Anaerobic Growth of Listeria monocytogenes on Rhamnose Is Stimulated by Vitamin B12 and Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization

The foodborne pathogen Listeria monocytogenes can form proteina-ceous organelles called bacterial microcompartments (BMCs) that optimize the utili-zation of substrates, such as 1,2-propanediol, and confer an anaerobic growth advantage. Rhamnose is a deoxyhexose sugar abundant in a range of environments, including the human intestine, and can be degraded in anaerobic conditions into 1,2-propanediol, next to acetate and lactate. Rhamnose-derived 1,2-propanediol was found to link with BMCs in some human pathogens such as Salmonella enterica, but the involvement of BMCs in rhamnose metabolism and potential physiological effects on L. monocytogenes are still unknown. In this study, we first test the effect of rham-nose uptake and utilization on anaerobic growth of L. monocytogenes EGDe without or with added vitamin B-12, followed by metabolic analysis. We show that vitamin B-12-de-pendent activation of pdu stimulates metabolism and anaerobic growth of L. monocyto-genes EGDe on rhamnose via 1,2-propanediol degradation into 1-propanol and propio-nate. Transmission electron microscopy of pdu-induced cells shows that BMCs are formed, and additional proteomics experiments confirm expression of pdu BMC shell proteins and enzymes. Finally, we discuss the physiological effects and energy efficiency of L. monocytogenes pdu BMC-driven anaerobic rhamnose metabolism and the impact on competitive fitness in environments such as the human intestine. IMPORTANCE Listeria monocytogenes is a foodborne pathogen causing severe illness and, as such, it is crucial to understand the molecular mechanisms contributing to its survival strategy and pathogenicity. Rhamnose is a deoxyhexose sugar abundant in a range of environments, including the human intestine, and can be degraded in anaero-bic conditions into 1,2-propanediol. In our previous study, the utilization of 1,2-pro-panediol (pdu) in L. monocytogenes was proved to be metabolized in bacterial micro-compartments (BMCs), which are self-assembling subcellular proteinaceous structures and analogs of eukaryotic organelles. Here, we show that the vitamin B-12-dependent activation of pdu stimulates metabolism and anaerobic growth of L. monocytogenes EGDe on rhamnose via BMC-dependent 1,2-propanediol utilization. Combined with metabolic and proteomics analysis, our discussion on the physiological effects and energy efficiency of BMC-driven rhamnose metabolism shed new light to understand the impact on L. monocytogenes competitive fitness in ecosystems such as the human intestine.

Automated summary

Listeria monocytogenes can form bacterial microcompartments (BMCs) for substrate utilization, such as 1,2-propanediol, potentially linked to rhamnose metabolism. This study demonstrates that vitamin B-12-dependent activation of pdu stimulates anaerobic growth of L. monocytogenes on rhamnose via BMC-dependent 1,2-propanediol utilization, highlighting the physiological effects and energy efficiency of this pathway.