Histidine betaine trimethylammonia-lyase, a novel enzyme coupled with terminal urocanate reductase in Shewanella woodyi grown anaerobically

Abstract

Bacteria coping with oxygen deficiency can switch to alternative terminal electron acceptors, which can be normal metabolic intermediates or products of dedicated coupled reactions. In the latter case, the genes for the respective terminal reductase and coupling enzyme are expected to cluster in the genome. Here, we determined the roles of two uncharacterized periplasmic proteins encoded by the swoo_3912-swoo_3913 gene cluster in the facultatively anaerobic marine bacterium Shewanella woodyi. We confirmed the current database annotation of the former protein as "urocanate reductase" but identified the latter protein as a previously unknown histidine betaine trimethylammonia-lyase (HBTL) enzyme. HBTL converts histidine betaine into urocanate and trimethylamine and is remarkably specific for histidine betaine as substrate. HBTL requires Mg2+ for activity and undergoes slow reversible inactivation at low Mg2+ concentrations. HBTL activity was not evident in S. woodyi cells grown aerobically but was induced in cells grown anaerobically. Both histidine betaine and urocanate supported anaerobic S. woodyi growth and, hence, respiration. Similar gene clusters are found in many anaerobic bacteria, suggesting a wide occurrence of the anaerobic respiration pathway discovered in this work in the bacterial world.