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 degrees C), i.e. above optimal temperature (T-opt). The maximal specific growth rate (mu(max)) of biomass, its concentration and yield on glucose (Y-x/glc) were measured across the whole thermal window (5-40 degrees C) of the yeast in batch anaerobic growth on glucose. Specific rate of glucose consumption, specific rate of glucose consumption for maintenance (m(glc)), true biomass yield on glucose (Y-x/glc(true)), fractional conservation of substrate carbon in product and ATP yield on glucose (Y-atp/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 (similar to 0.83). There were two temperature regions where m(glc) differed 12-fold, which points to the existence of a 'low' (within 5-31 degrees C) and a 'high' (within 33-40 degrees C) metabolic mode regarding maintenance requirements. The rise from the low to high mode occurred at 31-32 degrees C in step-wise manner and it was accompanied with onset of suppression of mu(max). High m(glc) 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 Y-atp/glc revealed that the efficiency of energy metabolism approaches its lower limit at 26-31 degrees C. This limit is reflected in the predetermined combination of Y-x/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 T-opt (e.g. > 31 degrees C) triggers both an increment in m(glc) and suppression of mu(max), which together contribute to an upshift of Y-atp/glc from the lower limit and thus compensate for the loss of the safety margin. This trade-off allows adding 10 more degrees to T-opt and extends the thermal window up to 40 degrees C, sustaining survival and reproduction in supraoptimal temperatures. Deeper understanding of the limits of thermal tolerance can be practically exploited in biotechnological applications. (C) 2015 Elsevier Ltd. All rights reserved.