Abstract
Listeria monocytogenes is a Gram-positive, intracellular pathogen responsible for the highly fatal foodborne illness listeriosis. Establishing intracellular infections requires the coordinated expressions of a variety of virulence factors, such as the pore-forming toxin listeriolysin O (LLO), in response to various intra- and extracellular signals. For example, we previously reported that L. monocytogenes differentially modulated LLO production in response to exogenous propionate, a short chain fatty acid either used in salt form as a human food ingredient or produced endogenously by gut microbial fermentation. Therefore, propionate is likely a continuously present signal throughout the L. monocytogenes transmission and infection process. However, little is known about the role of propionate in modulating L. monocytogenes-host interactions. Here we investigated the impact of propionate treatment on L. monocytogenes intracellular infections using cell culture infection models. Propionate treatment was performed separately on L. monocytogenes or host cells before or during infections to better distinguish pathogen-versus-host responses to propionate. Intracellular CFU in RAW264.7 macrophages and plaque diameters in L-fibroblasts were measured as proxy for intracellular infection outcomes. Nitrite levels and cellular morphology were also measured to assess host responses to propionate. We found that propionate pretreatment of anaerobic, but not aerobic, L. monocytogenes significantly enhanced subsequent intracellular infections in both cell types and nitrite production by infected macrophages. Propionate treatment of uninfected macrophages significantly altered cell morphology, seen by longer cells and greater migration, and reduced nitrite concentration in activated macrophages. Treatment of macrophages with propionate prior to or during infections significantly inhibited intracellular growth of L. monocytogenes, including those pre-treated with propionate. These results showcased an opposing effect of propionate on L. monocytogenes intracellular infections and strongly support propionate as an important signaling molecule for both the pathogen and the host cell that can potentially alter the outcome of L. monocytogenes-host interactions.
Highlights
Listeria monocytogenes is a Gram-positive, intracellular pathogen responsible for the foodborne illness listeriosis
While an overall lower level of intracellular CFU was observed in macrophages infected by anaerobically grown L. monocytogenes compared to those infected by aerobically grown L. monocytogenes, overnight propionate pretreatment exhibited no significant effects on bacterial entry and initial survival (Figure 1A)
Propionate pretreatment resulted in a notable but not statistically significant decrease in intracellular growth across three independent experiments (Figure 1B). These results suggest that propionate pretreatment in L. monocytogenes does not affect the initial entry and survival in macrophages but can influence subsequent intracellular growth
Summary
Listeria monocytogenes is a Gram-positive, intracellular pathogen responsible for the foodborne illness listeriosis. While the overall prevalence is low, listeriosis is often associated with a high mortality rate of 20–30%, which results in listeriosis accounting for 19% of all deaths caused by foodborne illnesses (Scallan et al, 2011; de Noordhout et al, 2014). Because of the disease severity, there is a zero-tolerance policy for L. monocytogenes surveillance in food processing facilities or products to minimize exposure and protect high-risk populations (United States Department of Agriculture (USDA), 2014). Listeria monocytogenes is difficult to control as it can grow in conditions typically used to restrict microbial growth. Despite improvements in food safety over the years, multiple L. monocytogenes outbreaks continue to take place every year in the United States [Center for Disease Control and Prevention (CDC), 2020], making additional infection control and prevention strategies a clear priority
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