Distinctions in adenylate metabolism among organisms inhabiting temperature extremes

Abstract

Microbiota from multiple kingdoms (e.g., Eubacteria, Fungi, Protista) thrive at temperature optima ranging from 0-20 degrees C (psychrophiles) to 40-85 degrees C (thermophiles). In this study, we have monitored changes in adenylate levels and growth rate as a function of temperature in disparate thermally adapted organisms. Our data indicate that growth rate and adenylate levels increase with temperature in mesophilic and thermophilic species, but rapid losses of adenosine 5'-triphosphate (ATP) occur upon cold or heat shock. By contrast, psychrophilic species decrease adenylate levels but increase growth rate as temperatures rise within their viable range. Moreover, psychrophilic ATP levels fell rapidly upon heat shock, but dramatic gains in ATP (approximately 20-50%) were observed upon cold shock, even at sub-zero temperatures. These results suggest that energy metabolism in thermophiles resembles that in mesophiles, but that elevated adenylate nucleotides in psychrophiles may constitute a compensatory strategy for maintaining biochemical processes at low temperature.

Adaptation and Acclimation of Photosynthetic Microorganisms to Permanently Cold Environments

“…Recently, Napolitano and Shain (178,179) have proposed an additional compensatory strategy for maintaining sufficient rates of biochemical reactions at low temperatures in a diverse collection of psychrophilic organisms. These authors found that in mesophilic and thermophilic organisms, levels of ATP and growth rates varied proportionally with respect to growth temperature, that is, at higher growth temperatures, an increase in energy demand (i.e., higher growth rates) coincided with an increase in energy supply (i.e., adenylate pools).…”

“…Light energy is absorbed by the light-harvesting complexes, and excitation energy is transferred to the reaction centers, where it is used to drive charge separation of a chlorophyll pair (P 680 and P 700 for PSII and PSI, respectively). Electrons are transported from PSII to cytochrome b 6 f across the thylakoid membrane by the mobile transporter plastoquinone (PQ/PQH 2 ), and from cytochrome b 6 f to PSI in the lumenal space by the small protein plastocyanin (PC [277]) exhibited an inverse relationship between adenylate levels and growth temperature (178), despite the fact that growth rates (i.e., energy demand) varied proportionally with growth temperature in all the psychrophilic organisms. Thus, it appears that elevated ATP and total adenylate pools may represent an additional adaptive strategy to compensate for lower rates of biochemical reactions at low temperatures.…”

“…It is likely that altered activity of a key enzyme(s) involved in adenylate metabolism, such as F 1 ATPase or AMP phosphatase/deaminase, governs the differences in energy metabolism between the psychrophiles and either the mesophiles or thermophiles. However, biochemical and genetic evidence is currently unavailable to address this hypothesis (178). While the research regarding enzymes from psychrophilic microorganisms has begun to increase in recent years, little attention has been paid to cold-adapted enzymes from phototrophic microorganisms.…”

“…As discussed above, one adaptive explanation for higher adenylate pools in the psychrophiles may be to compensate for reduced rates of molecular diffusion at low temperatures. Thus, higher levels of adenylates could represent an adaptive mechanism to provide adequate energy for ATP-dependent biochemical reactions at low temperatures (178,179).…”

An AMP nucleosidase gene knockout in Escherichia coli elevates intracellular ATP levels and increases cold tolerance

“…(c) ATP levels Bacterial cells were grown to log phase in LB medium at specified temperatures, upon which intracellular ATP levels were quantitated using a luciferin-luciferase ATP assay (Calbiochem), according to the proteinase K (600 U ml K1 ; MO BIO Laboratories, Inc.) extraction method described by Napolitano & Shain (2005), with the exception that 40 ml of releasing reagent were added to each sample (60 ml), followed by the addition of 1 ml of luciferinluciferase mix. Each sample was run in triplicate, and data points indicate the meanGs.e.m.…”