On the evolution of cytochrome oxidases consuming oxygen

Esposti, Mauro Degli

doi:10.1016/j.bbabio.2020.148304

Cited by 17 publications

(34 citation statements)

References 62 publications

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“…The latter analysis is focused on family A oxidases since the phylogenetic distribution of family B oxidases, which also have heme A, is rather patchy among bacteria. Indeed, it is possible that family B derived from some ancestral family A oxidase (Degli Esposti, 2020). Combined with other findings, our results suggest that family A COX has evolved in ancestors of extant acidophilic iron-oxidizing bacteria.…”

Section: Introductionsupporting

confidence: 79%

“…A common class of terminal oxidases is heme A-containing proton pumping cytochrome oxidase (COX), which has a relatively low affinity for oxygen ( Han et al, 2011 ; Degli Esposti et al, 2019 ) and consequently must have evolved during or after the Great Oxygenation Event (GOE), which produced stable levels of oxygen on earth ( Konhauser et al, 2011 ). COX of the family A of Heme Copper Oxygen Reductases (HCO) is widespread in all kingdoms of life ( Castresana and Saraste, 1995 ; Pereira et al, 2001 ; Han et al, 2011 ; Degli Esposti, 2020 ) due to extensive Lateral Gene Transfer (LGT) ( Nelson-Sathi et al, 2015 ; Soo et al, 2017 ). Subsequently bacterial COX became the cytochrome c oxidase of mitochondrial organelles.…”

Section: Introductionmentioning

confidence: 99%

“…COX2 contains two copper atoms in a binuclear center, Cu A ( Figure 1A ). The redox reaction of molecular oxygen reduction at the heme a 3 -Cu B center is coupled to the generation of an electrochemical gradient via conserved proton-conducting channels ( Pereira et al, 2001 ; Ferguson and Ingledew, 2008 ; Han et al, 2011 ; Sharma and Wikström, 2014 ; Degli Esposti, 2020 ). This gradient drives ATP synthesis and various other energy-demanding functions in the cell.…”

Section: Introductionmentioning

confidence: 99%

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Respiratory Heme A-Containing Oxidases Originated in the Ancestors of Iron-Oxidizing Bacteria

et al. 2021

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Respiration is a major trait shaping the biology of many environments. Cytochrome oxidase containing heme A (COX) is a common terminal oxidase in aerobic bacteria and is the only one in mammalian mitochondria. The synthesis of heme A is catalyzed by heme A synthase (CtaA/Cox15), an enzyme that most likely coevolved with COX. The evolutionary origin of COX in bacteria has remained unknown. Using extensive sequence and phylogenetic analysis, we show that the ancestral type of heme A synthases is present in iron-oxidizing Proteobacteria such as Acidithiobacillus spp. These bacteria also contain a deep branching form of the major COX subunit (COX1) and an ancestral variant of CtaG, a protein that is specifically required for COX biogenesis. Our work thus suggests that the ancestors of extant iron-oxidizers were the first to evolve COX. Consistent with this conclusion, acidophilic iron-oxidizing prokaryotes lived on emerged land around the time for which there is the earliest geochemical evidence of aerobic respiration on earth. Hence, ecological niches of iron oxidation have apparently promoted the evolution of aerobic respiration.

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Section: Introductionsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Respiratory Heme A-Containing Oxidases Originated in the Ancestors of Iron-Oxidizing Bacteria

et al. 2021

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“…5B). The presence of the gene for CtaA is unusual, since it is not observed in the gene cluster of cytochrome bo 3 ubiquinol oxidases of other bacteria, which often terminate with a CtaB homolog called CyoE [5]. Considering that A2type aa 3 cytochrome c oxidases (COX) are not present in the genomes of extant sulfur-oxidizing acidithiobacilli, we surmise that such bacteria possess an "A1-type" aa 3 ubiquinol oxidase, as supported by biochemical and spectral evidence reported previously [90].…”

Section: Other Terminal Oxidasesmentioning

confidence: 99%

“…ref. [5]). A similar presence of vestigial cysteines has been previously documented for the NuoD subunit in complex I, which in some bacteria retain vestigial Cys ligands of the Ni-Fe cofactor of their hydrogenase ancestors [87].…”

Section: Other Terminal Oxidasesmentioning

confidence: 99%

Genomic evolution of the class Acidithiobacillia: deep-branching Proteobacteria living in extreme acidic conditions

et al. 2021

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Members of the genus Acidithiobacillus, now ranked within the class Acidithiobacillia, are model bacteria for the study of chemolithotrophic energy conversion under extreme conditions. Knowledge of the genomic and taxonomic diversity of Acidithiobacillia is still limited. Here, we present a systematic analysis of nearly 100 genomes from the class sampled from a wide range of habitats. Some of these genomes are new and others have been reclassified on the basis of advanced genomic analysis, thus defining 19 Acidithiobacillia lineages ranking at different taxonomic levels. This work provides the most comprehensive classification and pangenomic analysis of this deep-branching class of Proteobacteria to date. The phylogenomic framework obtained illuminates not only the evolutionary past of this lineage, but also the molecular evolution of relevant aerobic respiratory proteins, namely the cytochrome bo3 ubiquinol oxidases.

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The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third

Mrnjavac,

Nagies,

Wimmer

et al. 2024

FEBS Letters

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Molecular oxygen is a stable diradical. All O2‐dependent enzymes employ a radical mechanism. Generated by cyanobacteria, O2 started accumulating on Earth 2.4 billion years ago. Its evolutionary impact is traditionally sought in respiration and energy yield. We mapped 365 O2‐dependent enzymatic reactions of prokaryotes to phylogenies for the corresponding 792 protein families. The main physiological adaptations imparted by O2‐dependent enzymes were not energy conservation, but novel organic substrate oxidations and O2‐dependent, hence O2‐tolerant, alternative pathways for O2‐inhibited reactions. Oxygen‐dependent enzymes evolved in ancestrally anaerobic pathways for essential cofactor biosynthesis including NAD+, pyridoxal, thiamine, ubiquinone, cobalamin, heme, and chlorophyll. These innovations allowed prokaryotes to synthesize essential cofactors in O2‐containing environments, a prerequisite for the later emergence of aerobic respiratory chains.

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On the evolution of cytochrome oxidases consuming oxygen

Cited by 17 publications

References 62 publications

Respiratory Heme A-Containing Oxidases Originated in the Ancestors of Iron-Oxidizing Bacteria

Respiratory Heme A-Containing Oxidases Originated in the Ancestors of Iron-Oxidizing Bacteria

Genomic evolution of the class Acidithiobacillia: deep-branching Proteobacteria living in extreme acidic conditions

The radical impact of oxygen on prokaryotic evolution—enzyme inhibition first, uninhibited essential biosyntheses second, aerobic respiration third

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