Proteome Adaptation of <i>Saccharomyces cerevisiae</i> to Severe Calorie Restriction in Retentostat Cultures

Binai, Nadine A.; Bisschops, Markus M.M.; Breukelen, Bas van; Mohammed, Shabaz; Loeff, Luuk; Pronk, Jack T.; Heck, Albert J. R.; Daran‐Lapujade, Pascale; Slijper, Monique

doi:10.1021/pr5003388

Cited by 17 publications

(31 citation statements)

References 72 publications

(147 reference statements)

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“…We have also recently shown that a gradual decrease of the specific growth rate to near-zero values in glucose-limited retentostats 50 yielded yeast cells with a thermotolerance that is as high as that of aerobic SP cultures (Figure 5), and with an even longer CLS during subsequent starvation 20. The transcriptional reprogramming observed in these anaerobic severely calorie-restricted cultures 51 strongly resembled the transcriptome changes observed in the present study for aerobic cultures entering SP and proteome analysis showed increased levels of proteins involved in stress resistance 52. Deletion of Rim15, a kinase under control of several nutrient signaling pathways 53, strongly reduced the acquisition of robustness in both anaerobic and aerobic calorie-restricted cultures 5455, suggesting a strong role for nutrient signaling independent of oxygen availability.…”

Section: Discussionsupporting

confidence: 72%

Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae

Bisschops¹,

Vos²,

Martínez-Moreno

et al. 2015

MIC

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Stationary-phase (SP) batch cultures of Saccharomyces cerevisiae, in which growth has been arrested by carbon-source depletion, are widely applied to study chronological lifespan, quiescence and SP-associated robustness. Based on this type of experiments, typically performed under aerobic conditions, several roles of oxygen in aging have been proposed. However, SP in anaerobic yeast cultures has not been investigated in detail. Here, we use the unique capability of S. cerevisiae to grow in the complete absence of oxygen to directly compare SP in aerobic and anaerobic bioreactor cultures. This comparison revealed strong positive effects of oxygen availability on adenylate energy charge, longevity and thermotolerance during SP. A low thermotolerance of anaerobic batch cultures was already evident during the exponential growth phase and, in contrast to the situation in aerobic cultures, was not substantially increased during transition into SP. A combination of physiological and transcriptome analysis showed that the slow post-diauxic growth phase on ethanol, which precedes SP in aerobic, but not in anaerobic cultures, endowed cells with the time and resources needed for inducing longevity and thermotolerance. When combined with literature data on acquisition of longevity and thermotolerance in retentostat cultures, the present study indicates that the fast transition from glucose excess to SP in anaerobic cultures precludes acquisition of longevity and thermotolerance. Moreover, this study demonstrates the importance of a preceding, calorie-restricted conditioning phase in the acquisition of longevity and stress tolerance in SP yeast cultures, irrespective of oxygen availability.

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Section: Discussionsupporting

confidence: 72%

Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae

Bisschops¹,

Vos²,

Martínez-Moreno

et al. 2015

MIC

Self Cite

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“…This transcriptional reprogramming could not be attributed solely to the alleviation of glucose repression (4,71) and, therefore, probably reflects a preparation for environmental changes. In general, many yeast genes that were previously shown to be characteristic for quiescent cells (22), i.e., postmitotic cells, were gradually upregulated during retentostat cultivation, suggesting a growth rate-dependent expression of these genes rather than an on-off switch of quiescence upon cessation of growth.…”

Section: Microbe-specific Transcriptional Responses At (Near-)zero Grmentioning

confidence: 92%

“…In anaerobic S. cerevisiae retentostat cultures, many genes involved in mitochondrial functions, including respiration, were upregulated at both the transcript and protein level, despite the absence of oxygen (4,71). This transcriptional reprogramming could not be attributed solely to the alleviation of glucose repression (4,71) and, therefore, probably reflects a preparation for environmental changes.…”

Section: Microbe-specific Transcriptional Responses At (Near-)zero Grmentioning

confidence: 96%

Physiological and Transcriptional Responses of Different Industrial Microbes at Near-Zero Specific Growth Rates

Ercan

Bisschops

Overkamp

et al. 2015

Appl Environ Microbiol

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The current knowledge of the physiology and gene expression of industrially relevant microorganisms is largely based on laboratory studies under conditions of rapid growth and high metabolic activity. However, in natural ecosystems and industrial processes, microbes frequently encounter severe calorie restriction. As a consequence, microbial growth rates in such settings can be extremely slow and even approach zero. Furthermore, uncoupling microbial growth from product formation, while cellular integrity and activity are maintained, offers perspectives that are economically highly interesting. Retentostat cultures have been employed to investigate microbial physiology at (near-)zero growth rates. This minireview compares information from recent physiological and gene expression studies on retentostat cultures of the industrially relevant microorganisms Lactobacillus plantarum, Lactococcus lactis, Bacillus subtilis, Saccharomyces cerevisiae, and Aspergillus niger. Shared responses of these organisms to (near-)zero growth rates include increased stress tolerance and a downregulation of genes involved in protein synthesis. Other adaptations, such as changes in morphology and (secondary) metabolite production, were species specific. This comparison underlines the industrial and scientific significance of further research on microbial (near-)zero growth physiology. Most research in microbial physiology focuses on growing cells, although under natural and industrial conditions, microbes frequently encounter a state in which neither growth nor deterioration of cells occurs. However, the experimental design to study microbes in this clearly relevant physiological state is far from trivial.In this minireview, we define zero growth as a nongrowing state in which the viability and metabolic activity of a microbial culture are maintained for prolonged periods. As such, zero growth differs from starvation, which is coupled to cellular deterioration, loss of activity, and ultimately, cell death (1, 2). Zero growth also differs from differentiated survival states, such as bacterial or fungal spores, in which metabolism comes to a standstill (3). Conversely, under zero-growth conditions, microbes exclusively use available substrates for processes that contribute to maintenance of cellular integrity and homeostasis (4-7). Such processes include homeostasis of transmembrane gradients of protons and solutes, defense and repair systems, osmoregulation, and protein turnover (8, 9).In classical food fermentation processes, (near-)zero growth occurs during prolonged periods of extremely restricted availability of energy substrates. Examples include cheese ripening by lactic acid bacteria (LAB) (10-12), wine fermentation by Saccharomyces cerevisiae (13,14), and natto fermentation by Bacillus subtilis (15). Despite the severely energy-limiting conditions, microbes manage to survive in these processes for many weeks, while continuing to produce aroma and flavor compounds in the product matrix (10,13,15,16). Another incentive for studying...

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“…In general, there is a large degree of conservation of age‐associated changes across different eukaryotic species . To investigate whether NPCs change in similar ways in aging cells and tissues from different species, we extracted data on the abundance of Nups from six published proteome datasets, derived from aging budding yeast , rat , and mouse . The studies using baker's yeast addressed proteome changes that occur during aging in nondividing cells, chronological aging (Fig.…”

Section: On the Search For Common Age‐related Changes In Npcs Of Diffmentioning

confidence: 99%

“…The studies using baker's yeast addressed proteome changes that occur during aging in nondividing cells, chronological aging (Fig. 2A) , and in dividing cells, replicative aging (Fig. 2B) .…”

Section: On the Search For Common Age‐related Changes In Npcs Of Diffmentioning

confidence: 99%

Poor old pores—The challenge of making and maintaining nuclear pore complexes in aging

2020

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The nuclear pore complex (NPC) is the sole gateway to the nuclear interior, and its function is essential to all eukaryotic life. Controlling the functionality of NPCs is a tremendous challenge for cells. Firstly, NPCs are large structures, and their complex assembly does occasionally go awry. Secondly, once assembled, some components of the NPC persist for an extremely long time and, as a result, are susceptible to accumulate damage. Lastly, a significant proportion of the NPC is composed of intrinsically disordered proteins that are prone to aggregation. In this review, we summarize how the quality of NPCs is guarded in young cells and discuss the current knowledge on the fate of NPCs during normal aging in different tissues and organisms. We discuss the extent to which current data supports a hypothesis that NPCs are poorly maintained during aging of nondividing cells, while in dividing cells the main challenge is related to the assembly of new NPCs. Our survey of current knowledge points toward NPC quality control as an important node in aging of both dividing and nondividing cells. Here, the loss of protein homeostasis during aging is central and the NPC appears to both be impacted by, and to drive, this process.

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Proteome Adaptation of Saccharomyces cerevisiae to Severe Calorie Restriction in Retentostat Cultures

Cited by 17 publications

References 72 publications

Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae

Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae

Physiological and Transcriptional Responses of Different Industrial Microbes at Near-Zero Specific Growth Rates

Poor old pores—The challenge of making and maintaining nuclear pore complexes in aging

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