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ABSTRACT: Mathematical models exist that quantify the effect of temperature on poikilotherm growth rate. One family of such models assumes a single rate-limiting 'master reaction' using terms describing the temperature-dependent denaturation of the reaction's enzyme. We consider whether such a model can describe growth in each domain of life.
A new model based on this assumption and using a hierarchical Bayesian approach fits simultaneously 95 data sets for temperature-related growth rates of diverse microorganisms from all three domains of life, Bacteria, Archaea and Eukarya. Remarkably, the model produces credible estimates of fundamental thermodynamic parameters describing protein thermal stability predicted over 20 years ago.
The analysis lends support to the concept of universal thermodynamic limits to microbial growth rate dictated by protein thermal stability that in turn govern biological rates. This suggests that the thermal stability of proteins is a unifying property in the evolution and adaptation of life on earth. The fundamental nature of this conclusion has importance for many fields of study including microbiology, protein chemistry, thermal biology, and ecological theory including, for example, the influence of the vast microbial biomass and activity in the biosphere that is poorly described in current climate models.
PLoS ONE 01/2012; 7(2):e32003. · 4.09 Impact Factor
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ABSTRACT: The specific growth rate constant for bacterial growth does not obey the Arrhenius-type kinetics displayed by simple chemical reactions. Instead, for bacteria, steep convex curves are observed on an Arrhenius plot at the low- and high-temperature ends of the biokinetic range, with a region towards the middle of the growth range loosely approximating linearity. This central region has been considered by microbiologists to be the "normal physiological range" for bacterial growth, a concept whose meaningfulness we now question. We employ a kinetic model incorporating thermodynamic terms for temperature-induced enzyme denaturation, central to which is a term to account for the large positive heat capacity change during unfolding of the proteins within the bacteria. It is now widely believed by biophysicists that denaturation of complex proteins and/or other macromolecules is due to hydrophobic hydration of non-polar compounds. Denaturation is seen as the process by which enthalpic and entropic forces becomes imbalanced both at high and at low temperatures resulting in conformational changes in the enzyme structure that expose hydrophobic amino acid groups to the surrounding water molecules. The "thermodynamic" rate model, incorporating the heat capacity change and its effect on the enthalpy and entropy of the system, fitted 35 sets of data for psychrophilic, psychrotrophic, mesophilic and thermophilic bacteria well, resulting in biologically meaningful estimates for the important thermodynamic parameters. As these results mirror those obtained by biophysicists for globular proteins, it appears that the same or a similar mechanism applies to bacteria as applies to proteins.
Journal of Theoretical Biology 05/2005; 233(3):351-62. · 2.21 Impact Factor
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ABSTRACT: The fatty acid composition of Listeria monocytogenes Scott A was determined by close-interval sampling over the entire biokinetic temperature range. There was a high degree of variation in the percentage of branched-chain fatty acids at any given temperature. The percentage of branched C17 components increased with growth temperature in a linear manner. However, the percentages of iso-C15:0 (i15:0) and anteiso-C15:0 (a15:0) were well described by third-order and second-order polynomial curves, respectively. There were specific temperature regions where the proportion of branched-chain fatty acids deviated significantly from the trend established over the entire growth range. In the region from 12 to 13 degrees C there were significant deviations in the percentages of both i15:0 and a15:0 together with a suggested deviation in a17:0, resulting in a significant change in the total branched-chain fatty acids. In the 31 to 33 degrees C region the percentage of total branched-chain components exhibited a significant deviation. The observed perturbations in fatty acid composition occurred near the estimated boundaries of the normal physiological range for growth.
Applied and Environmental Microbiology 07/2002; 68(6):2809-13. · 3.83 Impact Factor
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ABSTRACT: The maximum growth temperature, the optimal growth temperature, and the estimated normal physiological range for growth of Shewanella gelidimarina are functions of water activity (aw), which can be manipulated by changing the concentration of sodium chloride. The growth temperatures at the boundaries of the normal physiological range for growth were characterized by increased variability in fatty acid composition. Under hyper- and hypoosmotic stress conditions at an aw of 0.993 (1.0% [wt/vol] NaCl) and at an aw of 0.977 (4.0% [wt/vol] NaCl) the proportion of certain fatty acids (monounsaturated and branched-chain fatty acids) was highly regulated and was inversely related to the growth rate over the entire temperature range. The physical states of lipids extracted from samples grown at stressful aw values at the boundaries of the normal physiological range exhibited no abrupt gel-liquid phase transitions when the lipids were analyzed as liposomes. Lipid packing and adaptational fatty acid composition responses are clearly influenced by differences in the temperature-salinity regime, which are reflected in overall cell function characteristics, such as the growth rate and the normal physiological range for growth.
Applied and Environmental Microbiology 07/2000; · 3.83 Impact Factor
