Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes

Significance

Before the emergence of oxygenic photosynthesis and the accumulation of oxygen on Earth, life was essentially composed of anaerobic microorganisms. However, very little is known about which metabolisms were present at the time. Anaerobic carbon fixation through the Wood–Ljungdahl pathway is believed to be among the most ancient, and still plays a pivotal role in modern ecosystems. However, its origin and evolutionary history has been disputed. We analysed the distribution and phylogeny of carbon monoxide dehydrogenase/acetyl-CoA synthase, the main enzymatic complex of the pathway in thousands of bacterial and archaeal genomes. We show that this complex was already at work in the last universal common ancestor and has been remarkably conserved in microorganisms over more than 3.5 billion years.

Abstract

Carbon monoxide dehydrogenase/acetyl-CoA synthase (CODH/ACS) is a five-subunit enzyme complex responsible for the carbonyl branch of the Wood–Ljungdahl (WL) pathway, considered one of the most ancient metabolisms for anaerobic carbon fixation, but its origin and evolutionary history have been unclear. While traditionally associated with methanogens and acetogens, the presence of CODH/ACS homologs has been reported in a large number of uncultured anaerobic lineages. Here, we have carried out an exhaustive phylogenomic study of CODH/ACS in over 6,400 archaeal and bacterial genomes. The identification of complete and likely functional CODH/ACS complexes in these genomes significantly expands its distribution in microbial lineages. The CODH/ACS complex displays astounding conservation and vertical inheritance over geological times. Rare intradomain and interdomain transfer events might tie into important functional transitions, including the acquisition of CODH/ACS in some archaeal methanogens not known to fix carbon, the tinkering of the complex in a clade of model bacterial acetogens, or emergence of archaeal–bacterial hybrid complexes. Once these transfers were clearly identified, our results allowed us to infer the presence of a CODH/ACS complex with at least four subunits in the last universal common ancestor (LUCA). Different scenarios on the possible role of ancestral CODH/ACS are discussed. Despite common assumptions, all are equally compatible with an autotrophic, mixotrophic, or heterotrophic LUCA. Functional characterization of CODH/ACS from a larger spectrum of bacterial and archaeal lineages and detailed evolutionary analysis of the WL methyl branch will help resolve this issue.