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Corrinoids are cobalt-containing tetrapyrroles. They include adenosylcobalamin (vitamin B 12 ) and cobamides that function as cofactors and coenzymes for methyl transfer, radical-dependent and redox reactions. Though cobamides are the most complex cofactors in nature, they are essential in the acetyl-CoA pathway, thought to be the most ancient CO 2 -fixation pathway, where they perform a pterin-to-cobalt-to-nickel methyl transfer reaction catalyzed by the corrinoid iron-sulphur protein (CoFeS). CoFeS occurs in H 2 -dependent archaeal methanogens, the oldest microbial lineage by measure of physiology and carbon isotope data, dating corrinoids to ca. 3.5 billion years. However, CoFeS and cobamides are also essential in the acetyl-CoA pathway of H 2 -dependent bacterial acetogens. To determine whether corrin biosynthesis was established before archaea and bacteria diverged, whether the pathways arose independently or whether cobamide biosynthesis was transferred from the archaeal to the bacterial lineage (or vice versa) during evolution, we investigated phylogenies and structural data for 26 enzymes of corrin ring and lower ligand biosynthesis. The data trace cobamide synthesis to the common ancestor of bacteria and archaea, placing it in the last universal common ancestor of all lifeforms (LUCA), while pterin-dependent methyl synthesis pathways likely arose independently post-LUCA in the lineages leading to bacteria and archaea. Enzymes of corrin biosynthesis were recruited from preexisting ancient pathways. Evolutionary forerunners of CoFeS function were likely Fe-, Ni- and Co-containing solid-state surfaces, which, in the laboratory, catalyze the reactions of the acetyl-CoA pathway from CO 2 to pyruvate under serpentinizing hydrothermal conditions. The data suggest that enzymatic corrin biosynthesis replaced insoluble solid-state catalysts that tethered primordial CO 2 assimilation to the Earth's crust, suggesting a role for corrin synthesis in the origin of free-living cells., (© 2024 The Author(s). The FEBS Journal published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.)

Oxygen sensing mechanisms are essential for metazoans, their origin and evolution in the context of oxygen in Earth history are of interest. To trace the evolution of a main oxygen sensing mechanism among metazoans, the hypoxia induced factor, HIF, we investigated the phylogenetic distribution and phylogeny of 11 of its components across 566 eukaryote genomes. The HIF based oxygen sensing machinery in eukaryotes can be traced as far back as 800 million years (Ma) ago, likely to the last metazoan common ancestor (LMCA), and arose at a time when the atmospheric oxygen content corresponded roughly to the Pasteur point, or roughly 1% of present atmospheric level (PAL). By the time of the Cambrian explosion (541-485 Ma) as oxygen levels started to approach those of the modern atmosphere, the HIF system with its key components HIF1α, HIF1β, PHD1, PHD4, FIH and VHL was well established across metazoan lineages. HIF1α is more widely distributed and therefore may have evolved earlier than HIF2α and HIF3α, and HIF1β and is more widely distributed than HIF2β in invertebrates. PHD1, PHD4, FIH, and VHL appear in all 13 metazoan phyla. The O 2 consuming enzymes of the pathway, PHDs and FIH, have a lower substrate affinity, K m , for O 2 than terminal oxidases in the mitochondrial respiratory chain, in line with their function as an environmental signal to switch to anaerobic energy metabolic pathways. The ancient HIF system has been conserved and widespread during the period when metazoans evolved and diversified together with O 2 during Earth history., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Song, Modjewski, Kapust, Mizrahi and Martin.)