The Commensal Anaerobe Veillonella dispar Reprograms Its Lactate Metabolism and Short-Chain Fatty Acid Production during the Stationary Phase.

Abstract

Veillonella spp. are obligate, anaerobic, Gram-negative bacteria found in the human oral cavity and gut. Recent studies have indicated that gut Veillonella promote human homeostasis by producing beneficial metabolites, specifically short-chain fatty acids (SCFAs), by lactate fermentation. The gut lumen is a dynamic environment with fluctuating nutrient levels, so the microbes present shifting growth rates and significant variations of gene expression. The current knowledge of lactate metabolism by Veillonella has focused on log phase growth. However, the gut microbes are mainly in the stationary phase. In this study, we investigated the transcriptomes and major metabolites of Veillonella dispar ATCC 17748T during growth from log to stationary phases with lactate as the main carbon source. Our results revealed that V. dispar reprogrammed its lactate metabolism during the stationary phase. Lactate catabolic activity and propionate production were significantly decreased during the early stationary phase but were partially restored during the stationary phase. The propionate/acetate production ratio was lowered from 1.5 during the log phase to 0.9 during the stationary phase. Pyruvate secretion was also greatly decreased during the stationary phase. Furthermore, we have demonstrated that the gene expression of V. dispar is reprogrammed during growth, as evidenced by the distinct transcriptomes present during the log, early stationary, and stationary phases. In particular, propionate metabolism (the propanediol pathway) was downregulated during the early stationary phase, which explains the decrease in propionate production during the stationary phase. The fluctuations in lactate fermentation during the stationary phase and the associated gene regulation expand our understanding of the metabolism of commensal anaerobes in changing environments. IMPORTANCE Short-chain fatty acids produced by gut commensal bacteria play an important role in human physiology. Gut Veillonella and the metabolites acetate and propionate, produced by lactate fermentation, are associated with human health. Most gut bacteria in humans are in the stationary phase. Lactate metabolism by Veillonella spp. during the stationary phase is poorly understood and was therefore the focus of the study. To this end, we used a commensal anaerobic bacterium and explored its short-chain fatty acid production and gene regulation in order to provide a better understanding of lactate metabolism dynamics during nutrient limitation.