Biome-specific distribution of Ni-containing carbon monoxide dehydrogenases

Inoue, Masao; Omae, Kimiho; Nakamoto, Issei; Kamikawa, Ryoma; Yoshida, Takashi; Sako, Yoshihiko

doi:10.1007/s00792-022-01259-y

Cited by 7 publications

(19 citation statements)

References 67 publications

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“…Genomes having both cooS/cdhA and form I coxL were also explored for available genomes as described in our previous study (19). Briefly, CooS/CdhA was searched using the BLASTp search of DIAMOND v. 0.9.29 (105) against the NCBI non-redundant protein database (February 2,020) using representative sequences from clades A to G of CooS/CdhA and mini-CooS as queries.…”

Section: Methodsmentioning

confidence: 99%

“…An earlier phylogenetic classification of Ni-CODH included six distinct clades: Clade A corresponds to CdhA-type Ni-CODH, while clades B, C, D, E, and F corresponds to CooS-type Ni-CODH (18). A recent categorization based on phylogenetic relationships and the structure of active site motifs identified two additional clades: clade G and clade H (14, 19). Enzymatic activity has only been biochemically or physiologically confirmed for four of the seven Ni-CODH clades, namely Ni-CODHs from clades A (20), C (21), E (22), and F (23).…”

Section: Introductionmentioning

confidence: 99%

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Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Imaura

Okamoto

Hino

et al. 2023

Preprint

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Prokaryotes, known as carbon monoxide (CO) oxidizers, use CO as the carbon or energy source with CO dehydrogenases (CODHs), which are divided into nickel-containing CODH (Ni-CODH) that are sensitive to O2 and molybdenum-containing CODH (Mo-CODH) that are capable of aerobic functioning. The oxygen conditions for CO oxidizers to oxidize CO may be limited because CO oxidizers isolated and characterized so far have either Ni- or Mo-CODH. Here, we report a novel CO oxidizer capable of CO oxidation with both types of CODH based on genomic and physiological characterization of the isolate Parageobacillus sp. G301. This thermophilic facultative anaerobic Bacillota bacterium was isolated from the sediment of a freshwater lake. Genomic analyses showed that G301 was the only isolate possessing both Ni-CODH and Mo-CODH. Genome-based reconstruction of the respiratory machinery and physiological investigation indicated that CO oxidation by Ni-CODH was coupled with H2 production (proton reduction), and CO oxidation by Mo-CODH was coupled with O2 reduction under aerobic conditions and nitrate reduction under anaerobic conditions. G301 would thus be able to thrive via CO oxidation under a wide range of conditions, from aerobic environments to anaerobic environments even without terminal electron acceptors other than protons. As comparative genome analyses revealed no significant differences in genome structures and encoded cellular functions, except for CO oxidation between CO oxidizers and non-CO oxidizers in the genus Parageobacillus, CO oxidation genes would be retained exclusively for CO metabolism and related respiration. Importance Microbial CO oxidation has received a lot of attention because it contributes to global carbon cycling in addition to functioning as a remover of CO, which is toxic to many organisms. Microbial CO oxidizers have a punctate phylogenetic distribution throughout bacteria and archaea, even in genus-level monophyletic groups. In this study, we demonstrated that the new isolate Parageobacillus sp. G301 is capable of both anaerobic (hydrogenogenic) and aerobic CO oxidation, which had not been previously reported. The discovery of this new isolate, which is versatile in CO metabolism, would accelerate research into such CO oxidizers with diverse CO metabolisms, expanding our understanding of microbial diversity. Through comparative genomic analyses, we propose that CO oxidation genes are optional but not essential genetic elements in the genus Parageobacillus, providing insight into a factor that shapes the mosaic phylogenetic distribution of CO oxidizers, even in genus-level monophyletic groups.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Imaura

Okamoto

Hino

et al. 2023

Preprint

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“…The third is FNOR type that has been predicted to be associated with CO utilization in the previous studies (Geelhoed et al 2016;Inoue et al 2019Inoue et al , 2022. FNOR (COG1251) is often present in the CO utilizers and is involved in energy conservation through CO oxidation associated with the reduction of NAD(P) + (Geelhoed et al 2016).…”

Section: Eight Coos Genomic Contexts Were Identified In the Human Gut...mentioning

confidence: 98%

“…The catalytic subunit of Mo-CODH (CoxL) is phylogenetically classified into two groups, form I and II, whereas that of Ni-CODH (CooS and CdhA) is phylogenetically and structurally classified into eight distinct clades, A to H, and mini-CODH (Inoue et al . 2019, 2022).…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic diversity of the carbon monoxide-utilizing prokaryotes and their divergent carbon monoxide metabolisms in the human gut microbiome

Katayama,

Kamikawa,

Yoshida

2023

Preprint

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Although the production of toxic CO within the human body has been detected, only a few CO-utilizing prokaryotes (CO utilizers) have been reported in the human gut, and their phylogenetic and physiological diversity remains unclear. Here, we unveiled more than thousand representative genomes originating from previously unexplored potential CO-utilizing prokaryotes, which contain CO dehydrogenase (CODH) genes. More than half of CODH-bearing prokaryotes possess genes for the autotrophic Wood-Ljungdahl pathway (WLP). However, 95% of these prokaryotes commonly lack a key gene for WLP, which encodes enzyme that synthesizes formate from CO2 and H2, suggesting that they share a degenerated WLP. Instead, many were predicted to possess an alternative way of synthesizing formate from pyruvate, which is a product of glycolysis. This suggests that glycolysis may serve as a potential supplier of carbon and reducing power to degenerate WLP, which may no longer function as a complete autotrophic pathway. In addition to degenerated WLP, one of the seven predicted CO metabolic pathways involves CO oxidation, which is linked to nitrate reduction and oxaloacetate synthesis. Our findings reveal the unique and diverse nature of CO metabolism in the human gut microbiome, suggesting its potential contribution to CO consumption and gut homeostasis.

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“…( 15 ) successfully mined the protein database in search of novel polyethylene terephthalate (PET) hydrolases using sequence homology to a known PETase; (iii) Inoue et al. ( 16 ) used the sequence set to determine the relationship between specific clades of metabolically important Ni-containing carbon monoxide dehydrogenases (Ni-CODHs) and their biome distribution and (iv) Kazlauskas et al. ( 17 ) utilised the protein database in their analysis of the diversity and evolution of B-family DNA polymerases.…”

Section: Introductionmentioning

confidence: 99%

MGnify: the microbiome sequence data analysis resource in 2023

Richardson

Allen

Baldi

et al. 2022

Nucleic Acids Research

137

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The MGnify platform (https://www.ebi.ac.uk/metagenomics) facilitates the assembly, analysis and archiving of microbiome-derived nucleic acid sequences. The platform provides access to taxonomic assignments and functional annotations for nearly half a million analyses covering metabarcoding, metatranscriptomic, and metagenomic datasets, which are derived from a wide range of different environments. Over the past 3 years, MGnify has not only grown in terms of the number of datasets contained but also increased the breadth of analyses provided, such as the analysis of long-read sequences. The MGnify protein database now exceeds 2.4 billion non-redundant sequences predicted from metagenomic assemblies. This collection is now organised into a relational database making it possible to understand the genomic context of the protein through navigation back to the source assembly and sample metadata, marking a major improvement. To extend beyond the functional annotations already provided in MGnify, we have applied deep learning-based annotation methods. The technology underlying MGnify's Application Programming Interface (API) and website has been upgraded, and we have enabled the ability to perform downstream analysis of the MGnify data through the introduction of a coupled Jupyter Lab environment.

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Biome-specific distribution of Ni-containing carbon monoxide dehydrogenases

Cited by 7 publications

References 67 publications

Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Phylogenetic diversity of the carbon monoxide-utilizing prokaryotes and their divergent carbon monoxide metabolisms in the human gut microbiome

MGnify: the microbiome sequence data analysis resource in 2023

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