Molecular Evolution of [NiFe] Hydrogenase-related Energy Conservation Systems

Abstract

 To date, more than 15,000 bacterial and archaeal species have been isolated and characterized. It has become evident from recent biochemical and genomic studies that these microorganisms employ a variety of energy conservation systems to drive thermodynamically unfavorable reactions or harness marginal energy from exergonic reactions in the metabolic pathways required for energy metabolism. For example, a membrane-bound [NiFe] hydrogenase (Mbh) supports critical steps in glycolysis for a hyper-thermophilic archaeon Pyrococcus furiosus: glyceraldehyde 3-phosphate (GAP):ferredoxin (Fd) oxidoreductase and pyruvate:Fd oxidoreductase. However, the molecular evolution of energy conservation systems is still poorly understood. Targets of this study are: [NiFe] hydrogenase-related energy conservation systems including Mbh, energy conserving hydrogenases (Eha, Ehb, and Ech), hydrogenase 3 (Hyc), hydrogenase 4 (Hyf), hydrogen-evolving NADH/quinone-dependent hydrogenases (Hya and Hyb), and bidirectional soluble hydrogenase (Hox). A phylogenetic analysis shows that subunits having a [NiFe] active site of mbh (mbhL), which catalyzes proton reduction, are closely related to subunits of other energy conserving hydrogenases (i.e., ehaO, ehbN, and echE), and are distantly related to other subunits of [NiFe] hydrogenases (i.e., hya and hox) and NADH:ubiquinone oxidoreductase subunit D (nuoD). Combined phylogenetic analysis of hydrogenase-associated proton pomp modules indicates that ancestral Mbh containing mbhL and mbhH may have served as an energy conservation system for primordial metabolism.