[Show abstract][Hide abstract] ABSTRACT: Life on Earth is capable of growing from temperatures well below freezing to above the boiling point of water, with some organisms preferring cooler and others hotter conditions. The growth rate of each organism ultimately depends on its intracellular chemical reactions. Here we show that a thermodynamic model based on a single, rate-limiting, enzyme-catalysed reaction accurately describes population growth rates in 230 diverse strains of unicellular and multicellular organisms. Collectively these represent all three domains of life, ranging from psychrophilic to hyperthermophilic, and including the highest temperature so far observed for growth (122°C). The results provide credible estimates of thermodynamic properties of proteins and obtain, purely from organism intrinsic growth rate data, relationships between parameters previously identified experimentally, thus bridging a gap between biochemistry and whole organism biology. We find that growth rates of both unicellular and multicellular life forms can be described by the same temperature dependence model. The model results provide strong support for a single highly-conserved reaction present in the last universal common ancestor (LUCA). This is remarkable in that it means that the growth rate dependence on temperature of unicellular and multicellular life forms that evolved over geological time spans can be explained by the same model.
[Show abstract][Hide abstract] ABSTRACT: We review early work on the microbial growth curve and the concept of balanced growth followed by commentary on the stringent response and persister cells. There is a voluminous literature on the effect of antibiotics on resistance and persistence and we call for a greater focus in food microbiology on the effect of biocides in the same context. We also raise potential issues in development of resistance arising from “source–sink” dynamics and from horizontal gene transfer. Redox potential is identified as crucial in determining microbial survival or death, and the recently postulated role for reactive oxygen species in signalling also considered.“Traditional” predictive microbiology is revisited with emphasis on temperature dependence. We interpret the temperature vs growth rate curve as comprising 11 regions, some well-recognised but others leading to new insights into physiological responses. In particular we are intrigued by a major disruption in the monotonic rate of inactivation at a temperature, slightly below the actual maximum temperature for growth. This non-intuitive behaviour was earlier reported by other research groups and here we propose that it results from a rapid metabolic switch from the relaxed growth state to the stringent survival state.Finally, we envision the future of predictive microbiology in which models morph from empirical to mechanistic underpinned by microbial physiology and bioinformatics to grow into Systems Biology.
[Show abstract][Hide abstract] ABSTRACT: Domain parameter percent deviation by species. Shown are the maximum and minimum of the strain posterior means for each species, their difference, mid point, and percent deviation.
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] ABSTRACT: Detailed fits for strains 65–80. Shown are the observed growth rate data using symbols and fitted curves for strain 65–80. Observed data are shown as blue squares for strains of Archaea and red diamonds for strains of Eukarya. The fitted curves are calculated using the mean posterior parameter estimates and extend beyond the observed temperature range by ±2.5°.
[Show abstract][Hide abstract] ABSTRACT: Detailed fits for strains 81–95. Shown are the observed growth rate data using symbols and fitted curves for strain 81–95. Observed data are shown as red diamonds. All are strains of Eukarya. The fitted curves are calculated using the mean posterior parameter estimates and extend beyond the observed temperature range by ±2.5°.
[Show abstract][Hide abstract] ABSTRACT: Inferential techniques of numerical classification and principal coordinate analysis have been used to interpret data obtained on the Zn, Cd, and Cu concentration of 48 samples of oysters, comprising 473 individuals, grown at a variety of places around the Tasmanian coastline. A close association was obtained between proximity to heavily urbanized areas and concentration of metals found, oysters growing nearest urban areas having the highest concentrations of one or more of the metals. It appears that areas for commercial oyster growing should be sought in regions far from centers of urbanization and industrialization. Examination of samples of native oysters could be useful in providing an index or measure of environmental pollution.
[Show abstract][Hide abstract] ABSTRACT: D.A. RATKOWSKY, T. ROSS, T.A. WCMEEKIN AND J. OLLEY. 1991. The development of Arrhenius-type (‘Schoolfield’) and Bêlehrádek-type (square root) models that describe microbial growth rates is briefly described. Both types of model have been advocated for use in predictive microbiology. On the basis of published data sets for the growth of bacteria, the consequences of mathematical transformation of data and the use of invalid stochastic assumptions upon model predictions are demonstrated. Mean square error is shown to be an inappropriate criterion by which to compare the performance of predictive models. The data show that bacterial growth responses such as generation time and lag time become more variable as their mean magnitude increases. The practical consequences of such variability for predictive microbiology are discussed.
No preview · Article · Mar 2008 · Journal of Applied Microbiology
[Show abstract][Hide abstract] 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.
No preview · Article · May 2005 · Journal of Theoretical Biology
[Show abstract][Hide abstract] 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°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°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.
[Show abstract][Hide abstract] ABSTRACT: The shelf life of Atlantic salmon (Salmo salar) portions produced for retail distribution is examined and the dominant aerobic spoilage organism is identified. Characterization of the harvesting and processing operations allow the development of a stochastic mathematical model, a process risk model (PRM), which predicts the range of the possible shelf life for the portions under normal retail and distribution. The considered risk is the failure to achieve the nominal 'use by' date. Bacterial counts from surface swabs, water, ice, and fish samples, collected over a period of 9 months, are fitted to distribution functions for use within the model. Comparisons are made between the distributions fitted to the observed bacterial levels and the predicted levels for the slurry water, initial surface contamination on the fish, and for the predicted and observed shelf life. Storage temperature of the packaged salmon portions has the greatest influence on shelf life, with contamination from contact surfaces and other sources being the next most important. The range of bacterial counts on the portions was between -0.6 and 5 log10 cfu/cm2. The model predicts bacterial counts in the slurry water to have an average value of 3.36 log10 cfu/ml, whereas the observed slurry water bacterial counts were 3.35 log10 cfu/ml. The predicted average initial bacterial contamination is 3.31 log10 cfu/cm2 on the fish surface and 3.23 log10 cfu/cm2 on the observed. The average predicted shelf life is 6.5 days, compared to an observed value of 6.2 days at 4 degrees C.
No preview · Article · Mar 2002 · International Journal of Food Microbiology
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] ABSTRACT: Histamine (or scombroid) fish poisoning (HFP) is reviewed in a risk-assessment framework in an attempt to arrive at an informed characterisation of risk. Histamine is the main toxin involved in HFP, but the disease is not uncomplicated histamine poisoning. Although it is generally associated with high levels of histamine (> or =50 mg/100 g) in bacterially contaminated fish of particular species, the pathogenesis of HFP has not been clearly elucidated. Various hypotheses have been put forward to explain why histamine consumed in spoiled fish is more toxic than pure histamine taken orally, but none has proved totally satisfactory. Urocanic acid, like histamine, an imidazole compound derived from histidine in spoiling fish, may be the "missing factor" in HFP. cis-Urocanic acid has recently been recognised as a mast cell degranulator, and endogenous histamine from mast cell degranulation may augment the exogenous histamine consumed in spoiled fish. HFP is a mild disease, but is important in relation to food safety and international trade. Consumers are becoming more demanding, and litigation following food poisoning incidents is becoming more common. Producers, distributors and restaurants are increasingly held liable for the quality of the products they handle and sell. Many countries have set guidelines for maximum permitted levels of histamine in fish. However, histamine concentrations within a spoiled fish are extremely variable, as is the threshold toxic dose. Until the identity, levels and potency of possible potentiators and/or mast-cell-degranulating factors are elucidated, it is difficult to establish regulatory limits for histamine in foods on the basis of potential health hazard. Histidine decarboxylating bacteria produce histamine from free histidine in spoiling fish. Although some are present in the normal microbial flora of live fish, most seem to be derived from post-catching contamination on board fishing vessels, at the processing plant or in the distribution system, or in restaurants or homes. The key to keeping bacterial numbers and histamine levels low is the rapid cooling of fish after catching and the maintenance of adequate refrigeration during handling and storage. Despite the huge expansion in trade in recent years, great progress has been made in ensuring the quality and safety of fish products. This is largely the result of the introduction of international standards of food hygiene and the application of risk analysis and hazard analysis and critical control point (HACCP) principles.
Preview · Article · Jun 2000 · International Journal of Food Microbiology
[Show abstract][Hide abstract] ABSTRACT: The growth rates of four strains of Vibrio parahaemolyticus were measured and compared in a model broth system. The results for the fastest growing strain, based on 77 combinations of temperature and water activity (aw) using NaCl as the humectant, were summarised in the form of a predictive mathematical model. The model, of the square-root type includes a novel term to describe the effects of super-optimal water activity, and can be used to predict generation times for the temperature range (8-45 degrees C) and water activity range (0.936-0.995) which permit growth of Vibrio parahaemolyticus. Predicted generation times from the model were compared to literature data, using bias and accuracy factors, for both laboratory media and foods. The model was shown to give realistic growth estimates, with a bias value of 1.01, and an accuracy factor of 1.38.
Preview · Article · Sep 1997 · International Journal of Food Microbiology
[Show abstract][Hide abstract] ABSTRACT: Because microorganisms are easily dispersed, display physiologic diversity, and tolerate extreme conditions, they are ubiquitous and may contaminate and grow in many food products. The behavior of microbial populations in foods (growth, survival, or death) is determined by the properties of the food (e.g., water activity and pH) and the storage conditions (e.g., temperature, relative humidity, and atmosphere). The effect of these properties can be predicted by mathematical models derived from quantitative studies on microbial populations. Temperature abuse is a major factor contributing to foodborne disease; monitoring temperature history during food processing, distribution, and storage is a simple, effective means to reduce the incidence of food poisoning. Interpretation of temperature profiles by computer programs based on predictive models allows informed decisions on the shelf life and safety of foods. In- or on-package temperature indicators require further development to accurately predict microbial behavior. We suggest a basis for a "universal" temperature indicator. This article emphasizes the need to combine kinetic and probability approaches to modeling and suggests a method to define the bacterial growth/no growth interface. Advances in controlling foodborne pathogens depend on understanding the pathogens' physiologic responses to growth constraints, including constraints conferring increased survival capacity.
Full-text · Article · Jan 1997 · Emerging infectious diseases