Sok2p Transcription Factor Is Involved in Adaptive Program Relevant for Long Term Survival of Saccharomyces cerevisiae Colonies

Váchová, Libuše; Devaux, Frédéric; Kučerová, Helena; Řičicová, Markéta; Jacq, Claude; Palková, Zdena

doi:10.1074/jbc.m404594200

Cited by 40 publications

(47 citation statements)

References 27 publications

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“…On the contrary, these cells are spread throughout the whole colony. sod2⌬ colonies defective in a single metabolic enzyme thus resemble to some extent colonies formed by the strain deficient in the pleiotropic transcription regulator Sok2p (16,17) (Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

“…Determination of Catalase and Superoxide Dismutase Activity-The methods used were described previously (17). In brief, cells from the central and margin regions of 6 -12 colonies were broken in 10 mM MES buffer, pH 6, with Complete, EDTA-free protease inhibitor mixture (Roche Applied Science) and 1 mM 4-(2-aminoethyl)benzenesulfonyl fluoride (Sigma) with glass beads in a FastPrep instrument (QBiogene).…”

Section: Methodsmentioning

confidence: 99%

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Yeast Colony Survival Depends on Metabolic Adaptation and Cell Differentiation Rather Than on Stress Defense

Čáp

Váchová

Palková

2009

Journal of Biological Chemistry

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Enzymes scavenging reactive oxygen species (ROS) are important for cell protection during stress and aging. A deficiency in these enzymes leads to ROS imbalance, causing various disorders in many organisms, including yeast. In contrast to liquid cultures, where fitness of the yeast population depends on its ROS scavenging capability, the present study suggests that Saccharomyces cerevisiae cells growing in colonies capable of ammonia signaling use a broader protective strategy. Instead of maintaining high levels of antioxidant enzymes for ROS detoxification, colonies activate an alternative metabolism that prevents ROS production. Colonies of the strain deficient in cytosolic superoxide dismutase Sod1p thus developed the same way as wild type colonies. They produced comparable levels of ammonia and underwent similar developmental changes (expression of genes of alternative metabolism and center margin differentiation in ROS production, cell death occurrence, and activities of stress defense enzymes) and did not accumulate stress-resistant suppressants. An absence of cytosolic catalase Ctt1p, however, brought colonies developmental problems, which were even more prominent in the absence of mitochondrial Sod2p. sod2⌬ and ctt1⌬ colonies failed in ammonia production and sufficient activation of the alternative metabolism and were incapable of center margin differentiation, but they did not increase ROS levels. These new data indicate that colony disorders are not accompanied by ROS burst but could be a consequence of metabolic defects, which, however, could be elicited by imbalance in ROS produced in early developmental phases. Sod2p and homeostasis of ROS may participate in regulatory events leading to ammonia signaling.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Yeast Colony Survival Depends on Metabolic Adaptation and Cell Differentiation Rather Than on Stress Defense

Čáp

Váchová

Palková

2009

Journal of Biological Chemistry

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“…The Phd1p is implicated in pseudohyphal regulation (32). Sok2p is implicated in sporulation and long-term yeast adaptation (33). Cin5p and Msn4p have a more general stress-sensing role (34).…”

Section: Discussionmentioning

confidence: 99%

Regulation of yeast oscillatory dynamics

Murray

Beckmann

Kitano

2007

Proc. Natl. Acad. Sci. U.S.A.

137

151

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When yeast cells are grown continuously at high cell density, a respiratory oscillation percolates throughout the population. Many essential cellular functions have been shown to be separated temporally during each cycle; however, the regulatory mechanisms involved in oscillatory dynamics remain to be elucidated. Through GC-MS analysis we found that the majority of metabolites show oscillatory dynamics, with 70% of the identified metabolite concentrations peaking in conjunction with NAD(P)H. Through statistical analyses of microarray data, we identified that biosynthetic events have a defined order, and this program is initiated when respiration rates are increasing. We then combined metabolic, transcriptional data and statistical analyses of transcription factor activity, identified the top oscillatory parameters, and filtered a large-scale yeast interaction network according to these parameters. The analyses and controlled experimental perturbation provided evidence that a transcriptional complex formed part of the timing circuit for biosynthetic, reductive, and cell cycle programs in the cell. This circuitry does not act in isolation because both have strong translational, proteomic, and metabolic regulatory mechanisms. Our data lead us to conclude that the regulation of the respiratory oscillation revolves around coupled subgraphs containing large numbers of proteins and metabolites, with a potential to oscillate, and no definable hierarchy, i.e., heterarchical control. metabolic regulation ͉ respiratory oscillation ͉ temporal structure ͉ transcriptional regulation ͉ self-organization A s we obtain a greater understanding of systems dynamics, it is becoming apparent that biological oscillators play critical roles in the organization of physiology in all time scales, ranging from milliseconds to years (1, 2). At the end of yeast growth in batch culture, there is series of cycles in respiratory activity that occur before the culture entering stationary phase (3). When continuous culture is initiated, the culture can be maintained in this oscillatory state [40 min to 5 h; see supporting information (SI) Fig. 5] for months (4-6). These dynamics result in the temporal separation of many essential cellular functions, including redox biochemistry (7,8), transcription (9, 10), energetics (11), chromosome cycle (1), and mitochondrial function (5). Although respiration is always active, the cellular redox state cycles between an oxidative phase and reductive phase. It is known that at least two redox active compounds, acetaldehyde and H 2 S, mediate cell-cell communication (12), but little is known regarding how synchrony is generated within the cell and how the network is regulated.A major problem in elucidating the oscillatory mechanism is the extent to which the cellular network is entrained, i.e., in a system where the majority of parameters oscillate how does one pull out core mechanisms. Fortunately, Saccharomyces cerevisiae has been used extensively as a proving ground for many of the new low-and high-throughpu...

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“…After 10 days of incubation, these colonies begin to cycle through alternating alkali and acid phases. These temporal phases are accompanied by periodic changes in the expression levels for hundreds of genes (40,60). Spatial organization of these colonies occurs at the start of the first alkali phase; at this time, cells in the colony's center begin to undergo apoptosis, while cells at the colony's edge remain viable and continue to divide (35,62).…”

Section: Background (I) the Multifarious Yeast Communitymentioning

confidence: 99%

“…A third cell-cell signal in yeasts is ammonia/ammonium (reviewed in reference 42). For example, S. cerevisiae colonies produce and export ammonium during the alkaline phase (40,60). A mutant (sok2⌬) that is defective in ammonium production is also defective in the subdivision of colonies into apoptotic and viable zones, suggesting that ammonium signals are required for this pattern (62).…”

Section: (Iii) Diffusible Signals Between Cellsmentioning

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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Sok2p Transcription Factor Is Involved in Adaptive Program Relevant for Long Term Survival of Saccharomyces cerevisiae Colonies

Cited by 40 publications

References 27 publications

Yeast Colony Survival Depends on Metabolic Adaptation and Cell Differentiation Rather Than on Stress Defense

Yeast Colony Survival Depends on Metabolic Adaptation and Cell Differentiation Rather Than on Stress Defense

Regulation of yeast oscillatory dynamics

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

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