Abstract
BackgroundOscillation is a special cell behavior in microorganisms during continuous fermentation, which poses threats to the output stability for industrial productions of biofuels and biochemicals. In previous study, a spontaneous oscillatory behavior was observed in Clostridium butyricum-intensive microbial consortium in continuous fermentation for 1,3-propanediol (1,3-PDO) production from glycerol, which led to the discovery of oscillation in species C. butyricum.ResultsSpontaneous oscillations by C. butyricum tended to occur under glycerol-limited conditions at low dilution rates. At a glycerol feed concentration of 88 g/L and a dilution rate of 0.048 h−1, the oscillatory behavior of C. butyricum was observed after continuous operation for 146 h and was sustained for over 450 h with an average oscillation period of 51 h. During oscillations, microbial glycerol metabolism exhibited dramatic periodic changes, in which productions of lactate, formate and hydrogen significantly lagged behind that of other products including biomass, 1,3-PDO and butyrate. Analysis of extracellular oxidation–reduction potential and intracellular ratio of NAD+/NADH indicated that microbial cells experienced distinct redox changes during oscillations, from oxidized to reduced state with decreasing of growth rate. Meanwhile, C. butyricum S3 exhibited periodic morphological changes during oscillations, with aggregates, elongated shape, spores or cell debris at the trough of biomass production. Transcriptome analysis indicated that expression levels of multiple genes were up-regulated when microbial cells were undergoing stress, including that for pyruvate metabolism, conversion of acetyl-CoA to acetaldehyde as well as stress response.ConclusionThis study for the first time systematically investigated the oscillatory behavior of C. butyricum in aspect of occurrence condition, metabolism, morphology and transcriptome. Based on the experimental results, two hypotheses were put forward to explain the oscillatory behavior: disorder of pyruvate metabolism, and excessive accumulation of acetaldehyde.
Highlights
Oscillation is a special cell behavior in microorganisms during continuous fermentation, which poses threats to the output stability for industrial productions of biofuels and biochemicals
This study for the first time systematically investigated the oscillatory behavior of C. butyricum in aspect of occurrence condition, metabolism, morphology and transcriptome
Conditions for oscillation occurrence In the previous study, the oscillatory behavior of C. butyricum-intensive microbial consortium C2-2M tended to occur in continuous fermentation under conditions when the residual glycerol concentrations were low, and no oscillation was observed in continuous fermentation when glycerol supply was sufficient for C. butyricum S3 [19]
Summary
Oscillation is a special cell behavior in microorganisms during continuous fermentation, which poses threats to the output stability for industrial productions of biofuels and biochemicals. Zhou et al Biotechnol Biofuels (2020) 13:191 converted to numerous chemicals such as 1,3-propanediol (1,3-PDO), 1,2-propanediol, ethanol, butanol, citrate and succinate by microbial fermentation [4,5,6]. Among these cases, 1,3-PDO is one of the most valuable products with versatile applications in medicine, cosmetic and textile industry. There are a few types of microorganisms that can directly convert glycerol to 1,3-PDO, including genus Clostridium, Klebsiella, Lactobacillus, Enterobacter and Citrobacter [9]. C. butyricum first converts glycerol to 3-hydroxypropionaldehyde (3-HPA) via glycerol dehydratase (GDHt), followed by formation of 1,3-PDO via 1,3-propanediol oxidoreductase (PDOR) using NADH as the electron donor. The oxidative pathway generates energy (ATP) and reducing power (NADH/NADPH) for microbial biosynthesis and 1,3-PDO production
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