Abstract
Bacterial microcompartments (BMCs) are proteinaceous organelles that optimize specific metabolic pathways referred to as metabolosomes involving transient production of toxic volatile metabolites such as aldehydes. Previous bioinformatics analysis predicted the presence of BMCs in 23 bacterial phyla including foodborne pathogens and a link with gene clusters for the utilization of host-derived substrates such as 1,2-propanediol utilization, i.e., the Pdu cluster. Although, transcriptional regulation of the Pdu cluster and its role in Listeria monocytogenes virulence in animal models have recently been reported, the experimental identification and the physiological role of BMCs in L. monocytogenes is still unexplored. Here, we ask whether BMCs could enable utilization of 1,2-propanediol (Pd) in L. monocytogenes under anaerobic conditions. Using L. monocytogenes EGDe as a model strain, we could demonstrate efficient utilization of Pd with concomitant production of 1-propanol and propionate after 24 h of anaerobic growth, while the utilization was significantly reduced in aerobic conditions. In line with this, expression of genes encoding predicted shell proteins and the signature enzyme propanediol dehydratase is upregulated more than 20-fold in cells anaerobically grown in Pdu-induced versus non-induced control conditions. Additional proteomics analysis confirmed the presence of BMC shell proteins and Pdu enzymes in cells that show active degradation of Pd. Furthermore, using transmission electron microscopy, BMC structures have been detected in these cells linking gene expression, protein composition, and BMCs to activation of the Pdu cluster in anaerobic growth of L. monocytogenes. Studies in defined minimal medium with Pd as an energy source showed a significant increase in cell numbers, indicating that Pdu and the predicted generation of ATP in the conversion of propionyl-phosphate to the end product propionate can support anaerobic growth of L. monocytogenes. Our findings may suggest a role for BMC-dependent utilization of Pd in L. monocytogenes growth, transmission, and interaction with the human host.
Highlights
Cellular organelles play crucial roles in establishing physical boundaries for biological processes (Yates et al, 2005)
A whole genome search of Pf00936 and Pf03319 domains revealed that the propanediol utilization (Pdu) cluster in L. monocytogenes EGDe contains seven genes encoding for Bacterial microcompartments (BMCs) shell proteins, PduTUABKJN (Figure 1A)
The genome similarity heat map illustrates the evolutionary dynamics of the Pdu cluster and reveals that except for the loss of pduJ in L. marthii FSL S4-120, the Pdu cluster is highly conserved in Listeria sensu stricto species but absent in Listeria sensu lato species, in line with previous studies of Listeria sensu stricto and Listeria sensu lato species (Chiara et al, 2015; Schardt et al, 2017)
Summary
Cellular organelles play crucial roles in establishing physical boundaries for biological processes (Yates et al, 2005). The BMCs that have been characterized and that participate in the heterotrophic metabolism via short-chain aldehydes are collectively termed metabolosomes (Aussignargues et al, 2015; Kerfeld and Erbilgin, 2015; Sutter et al, 2017; Kerfeld et al, 2018) These BMCs share a common encapsulated chemistry driven by three core enzymes: aldehyde dehydrogenase, alcohol dehydrogenase, and phosphotransacylase, and their functions have been studied mostly in Gammaproteobacteria including BMCs for the utilization of Pd and ethanolamine in Salmonella enterica and Escherichia coli and for choline metabolism in Desulfovibrio desulfuricans (Bobik et al, 1999; Garsin, 2010; Craciun and Balskus, 2012; Kerfeld et al, 2018).
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