Insights into the Mechanism of Homeoviscous Adaptation to Low Temperature in Branched-Chain Fatty Acid-Containing Bacteria through Modeling FabH Kinetics from the Foodborne Pathogen Listeria monocytogenes

Abstract

The psychrotolerant foodborne pathogen Listeria monocytogenes withstands the stress of low temperatures and can proliferate in refrigerated food. Bacteria adapt to growth at low temperatures by increasing the production of fatty acids that increase membrane fluidity. The mechanism of homeoviscous increases in unsaturated fatty acid amounts in bacteria that predominantly contain straight-chain fatty acids is relatively well understood. By contrast the analogous mechanism in branched-chain fatty acid-containing bacteria, such as L. monocytogenes, is poorly understood. L. monocytogenes grows at low temperatures by altering its membrane composition to increase membrane fluidity, primarily by decreasing the length of fatty acid chains and increasing the anteiso to iso fatty acid ratio. FabH, the initiator of fatty acid biosynthesis, has been identified as the primary determinant of membrane fatty acid composition, but the extent of this effect has not been quantified. In this study, previously determined FabH steady-state parameters and substrate concentrations were used to calculate expected fatty acid compositions at 30°C and 10°C. FabH substrates 2-methylbutyryl-CoA, isobutyryl-CoA, and isovaleryl-CoA produce the primary fatty acids in L. monocytogenes, i.e., anteiso-odd, iso-even, and iso-odd fatty acids, respectively. In vivo concentrations of CoA derivatives were measured, but not all were resolved completely. In this case, estimates were calculated from overall fatty acid composition and FabH steady-state parameters. These relative substrate concentrations were used to calculate the expected fatty acid compositions at 10°C. Our model predicted a higher level of anteiso lipids at 10°C than was observed, indicative of an additional step beyond FabH influencing fatty acid composition at low temperatures. The potential for control of low temperature growth by feeding compounds that result in the production of butyryl-CoA, the precursor of SCFAs that rigidify the membrane and are incompatible with growth at low temperatures, is recognized.

Nutritional change due to climate warming: an analysis of fatty acid content of pasture plants common to Southern Ontario

“…If sterols were stabilizing the membrane as temperature was increased, desaturase activity may not have decreased as would be expected (Ferguson 1975), leading to continued double bond insertion and therefore decreased relative SFA content, increased relative PUFA content, and higher UI values. This may explain why I observed decreased SFA and increased PUFA, contrary to other studies on terrestrial plant lipid dynamics (Tremolieres et al 1982, Behrouzian and Buist 2002, Upchurch 2008, Nozawa 2011, Ernst et al 2016, Saunders et al 2016.…”

Listeria monocytogenes Response to Propionate Is Differentially Modulated by Anaerobicity

“…Propionate supplementations did not alter the anteiso- to iso-branched chain fatty acid ratios under aerobic conditions but raised the ratio in anaerobically grown L. monocytogenes , an observation suggesting that the ability of L. monocytogenes to synthesize specific subtypes of branched chain fatty acids is impacted by propionate under anaerobic but not aerobic conditions. FabH, the enzyme that facilitates the incorporation of acyl-CoA substrates into the fatty acid synthesis pathway, exhibits a selectivity toward branched acyl-CoA over straight acyl-CoA, resulting in a membrane composition enriched with branched chain fatty acids [ 49 ]. Moreover, among different branched acyl-CoA, the preference for the precursors for anteiso-branched chain fatty acids was also enhanced at 10 °C, compared to 30 °C [ 50 ].…”

Adaptive Metabolism in Staphylococci: Survival and Persistence in Environmental and Clinical Settings

“…The staphylococcal CM is also rich in fatty acids (FAs) and lipid content, essential to its adaptive functions in the presence of host defences, antimicrobial challenges, and acclimatization to environmental fluctuations [ 21 ]. FAs particularly help staphylococci prevent temperate-induced impairments in a process referred to as homeoviscous adaptation [ 22 – 24 ]. At optimal temperatures of 37°C, the CM of S. aureus is mainly composed of branched saturated FAs which determine membrane fluidity.…”