Listeria monocytogenes Response to Propionate Is Differentially Modulated by Anaerobicity

Abstract

Propionate is a common food preservative and one of the major fermentation acids in the intestines. Therefore, exposure to propionate is frequent for foodborne pathogens and likely takes place under suboxic conditions. However, it is not clear whether the absence of oxygen affects how pathogens respond to propionate. Here, we investigated how propionate exposure affects Listeria monocytogenes growth and virulence factor production under aerobic or anaerobic conditions and showed that oxygen indeed plays a key role in modulating L. monocytogenes response to propionate. Under aerobic conditions, propionate supplementations had no effect on planktonic growth but resulted in decreased adherent growth. Under anaerobic conditions, propionate supplementations resulted in a pH-dependent inhibition of planktonic growth and increased adherent growth. Cultures grown with propionate accumulated higher levels of acetoin under aerobic conditions but lower levels of ethanol under both aerobic and anaerobic conditions. Metabolic perturbations by propionate were also evident by the increase in straight chain fatty acids. Finally, propionate supplementations resulted in increased listeriolyin O (LLO) production under anaerobic conditions but decreased LLO production under aerobic conditions. These results demonstrate for the first time that the presence or absence of oxygen plays a critical role in shaping L. monocytogenes responses to propionate.

The Production of Listeriolysin O and Subsequent Intracellular Infections by Listeria monocytogenes Are Regulated by Exogenous Short Chain Fatty Acid Mixtures

“…Both propionate and butyrate, separately, have been demonstrated to decrease the abundance of branched chain fatty acids (BCFAs) and increase the abundance of straight chain fatty acids in L. monocytogenes [8,9]. Here we investigated how the membrane fatty acid composition was affected by supplementation of SCFAs in mixtures and whether there was an oxygen-dependent alteration of fatty acid composition in response to SCFA exposure.…”

“…In a subsequent study investigating the effects of propionate on L. monocytogenes under aerobic as well as anaerobic conditions identified that the production of LLO was highly sensitive to regulation by exogenous propionate [9]. More specifically, while aerobic propionate exposure resulted in a dose-dependent decrease in LLO production, anaerobic propionate exposure resulted in a dose-dependent increase in LLO production [9].…”

“…For example, transcription of the hly gene, which encodes listeriolysin O (LLO)-a cholesterol-dependent pore forming toxin that facilitates L. monocytogenes entry into the host cell cytosol [3], is responsive to a multitude of environmental factors, ranging from salt concentrations [4], growth temperature [5], to culture pH [5,6]. We have also shown that anaerobic conditions and propionate, two important environmental signals present in the intestinal lumen, can impact LLO production [7][8][9].…”

“…In a subsequent study investigating the effects of propionate on L. monocytogenes under aerobic as well as anaerobic conditions identified that the production of LLO was highly sensitive to regulation by exogenous propionate [9]. More specifically, while aerobic propionate exposure resulted in a dose-dependent decrease in LLO production, anaerobic propionate exposure resulted in a dose-dependent increase in LLO production [9]. Given that overall BCFA levels were also decreased in propionate-treated L. monocytogenes under aerobic as well as anaerobic conditions [9], it is clear that the general loss of BCFAs upon propionate or butyrate exposure is not the only mechanism mediating the regulation of LLO production.…”

“…More specifically, while aerobic propionate exposure resulted in a dose-dependent decrease in LLO production, anaerobic propionate exposure resulted in a dose-dependent increase in LLO production [9]. Given that overall BCFA levels were also decreased in propionate-treated L. monocytogenes under aerobic as well as anaerobic conditions [9], it is clear that the general loss of BCFAs upon propionate or butyrate exposure is not the only mechanism mediating the regulation of LLO production. Moreover, these results highlight a potential opposing effect of individual SCFAs on LLO production and justify a need to consider the effects of SCFAs on L. monocytogenes as mixtures in addition to individual components to identify potential interactions.…”