A Pan-Genome Guided Metabolic Network Reconstruction of Five Propionibacterium Species Reveals Extensive Metabolic Diversity

Abstract

Propionibacteria have been studied extensively since the early 1930s due to their relevance to industry and importance as human pathogens. Still, their unique metabolism is far from fully understood. This is partly due to their signature high GC content, which has previously hampered the acquisition of quality sequence data, the accurate annotation of the available genomes, and the functional characterization of genes. The recent completion of the genome sequences for several species has led researchers to reassess the taxonomical classification of the genus Propionibacterium, which has been divided into several new genres. Such data also enable a comparative genomic approach to annotation and provide a new opportunity to revisit our understanding of their metabolism. Using pan-genome analysis combined with the reconstruction of the first high-quality Propionibacterium genome-scale metabolic model and a pan-metabolic model of current and former members of the genus Propionibacterium, we demonstrate that despite sharing unique metabolic traits, these organisms have an unexpected diversity in central carbon metabolism and a hidden layer of metabolic complexity. This combined approach gave us new insights into the evolution of Propionibacterium metabolism and led us to propose a novel, putative ferredoxin-linked energy conservation strategy. The pan-genomic approach highlighted key differences in Propionibacterium metabolism that reflect adaptation to their environment. Results were mathematically captured in genome-scale metabolic reconstructions that can be used to further explore metabolism using metabolic modeling techniques. Overall, the data provide a platform to explore Propionibacterium metabolism and a tool for the rational design of strains.

Effect of Oxygen Contamination on Propionate and Caproate Formation in Anaerobic Fermentation

“…Even though it can express O 2 -sensitive enzymes for fermentative growth similar to those in Clostridium, Acidipropionibacterium also has aerotolerant enzymes with similar functions (Piwowarek et al, 2018;McCubbin et al, 2020). Members of this genus are not only more tolerant to O 2 than clostridia, they have also been found to increase propionate and energy yields when exposed to O 2 (McCubbin et al, 2020).…”

Genome-scale metabolic modelling enables deciphering ethanol metabolism via the acrylate pathway in the propionate-producer Anaerotignum neopropionicum

“…All GEMs of propionigenic bacteria published to date concern strains that harbour the methylmalonyl-CoA pathway. One of these works described the reconstruction of five Propionibacterium freudenreichii species using pan-genome guided metabolic analysis [34]. Navone et.…”

Antibacterial Activity of the Essential Oil From Litsea cubeba Against Cutibacterium acnes and the Investigations of Its Potential Mechanism by Gas Chromatography-Mass Spectrometry Metabolomics

“…In our study, we observed a significant increase in the catalytic activity of HK, and the phenomenon may be caused by the defense response of C. acnes under environmental stress, which can avoid the damage of EO on bacterial metabolism by increasing glucose uptake, according to the literature investigation ( Figures 6C , 7A,B ; Wang et al, 2018 ). Pyruvate is the critical hub of the pathways in carbohydrate and amino acid metabolism, in the Propionibacterium genus, the synthesis of propanoate through the Wood-Werkman cycle is one of the essential pathways of pyruvate metabolism ( McCubbin et al, 2020 ). Pyruvate forms oxaloacetate under pyruvate carboxylase (PC), which starts the first step of the propanoate synthesis.…”

“…Moreover, C. acnes also utilize substrate-level phosphorylation to produce ATP, such as glycolysis and pyruvate to acetate. Although acetate is a by-product of the metabolism, it is vital to C. acnes ( McCubbin et al, 2020 ). Our result suggested that, as a biomarker, the abundance of acetate decreased significantly after EO treatment, indicating that the pathway of pyruvate to acetate was inhibited.…”