Abstract
Lineages within the species Limosilactobacillus reuteri have specialized to various hosts and their genomes reflect these adaptations. The pdu-cbi-cob-hem gene cluster is conserved in most human and poultry isolates but is infrequent in rodent and porcine isolates. This gene cluster confers the transformation of glycerol into 3-hydroxy-propionaldehyde (reuterin), which can either be secreted and function as precursor of the antimicrobial compound acrolein or serve as an electron acceptor that enhances the organisms’ growth rate. However, it remains unclear which of these two functions is more relevant for L. reuteri evolution and ecology. Here we characterized the effect of glycerol on growth rate and reuterin formation in L. reuteri strains across different phylogenetic lineages during growth on ecologically relevant carbohydrates. We further evaluated the innate reuterin resistance among these strains to infer a possible role of reuterin in the evolution of strains. Results revealed that the poultry/human lineage VI strain, L. reuteri DSM 17938 shows more growth enhancement through glycerol and greater capacity for reuterin production on glucose and maltose as compared to human lineage II strains. Interestingly, reuterin production in lineage II strains was significantly elevated on raffinose and lactose, reaching levels similar to DSM 17938. On all carbohydrates tested, reuterin production occurred during the exponential growth phase and became undetectable during the stationary growth phase. The amount of reuterin produced was sufficient to inhibit E. coli, suggesting that it could be ecologically relevant, but the resistance towards reuterin among L. reuteri strains was highly variable and, for the most part, unrelated to the strain’s capacity for reuterin production. Overall, the findings suggest differences in the substrate-specific regulation of the pdu cluster in L. reuteri lineages that might be reflective of their ecological niches, e.g., chicken foregut versus human infant and adult large intestine. Such information can inform future studies on the ecology of L. reuteri and guide the development of synbiotic applications to improve the therapeutic use of this species.
Highlights
Limosilactobacillus reuteri inhabits the gut of vertebrate animals and has diversified into host specific phylogenetic lineages whose gene content reflects adaptation to their particular hosts (Walter et al, 2011; Duar et al, 2017)
To characterize the functional significance of the pdu cluster in a phylogenetic context, we assessed the acceleration of growth by glycerol in 15 L. reuteri strains across six lineages using the carbohydrate sources glucose, maltose, lactose, and raffinose
The results revealed that the ability to utilize glycerol for enhancing growth rate was strictly dependent on the pdu cluster
Summary
Limosilactobacillus reuteri (formerly Lactobacillus reuteri, Zheng et al, 2020) inhabits the gut of vertebrate animals and has diversified into host specific phylogenetic lineages whose gene content reflects adaptation to their particular hosts (Walter et al, 2011; Duar et al, 2017). The pdu cluster was likely acquired by horizontal gene transfer early in the evolution of L. reuteri (Morita et al, 2008) but appears to have been deleted in most lineages in response to the host environment while being retained in the human and poultry lineages (Frese et al, 2011) This distribution suggests a possible role of the cluster in the host adaptation process of L. reuteri. The evolutionary and ecological role of the pdu cluster has not been elucidated, and it remains unclear which of the two functions (growth enhancement and reuterin formation) determine the relevance of the cluster in this context This question is especially relevant as the pdu cluster constitutes a fitness burden on L. reuteri in the mouse gut in absence of relevant substrates (Cheng et al, 2020)
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