Increased Biomass Production by Mesophilic Food-Associated Bacteria through Lowering the Growth Temperature from 30°C to 10°C

Abstract

Five isolates from chilled food and refrigerator inner surfaces and closely related reference strains of the species Escherichia coli, Listeria monocytogenes, Staphylococcus xylosus, Bacillus cereus, Pedobacter nutrimenti, and Pedobacter panaciterrae were tested for the effect of growth temperature (30°C and 10°C) on biomass formation. Growth was monitored via optical density, and biomass formation was measured at the early stationary phase based on the following parameters in complex and defined media: viable cell count, total cell count, cell dry weight, whole-cell protein content, and cell morphology. According to the lack of growth at 1°C, all strains were assigned to the thermal class of mesophiles. Glucose and ammonium consumption related to cell yield were analyzed in defined media. Except for the protein content, temperature had a significant (t test, P < 0.05) effect on all biomass formation parameters for each strain. The results show a significant difference between the isolates and the related reference strains. Isolates achieved an increase in biomass production between 20% and 110% at the 10°C temperature, which is 15 to 25°C lower than their maximum growth rate temperatures. In contrast, reference strains showed a maximum increase of only about 25%, and some reference strains showed no increase or a decrease of approximately 25%. As expected, growth rates for all strains were higher at 30°C than at 10°C, while biomass production for isolates was higher at 10°C than at 30°C. In contrast, the reference strains showed similar growth yields at the two temperatures. This also demonstrates for mesophilic bacterial strains more efficient nutrient assimilation during growth at low temperatures. Until now, this characteristic was attributed only to psychrophilic microorganisms. IMPORTANCEFor several psychrophilic species, increased biomass formation was described at temperatures lower than optimum growth temperatures, which are defined by the highest growth rate. This work shows increased biomass formation at low growth temperatures for mesophilic isolates. A comparison with closely related reference strains from culture collections showed a significantly smaller increase or no increase in biomass formation. This indicates a loss of specific adaptive mechanisms (e.g., cold adaptation) for mesophiles during long-term cultivation. The increased biomass production for mesophiles under low-temperature conditions opens new avenues for a more efficient biotechnological transformation of nutrients to microbial biomass. These findings may also be important for risk assessment of cooled foods since risk potential is often correlated with the cell numbers present in food samples.T emperature has an obvious influence on the physiological functions and, consequently, on the growth and survival of bacteria (1, 2). Accordingly, bacteria have adapted to the specific temperature ranges of various environments, which can be summarized in different temperature classes.Cold-adapted microorganisms are classified as ps...

Carotenoids are used as regulators for membrane fluidity by Staphylococcus xylosus

“…Two of this major protein folding mechanisms (GroEL/ES and DnaK/J) showed medium to strong reduction of the corresponding genes (Table 3 38 ). This also demonstrates a possible energy saving potential in cell maintenance through more efficient biosynthesis, www.nature.com/scientificreports www.nature.com/scientificreports/ which might also lead to better cell yields at low temperature 39 . Overall we could not observe significant changes in expression of genes involved in menaquinone synthesis 40 .…”

Thermodynamic Control on Biogeography and Functioning of Rare-Biosphere Propionate Syntrophs in Paddy Field Soils

“…With identical quantity of substrate consumption, a longer duration would be expected to produce a greater biomass (yield) [60]. Such a rate-yield tradeoff relationship has been demonstrated in E. coli [61,62] and methanogens [63]. It remains, however, unknown if such a relationship also occurs for propionate syntrophs in paddy soils in situ.…”

Modeling and Exploiting Microbial Temperature Response

“…The simulated optimal specific growth rate (µ opt ) with the maximum turning point at the temperature optimum (T opt ) and growth rate at half of µ opt (µ 50%opt ) are marked in the model of a thermal growth curve. It has been pointed out that the term "optimal temperature" may need further specification to distinguish between the temperature for the optimal growth rate and the optimal temperature of the maximum biomass yield [52]. The minimum and maximum temperatures (T min and T max , respectively) for growth flank the asymmetric function and mark the thermal tolerance or thermal niche of an organism [53,54].…”

“…Hence, the probability function Equation 50is composed of the maximum amount (E L ) by which an active enzyme can lower the activation energy and the probability of the enzyme being correctly folded and active, given by the ratio of ∆G to ∆G max . This transformation yields probability terms for each parameter in Equation 49, as presented in Equations (51) and (52). Therefore, Equation (49) can be rewritten as Equation (53).…”

“…Downshifts in temperature may somewhat be beneficial for a bioprocess, depending on the intended outcome. Seel et al were able to increase biomass yields to optimize nutrient assimilation at suboptimal temperatures (10 • C) for mesophilic isolates from chilled foods and refrigerators in defined medium compared to their reference strains [52]. They emphasized the importance of defining the "optimum temperature".…”