Metabolic efficiency in yeast Saccharomyces cerevisiae in relation to temperature dependent growth and biomass yield.
Canonized view on temperature effects on growth rate of microorganisms is based on assumption of protein denaturation, which is not confirmed experimentally so far. We develop an alternative concept, which is based on view that limits of thermal tolerance are based on imbalance of cellular energy allocation. Therefore, we investigated growth suppression of yeast Saccharomyces cerevisiae in the supraoptimal temperature range (30-40°C), i.e. above optimal temperature (Topt). The maximal specific growth rate (μmax) of biomass, its concentration and yield on glucose (Yx/glc) were measured across the whole thermal window (5-40°C) of the yeast in batch anaerobic growth on glucose. Specific rate of glucose consumption, specific rate of glucose consumption for maintenance (mglc), true biomass yield on glucose (Yx/glc(true)), fractional conservation of substrate carbon in product and ATP yield on glucose (Yatp/glc) were estimated from the experimental data. There was a negative linear relationship between ATP, ADP and AMP concentrations and specific growth rate at any growth conditions, whilst the energy charge was always high (~0.83). There were two temperature regions where mglc differed 12-fold, which points to the existence of a 'low' (within 5-31°C) and a 'high' (within 33-40°C) metabolic mode regarding maintenance requirements. The rise from the low to high mode occurred at 31-32°C in step-wise manner and it was accompanied with onset of suppression of μmax. High mglc at supraoptimal temperatures indicates a significant reduction of scope for growth, due to high maintenance cost. Analysis of temperature dependencies of product formation efficiency and Yatp/glc revealed that the efficiency of energy metabolism approaches its lower limit at 26-31°C. This limit is reflected in the predetermined combination of Yx/glc(true), elemental biomass composition and degree of reduction of the growth substrate. Approaching the limit implies a reduction of the safety margin of metabolic efficiency. We hypothesize that a temperature increase above Topt (e.g. >31°C) triggers both an increment in mglc and suppression of μmax, which together contribute to an upshift of Yatp/glc from the lower limit and thus compensate for the loss of the safety margin. This trade-off allows adding 10 more degrees to Topt and extends the thermal window up to 40°C, sustaining survival and reproduction in supraoptimal temperatures. Deeper understanding of the limits of thermal tolerance can be practically exploited in biotechnological applications.
Alfred Wegener Institute for Marine and Polar Research (AWI), Bremerhaven, Germany; Institute of Biochemical Engineering (IBVT), University of Stuttgart, Stuttgart, Germany; Institute of Pharmacy and Molecular Biotechnology (IPMB), University of Heidelberg, Germany. Electronic address: maksim.zakhartsev@uni-hohenheim.de.
Maksim
M
Zakhartsev
Institute of Biochemical Engineering (IBVT), University of Stuttgart, Stuttgart, Germany; Beijing Engineering and Technology Research Center of Food Additives, Beijing Technology & Business University, Beijing, China.
Xuelian
X
Yang
Institute of Biochemical Engineering (IBVT), University of Stuttgart, Stuttgart, Germany.
Matthias
M
Reuss
Alfred Wegener Institute for Marine and Polar Research (AWI), Bremerhaven, Germany.
Hans Otto
HO
Pörtner
D000227:Adenine Nucleotides / Q000378:metabolism; D000255:Adenosine Triphosphate / Q000378:metabolism; D000465:Algorithms; D000693:Anaerobiosis; D018533:Biomass; D003365:Costs and Cost Analysis; D004734:Energy Metabolism; D000431:Ethanol / Q000032:analysis / Q000378:metabolism; D005947:Glucose / Q000378:metabolism; D007700:Kinetics; D012441:Saccharomyces cerevisiae / Q000254:growth & development / Q000378:metabolism*; D013696:Temperature
D000227:Adenine Nucleotides; D000431:Ethanol; D000255:Adenosine Triphosphate; D005947:Glucose
ATP yield on substrate; Biomass yield on glucose; Growth rate; Intracellular ATP concentration; Maintenance costs; Product formation efficiency; Temperature