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Evolutionary History of Carbon Monoxide Dehydrogenase/Acetyl-Coa Synthase, One of the Oldest Enzymatic Com- Plexes,” by Panagiotis S

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Evolutionary History of Carbon Monoxide Dehydrogenase/Acetyl-Coa Synthase, One of the Oldest Enzymatic Com- Plexes,” by Panagiotis S Correction EVOLUTION Correction for “Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic com- plexes,” by Panagiotis S. Adam, Guillaume Borrel, and Simonetta Gribaldo, which was first published January 22, 2018; 10.1073/ pnas.1716667115 (Proc Natl Acad Sci USA 115:E1166–E1173). The authors wish to note the following: “We would like to clarify that, for reasons of simplicity, we chose to use the term ‘CODH/ACS’ in the main text and Fig. 1 to refer to all enzymes of the carbonyl branch, which form a complex in archaea. In bacteria, ‘CODH/ACS’ refers generally to the AcsA (β)and AcsB (α) tetrameric complex. Also, the term ‘oxidoreductase module’ should be more correctly referred to as ‘oxidoreductase/ synthase module’ because it also catalyzes the synthesis of acetyl- CoA. Fig. 1 has been corrected accordingly. We apologize for any confusion resulting from this oversight.” The corrected Fig. 1 and its corrected legend appear below. E5836–E5837 | PNAS | June 19, 2018 | vol. 115 | no. 25 www.pnas.org Downloaded by guest on September 30, 2021 A B CORRECTION C Fig. 1. (A) The reactions of the WL pathway. In the methyl branch, CO2 is progressively reduced to formyl/formate (-CHO, HCOOH), methenyl (-CH), methylene (-CH2),andeventuallymethyl(-CH3). There are two nonhomologous versions of the methyl branch, each using a different cofactor to which the reduced carbon compounds are bound, tetrahydromethanopterin (H4MPT) or tetrahydrofolate (THF), which are commonly associated with methanogenic Archaea and acetogenic Bacteria, respectively. The carbonyl branch reduces a CO2 molecule to CO (carbonyl moiety), which is combined with the methyl coming from the methyl branch − + and CoA to form acetyl-CoA. Double arrows indicate that both branches are reversible. [H] denotes one reducing equivalent (=1e +1H ). (B) Nomenclature and function of the carbonyl branch proteins. (C) Organization of the carbonyl branch gene cluster in Bacteria and Archaea with indication of homologous proteins. The genes in pink correspond to the homologous accessory proteins CooC and AcsF, which are responsible for nickel insertion. Published under the PNAS license. Published online June 11, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1807540115 PNAS | June 19, 2018 | vol. 115 | no. 25 | E5837 Downloaded by guest on September 30, 2021 Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes Panagiotis S. Adama,b, Guillaume Borrela, and Simonetta Gribaldoa,1 aUnit Evolutionary Biology of the Microbial Cell, Department of Microbiology, Institut Pasteur, 75015 Paris, France; and bUniversité Paris Diderot, Sorbonne Paris Cité, Paris, France Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved December 12, 2017 (received for review September 21, 2017) Carbon monoxide dehydrogenase/acetyl-CoA synthase (CODH/ (α), AcsD (δ), and AcsC (γ). In addition, there exists a subunit ACS) is a five-subunit enzyme complex responsible for the carbonyl exclusive to Archaea called CdhB (e-subunit), and one exclusive branch of the Wood–Ljungdahl (WL) pathway, considered one of to Bacteria (AcsE). For the remainder of this work we shall refer the most ancient metabolisms for anaerobic carbon fixation, but its to components by the names of their archaeal homologs. origin and evolutionary history have been unclear. While tradition- Functional studies have dissected the role of each subunit in the ally associated with methanogens and acetogens, the presence of overall reaction in Bacteria and Archaea. CdhA catalyzes the first CODH/ACS homologs has been reported in a large number of un- step: the reduction of CO2 to CO or the reverse reaction, CO cultured anaerobic lineages. Here, we have carried out an exhaus- oxidationintoCO2. CdhA has a homolog called CooS that per- tive phylogenomic study of CODH/ACS in over 6,400 archaeal and formsthesamereaction,butisnotpartoftheCODH/ACScluster bacterial genomes. The identification of complete and likely (6). In Methanosarcina, the archaeal-specific subunit CdhB has functional CODH/ACS complexes in these genomes significantly beenshowntobindtoCdhAandsuggestedtoprovidethecofactor- expands its distribution in microbial lineages. The CODH/ACS com- binding sites for FAD during FAD-dependent CO oxidation, or plex displays astounding conservation and vertical inheritance FAD/FADH2-mediated activity regulation during autotrophic or over geological times. Rare intradomain and interdomain transfer acetotrophic growth (7). CdhC catalyzes the second step: con- events might tie into important functional transitions, including densation of CO (carbonyl moiety) with a methyl moiety and CoA the acquisition of CODH/ACS in some archaeal methanogens to form acetyl-CoA. CdhD–CdhE form a corrinoid iron–sulfur not known to fix carbon, the tinkering of the complex in a clade complex that provides the methyl for this second step of the of model bacterial acetogens, or emergence of archaeal–bacterial reaction. In Archaea, this complex alone suffices to transfer the hybrid complexes. Once these transfers were clearly identified, methyl moiety bound to H4MPT from the methyl branch to a corrinoid our results allowed us to infer the presence of a CODH/ACS com- cofactor, which is used by CdhC (8). Conversely, in Bacteria the plex with at least four subunits in the last universal common CdhD–CdhE subcomplex contains an extra subunit, AcsE, which ancestor (LUCA). Different scenarios on the possible role of an- catalyzes the transfer of the methyl moiety bound to tetrahydrofolate cestral CODH/ACS are discussed. Despite common assumptions, (THF) (from the methyl branch) to the corrinoid (9). In this work, all are equally compatible with an autotrophic, mixotrophic, or we will refer to CdhABC as the oxidoreductase module and CdhDE/ heterotrophic LUCA. Functional characterization of CODH/ACS AcsE as the methyltransferase module (Fig. 1B). from a larger spectrum of bacterial and archaeal lineages and de- The fact that four CODH/ACS subunits are homologous be- tailed evolutionary analysis of the WL methyl branch will help re- tween Archaea and Bacteria would suggest that this enzyme was solve this issue. present before the divergence between these two domains of life, Wood–Ljungdahl pathway | evolution | methanogens | acetogens | LUCA Significance mong the six carbon fixation pathways encountered in pro- Before the emergence of oxygenic photosynthesis and the ac- – Akaryotes (1), the Wood Ljungdahl (WL) (or reductive cumulation of oxygen on Earth, life was essentially composed acetyl-CoA) pathway has been proposed to be one of the oldest of anaerobic microorganisms. However, very little is known (2). It consists of two branches, the methyl (Eastern) and the about which metabolisms were present at the time. Anaerobic A carbonyl (Western) (3, 4) (Fig. 1 ). In the methyl branch, CO2 is carbon fixation through the Wood–Ljungdahl pathway is be- progressively reduced to methyl (-CH3), whereas in the carbonyl lieved to be among the most ancient, and still plays a pivotal branch, a CO2 molecule is reduced to CO (carbonyl moiety), role in modern ecosystems. However, its origin and evolu- which is combined with the methyl coming from the methyl branch tionary history has been disputed. We analysed the distribu- and CoA to form acetyl-CoA (Fig. 1A). This complex reaction is tion and phylogeny of carbon monoxide dehydrogenase/acetyl- carried out by a single multimeric, bifunctional, and oxygen-sensitive CoA synthase, the main enzymatic complex of the pathway in enzyme complex called carbon monoxide dehydrogenase/acetyl-CoA thousands of bacterial and archaeal genomes. We show that this synthase (CODH/ACS). In addition, CODH/ACS can also function complex was already at work in the last universal common an- in reverse in some bacteria and archaea to carry out acetyl-CoA cestor and has been remarkably conserved in microorganisms degradation to CO2 and tetrahydromethanopterin/tetrahydrofolate over more than 3.5 billion years. (H4MPT/THF)-bound methyl, e.g., from lactate in Archaeoglobus fulgidus (5). Author contributions: S.G. designed research; P.S.A. performed research; P.S.A., G.B., and Five different subunits constitute the CODH/ACS complex, S.G. analyzed data; and P.S.A., G.B., and S.G. wrote the paper. and their coding genes are often found in a cluster (Fig. 1 B and The authors declare no conflict of interest. C). Four of them are homologous between Bacteria and Ar- This article is a PNAS Direct Submission. chaea, but follow a different and somewhat confusing terminol- Published under the PNAS license. ogy. In Archaea, they are called CdhA (α-subunit), CdhC 1To whom correspondence should be addressed. Email: [email protected]. β δ γ ( -subunit), CdhD ( subunit), and CdhE ( subunit), while in This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Bacteria, their respective homologs are called AcsA (β), AcsB 1073/pnas.1716667115/-/DCSupplemental. E1166–E1173 | PNAS | Published online January 22, 2018 www.pnas.org/cgi/doi/10.1073/pnas.1716667115 A PNAS PLUS B C Fig. 1. (A) The reactions of the WL pathway. In the methyl branch, CO2 is progressively reduced to formyl/formate (-CHO, HCOOH), methenyl (-CH), methylene (-CH2), and eventually methyl (-CH3). There are two nonhomologous versions of the methyl branch, each using a different cofactor to which the reduced carbon compounds are bound, tetrahydromethanopterin (H4MPT) or
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