Chemo-organo-autotrophic degradation of aromatic hydrocarbons indicates a new type of bacterial metabolism

Abstract

The sulfate-reducing culture N47 can grow with naphthalene and has a complete tricarboxylic acid cycle (TCA) and Wood-Ljungdahl pathway (WLP) while other organisms have only either of them. Here, we wanted to elucidate why N47 has two complete pathways potentially able to oxidize acetyl-CoA. Enzyme activities were measured in cell extracts indicating a fully functional rTCA and WLP. To elucidate the carbon flux through the pathways, cells were grown with 13 C-labeled naphthalene or 13 C-bicarbonate buffer. Amino acids and fatty acids were analysed for position specific 13 C-incorporation with GC-MS, which indicated that in catabolism, acetyl-CoA from naphthalene was fully oxidized to CO 2 via the WLP. Acetyl-CoA for anabolism of amino acids, fatty acids and carbohydrates was surprisingly not coming from the substrate naphthalene but is generated de novo by CO 2 -fixation, making N47 a chemoorganoauto-trophic microorganism. This indicates that chemoorganoauto-trophy can also occur with complex substrates but probably requires a complete WLP and rTCA in anaerobic microorganisms.