Impact of bacterial microcompartment-dependent ethanolamine and propanediol metabolism on Listeria monocytogenes interactions with Caco-2 cells

Abstract

Bacterial microcompartment (BMC) dependent ethanolamine (eut) and propanediol utilization (pdu) has recently been shown to stimulate anaerobic growth of Listeria monocytogenes. This metabolic repertoire conceivably contributes to the competitive fitness of L. monocytogenes in the human gastrointestinal (GI) tract, where these compounds become available following phospholipid degradation and mucus-derived rhamnose metabolism by commensal microbiota. Previous transcriptomics and mutant studies of eut and pdu L. monocytogenes suggested a possible role of eut and pdu BMC metabolism in transmission in foods and pathogenicity, but data on a potential role of L. monocytogenes interaction with human cells is currently absent. First, we ask which cellular systems are expressed in the activation of eut and pdu BMC metabolism and the extent to which these systems are conserved between the states. We find common and unique systems related to metabolic shifts, stress and virulence factors. Next, we hypothesize that these common and unique activated cellular systems contribute to a role in the interaction of L. monocytogenes interaction with human cells. We present evidence that metabolically primed L. monocytogenes with active eut and pdu BMCs, as confirmed by metabolic analysis, transmission electron microscopy and proteomics, show significantly enhanced translocation efficacy compared to non-induced cells in a trans-well assay using Caco-2 cells, while adhesion and invasion capacity was similar. Taken together, our results provide insights into the possible key cellular players that drive translocation efficacy upon eut and pdu BMC activation.