. In contrast, flocs arise relatively quickly by aggregation of planktonic cells growing in liquid cultures after they reach the appropriate growth phase and/or exhaust nutrients such as glucose. Creation of both types of structures is dependent on the presence of flocculins: Flo11p in the former case and Flo1p in the latter. We recently showed that formation of both types of structures by wild Saccharomyces cerevisiae strain BR-F is regulated via transcription regulators Tup1p and Cyc8p, but in a divergent manner. Biofilm formation is regulated by Cyc8p and Tup1p antagonistically: Cyc8p functions as a repressor of FLO11 gene expression and biofilm formation, whereas Tup1p counteracts the Cyc8p repressor function and positively regulates biofilm formation and Flo11p expression. In addition, Tup1p stabilizes Flo11p probably by repressing a gene coding for a cell wall or extracellular protease that is involved in Flo11p degradation. In contrast, formation of BR-F flocs is co-repressed by the Cyc8p-Tup1p complex. These findings point to different mechanisms involved in yeast multicellularity.
- MeSH
- Biofilms MeSH
- Cell Wall genetics metabolism MeSH
- Species Specificity MeSH
- Nuclear Proteins genetics metabolism MeSH
- Gene Expression Regulation, Fungal * MeSH
- Repressor Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae classification genetics physiology MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Yeasts, like other microorganisms, create numerous types of multicellular communities, which differ in their complexity, cell differentiation and in the occupation of different niches. Some of the communities, such as colonies and some types of biofilms, develop by division and subsequent differentiation of cells growing on semisolid or solid surfaces to which they are attached or which they can penetrate. Aggregation of individual cells is important for formation of other community types, such as multicellular flocs, which sediment to the bottom or float to the surface of liquid cultures forming flor biofilms, organized at the border between liquid and air under specific circumstances. These examples together with the existence of more obscure communities, such as stalks, demonstrate that multicellularity is widespread in yeast. Despite this fact, identification of mechanisms and regulations involved in complex multicellular behavior still remains one of the challenges of microbiology. Here, we briefly discuss metabolic differences between particular yeast communities as well as the presence and functions of various differentiated cells and provide examples of the ability of these cells to develop different ways to cope with stress during community development and aging.
During their development and aging on solid substrates, yeast giant colonies produce ammonia, which acts as a quorum sensing molecule. Ammonia production is connected with alkalization of the surrounding medium and with extensive reprogramming of cell metabolism. In addition, ammonia signaling is important for both horizontal (colony centre versus colony margin) and vertical (upper versus lower cell layers) colony differentiations. The centre of an aging differentiated giant colony is thus composed of two major cell subpopulations, the subpopulation of long-living, metabolically active and stress-resistant cells that form the upper layers of the colony and the subpopulation of stress-sensitive starving cells in the colony interior. Here, we show that microcolonies originating from one cell pass through similar developmental phases as giant colonies. Microcolony differentiation is linked to ammonia signaling, and cells similar to the upper and lower cells of aged giant colonies are formed even in relatively young microcolonies. A comparison of the properties of these cells revealed a number of features that are similar in microcolonies and giant colonies as well as a few that are only typical of chronologically aged giant colonies. These findings show that colony age per se is not crucial for colony differentiation.
- MeSH
- Ammonia metabolism MeSH
- Yeasts metabolism MeSH
- Signal Transduction physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
When growing on solid surfaces, yeast, like other microorganisms, develops organized multicellular populations (colonies and biofilms) that are composed of differentiated cells with specialized functions. Life within these populations is a prevalent form of microbial existence in natural settings that provides the cells with capabilities to effectively defend against environmental attacks as well as efficiently adapt and survive long periods of starvation and other stresses. Under such circumstances, the fate of an individual yeast cell is subordinated to the profit of the whole population. In the past decade, yeast colonies, with their complicated structure and high complexity that are also developed under laboratory conditions, have become an excellent model for studies of various basic cellular processes such as cell interaction, signaling, and differentiation. In this paper, we summarize current knowledge on the processes related to chronological aging, adaptation, and longevity of a colony cell population and of its differentiated cell constituents. These processes contribute to the colony ability to survive long periods of starvation and mostly differ from the survival strategies of individual yeast cells.
- MeSH
- Models, Biological MeSH
- Time Factors MeSH
- Longevity physiology MeSH
- Adaptation, Physiological MeSH
- Yeasts cytology growth & development metabolism physiology MeSH
- Humans MeSH
- Colony Count, Microbial MeSH
- Environment MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Much like other microorganisms, wild yeasts preferentially form surface-associated communities, such as biofilms and colonies, that are well protected against hostile environments and, when growing as pathogens, against the host immune system. However, the molecular mechanisms underlying the spatiotemporal development and environmental resistance of biofilms and colonies remain largely unknown. In this paper, we show that a biofilm yeast colony is a finely tuned, complex multicellular organism in which specialized cells jointly execute multiple protection strategies. These include a Pdr1p-regulated mechanism whereby multidrug resistance transporters Pdr5p and Snq2p expel external compounds solely within the surface cell layers as well as developmentally regulated production by internal cells of a selectively permeable extracellular matrix. The two mechanisms act in concert during colony development, allowing growth of new cell generations in a well-protected internal cavity of the colony. Colony architecture is strengthened by intercellular fiber connections.
- MeSH
- ATP-Binding Cassette Transporters genetics metabolism MeSH
- Biofilms growth & development MeSH
- Models, Biological MeSH
- Gene Deletion MeSH
- DNA-Binding Proteins genetics metabolism MeSH
- Extracellular Matrix physiology MeSH
- Galactokinase genetics metabolism MeSH
- Galactose metabolism MeSH
- Hydroxymethylglutaryl CoA Reductases genetics metabolism MeSH
- Copper metabolism MeSH
- Membrane Glycoproteins genetics metabolism MeSH
- Metallothionein genetics metabolism MeSH
- Oxazines metabolism MeSH
- Permeability MeSH
- Profilins genetics MeSH
- Cell Cycle Proteins genetics MeSH
- Multidrug Resistance-Associated Proteins genetics metabolism MeSH
- Recombinant Fusion Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae cytology growth & development metabolism MeSH
- Transcription Factors genetics metabolism MeSH
- Green Fluorescent Proteins genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Yeast multicellular colonies possess several traits that are absent from individual yeasts. These include the ability to synchronize colony population development and adapt its metabolism to different environmental changes, such as nutrient depletion. This, together with cell diversification to cell variants with distinct metabolic and other properties, contributes to the main goal of the colony population: to achieve longevity. In this respect, a benefit to individual cells is subordinated to the benefit to the whole population, exhibiting a kind of altruistic behaviour. For example, some colony cells located at particular positions undergo regulated cell dying and provide components to other cells located in more propitious areas. The enhancement of techniques that enable the in vivo investigation of three-dimensional spatiotemporal colony development may lead to new discoveries on metabolic differentiation and regulation in the near future.
- MeSH
- Cell Differentiation physiology MeSH
- Cell Death MeSH
- Longevity physiology MeSH
- Energy Metabolism physiology MeSH
- Saccharomyces cerevisiae cytology metabolism physiology MeSH
- Cellular Senescence physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Microorganisms in nature form organized multicellular structures (colonies, biofilms) possessing properties absent in individual cells. These are often related to the better ability of communities to survive long-lasting starvation and stress and include mechanisms of adaptation and cell specialization. Thus, yeast colonies pass through distinct developmental phases characterized by changes in pH and the production of ammonia-signalling molecules. Here, we show that Saccharomyces cerevisiae colony transition between major developmental phases (first acidic, alkali, second acidic) is accompanied by striking transcription changes, while the development within each particular phase is guided mostly at the post-transcriptional level. First- and second-acidic-phase colonies markedly differ. Second-acidic-phase colonies maintain the adaptive metabolism activated in the ammonia-producing period, supplemented by additional changes, which begin after colonies enter the second acidic phase. Cells with particular properties are not homogenously dispersed throughout the colony population, but localize to specific colony regions. Thus, cells located at the colony margin are able to export higher amounts of ammonium than central cells and to activate an adaptive metabolism. In contrast, central chronologically aged cells are unable to undergo these changes but they maintain higher levels of various stress-defence enzymes. These divergent properties of both cell types determine their consequent dissimilar fate.
- MeSH
- Ammonia metabolism MeSH
- Financing, Organized MeSH
- Adaptation, Physiological MeSH
- Culture Media chemistry MeSH
- Humans MeSH
- Gene Expression Regulation, Fungal MeSH
- Saccharomyces cerevisiae Proteins metabolism MeSH
- Saccharomyces cerevisiae metabolism growth & development MeSH
- Check Tag
- Humans MeSH
- MeSH
- Ammonia metabolism MeSH
- Apoptosis genetics MeSH
- Research Support as Topic MeSH
- Caspases metabolism MeSH
- NADH, NADPH Oxidoreductases metabolism MeSH
- Gene Expression Regulation, Fungal physiology MeSH
- Repressor Proteins genetics MeSH
- Saccharomyces cerevisiae Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae metabolism MeSH
- Signal Transduction physiology MeSH
