Abstract
Ni-containing carbon monoxide dehydrogenase (Ni-CODH) plays an important role in the CO/CO2-based carbon and energy metabolism of microbiomes. Ni-CODH is classified into distinct phylogenetic clades, A–G, with possibly distinct cellular roles. However, the types of Ni-CODH clade used by organisms in different microbiomes are unknown. Here, we conducted a metagenomic survey of a protein database to determine the relationship between the phylogeny and biome distribution of Ni-CODHs. Clustering and phylogenetic analyses showed that the metagenome assembly-derived Ni-CODH sequences were distributed in ~ 60% Ni-CODH clusters and in all Ni-CODH clades. We also identified a novel Ni-CODH clade, clade H. Biome mapping on the Ni-CODH phylogenetic tree revealed that Ni-CODHs of almost all the clades were found in natural aquatic environmental and engineered samples, whereas those of specific subclades were found only in host-associated samples. These results are comparable with our finding that the diversity in the phylum-level taxonomy of host-associated Ni-CODH owners is statistically different from those of the other biomes. Our findings suggest that while Ni-CODH is a ubiquitous enzyme produced across diverse microbiomes, its distribution in each clade is biased and mainly affected by the distinct composition of microbiomes.
Highlights
Ni-containing carbon-monoxide dehydrogenase (NiCODH) is a primordial microbial enzyme that catalyzes the reversible conversion between CO2 and CO (CO2 + 2H+ + 2e− ⇔ CO + H2O), a key reaction for carbon fixation and energy conservation (Oelgeschläger and Rother 2008; Sokolova et al 2009; Nitschke and Russell 2013; Can et al 2014; Adam et al 2018; Inoue et al 2019a; Schoelmerich and Müller 2019). CO2 reduction by the NiCODH/CO-methylating acetyl-CoA synthase complex constitutes the carbonyl branch of the Wood–Ljungdahl pathway (WLP) in acetogens and methanogens (Doukov et al 2002; Gong et al 2008; Nitschke and Russell 2013; Can et al 2014; Schuchmann and Müller 2014)
We found the novel phylogenetic clades including the two RefSeq/GenBank sequences, which were previously unidentified since they had been excluded because of differences in the selection criteria. Both the MGnify and RefSeq/GenBank sequences were found in all clades and broadly distributed in the Ni-containing carbon monoxide dehydrogenase (Ni-CODH) phylogeny (Fig. 1A)
Ni-CODH is a key enzyme for energy conservation and carbon fixation with CO, a mysterious but ubiquitous microbial metabolite (Oelgeschläger and Rother 2008; Nitschke and Russell 2013; Robb and Techtmann 2018)
Summary
Ni-containing carbon-monoxide dehydrogenase (NiCODH) is a primordial microbial enzyme that catalyzes the reversible conversion between CO2 and CO (CO2 + 2H+ + 2e− ⇔ CO + H2O), a key reaction for carbon fixation and energy conservation (Oelgeschläger and Rother 2008; Sokolova et al 2009; Nitschke and Russell 2013; Can et al 2014; Adam et al 2018; Inoue et al 2019a; Schoelmerich and Müller 2019). Ni-CODH is a part of the respiratory module via CO oxidation in anaerobic carboxydotrophs, where electrons from CO are transferred to various terminal electron acceptors (e.g., H+, Fe3+, fumarate, sulfur oxides, and nitrogen oxides) via the corresponding respiratory enzymes (Oelgeschläger and Rother 2008; Sokolova et al 2009; Fukuyama et al 2020). Ni-CODH associated with flavin adenine dinucleotide-dependent NAD(P) oxidoreductase (FNOR) and CooF is considered to enable NAD(P)H-mediated CO-driven respiration (Whitham et al 2015; Geelhoed et al 2016; Slobodkin et al 2019)
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