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.
Highlights
The foodborne Gram-positive bacterial pathogen Listeria monocytogenes is the cause of the potentially serious disease listeriosis that is characterized by a high fatality rate
No other studies have measured endogenous FabH substrate concentrations, so there is no basis for comparison to determine how well FabH substrate preference in other organisms compares to final fatty acid composition
Fatty acid composition was calculated from FabH substrate preferences and composition, and the differences between this model and the actual fatty acid compositions of L. monocytogenes were compared
Summary
The foodborne Gram-positive bacterial pathogen Listeria monocytogenes is the cause of the potentially serious disease listeriosis that is characterized by a high fatality rate. There has been a multistate outbreak of listeriosis linked to frozen vegetables (http://www.cdc.gov/listeria/outbreaks) that has resulted in an extensive recall of 358 consumer frozen vegetable and fruit products sold under 42 separate brands. Such outbreaks are very expensive, the costs of a 2008 outbreak in Canada being estimated at $242 million Canadian dollars (Thomas et al, 2015). When the bacterium is grown at low temperatures the content of anteiso C15:0 rises markedly through a combination of reduction in fatty acid chain length and branching switching from iso to anteiso fatty acids (Annous et al, 1997; Nichols et al, 2002; Zhu et al, 2005). Anteiso fatty acids, which have a methyl branch on the antepenultimate carbon atom, disrupt the close packing of fatty acyl chains (Willecke and Pardee, 1971; Poger et al, 2014), resulting in increased membrane fluidity (Edgcomb et al, 2000), in what is termed homeoviscous adaptation (Sinensky, 1974)
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