Abstract
Capnophilic lactic fermentation (CLF) is a novel anaplerotic pathway able to convert sugars to lactic acid (LA) and hydrogen using CO2 as carbon enhancer in the hyperthermophilic bacterium Thermotoga neapolitana. In order to give further insights into CLF metabolic networks, we investigated the transcriptional modification induced by CO2 using a RNA-seq approach. Transcriptomic analysis revealed 1601 differentially expressed genes (DEGs) in an enriched CO2 atmosphere over a total of 1938 genes of the T. neapolitana genome. Transcription of PFOR and LDH genes belonging to the CLF pathway was up-regulated by CO2 together with 6-phosphogluconolactonase (6PGL) and 6-phosphogluconate dehydratase (EDD) of the Entner–Doudoroff (ED) pathway. The transcriptomic study also revealed up-regulation of genes coding for the flavin-based enzymes NADH-dependent reduced ferredoxin:NADP oxidoreductase (NFN) and NAD-ferredoxin oxidoreductase (RNF) that control supply of reduced ferredoxin and NADH and allow energy conservation-based sodium translocation through the cell membrane. These results support the hypothesis that CO2 induces rearrangement of the central carbon metabolism together with activation of mechanisms that increase availability of the reducing equivalents that are necessary to sustain CLF. In this view, this study reports a first rationale of the molecular basis of CLF in T. neapolitana and provides a list of target genes for the biotechnological implementation of this process.
Highlights
Thermotoga neapolitana is a hyperthermophilic anaerobic bacterium of the order Thermotogales (Belkin et al, 1986)
We reported that T. neapolitana operates a novel, anaplerotic process named capnophilic lactic fermentation (CLF) for the synthesis of almost enantiopure L-lactic acid
The metabolic process is activated by CO2 and, nominally, is dependent on a Janus pathway including a catabolic branch leading to acetylCoA (AcCoA) from sugars by glycolysis, and an anabolic branch that combines AcCoA and CO2 to give lactic acid (LA) through reduction of newly synthesized pyruvate (PYR) by a NADH-dependent lactic dehydrogenase (LDH) (Figure 1)
Summary
Thermotoga neapolitana is a hyperthermophilic anaerobic bacterium of the order Thermotogales (Belkin et al, 1986). T. neapolitana and other sister species are good candidates for the sustainable and efficient conversion of food and agriculture residues to hydrogen (H2) by Dark Fermentation (Conners et al, 2006; Manish and Banerjee, 2008; Hallenbeck and Ghosh, 2009; Guo et al, 2010; d’Ippolito et al, 2010; Elleuche et al, 2014; Pradhan et al, 2015, 2016a). We reported that T. neapolitana operates a novel, anaplerotic process named capnophilic lactic fermentation (CLF) for the synthesis of almost enantiopure L-lactic acid. Frontiers in Microbiology | www.frontiersin.org d’Ippolito et al. Effects of CO2 in T. neapolitana (LA) without affecting H2 production (Dipasquale et al, 2014; d’Ippolito et al, 2014; Pradhan et al, 2016b, 2019; Nuzzo et al, 2019). The metabolic process is activated by CO2 (capnophilic means “requiring CO2”) and, nominally, is dependent on a Janus pathway including a catabolic branch leading to acetylCoA (AcCoA) from sugars by glycolysis, and an anabolic branch that combines AcCoA and CO2 to give LA through reduction of newly synthesized pyruvate (PYR) by a NADH-dependent lactic dehydrogenase (LDH) (Figure 1)
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