Evolution of the cytochrome-bd type oxygen reductase superfamily and the function of cydAA in Archaea

Cytochrome bd-type oxygen reductases (cytbd) belong to one of three enzyme superfamilies that catalyze oxygen reduction to water. They are widely distributed in Bacteria and Archaea, but the full extent of their biochemical diversity is unknown. Here we used phylogenomics to identify 3 families and several subfamilies within the cytbd superfamily. The core architecture shared by all members of the superfamily consists of four transmembrane helices that bind two active site hemes, which are responsible for oxygen reduction. While previously characterized cytochrome bd-type oxygen reductases use quinol as an electron donor to reduce oxygen, sequence analysis shows that only one of the identified families has a conserved quinol binding site. The other families are missing this feature, suggesting that they use an alternative electron donor. Multiple gene duplication events were identified within the superfamily, resulting in significant evolutionary and structural diversity. The CydAA’ cytbd, found exclusively in Archaea, is formed by the co-association of two superfamily paralogs. We heterologously expressed CydAA’ from Caldivirga maquilingensis and demonstrated that it performs oxygen reduction with quinol as an electron donor. Strikingly, CydAA’ is the first isoform of cytbd containing only b-type hemes shown to be active when isolated, demonstrating that oxygen reductase activity in this superfamily is not dependent on heme d

Convergent evolution of unusual complex I homologs with increased proton pumping capacity: energetic and ecological implications

Respiratory complex I is part of a large family of homologous enzymes that carry out the transfer of electrons between soluble cytoplasmic electron carriers and membrane-bound electron carriers. These complexes are vital bioenergetic enzymes that serve as the entry points into electron transport chains for a wide variety of microbial metabolisms, and electron transfer is coupled to proton translocation. The core complex of this enzyme is made up of 11 protein subunits, with three major proton pumping subunits. Here, we document a large number of modified complex I gene cassettes found in genome sequences from diverse cultured bacteria, shotgun metagenomics, and environmentally derived archaeal fosmids all of which encode a fourth proton pumping subunit. The incorporation of this extra subunit into a functional protein complex is supported by large amino acid insertions in the amphipathic helix that runs the length of the protein complex. Phylogenetic analyses reveal that these modified complexes appear to have arisen independently multiple times in a remarkable case of convergent molecular evolution. From an energetic perspective, we hypothesize that this modification on the canonical complex I architecture allows for the translocation of a fifth proton per reaction cycle—the physiological utility of this modified complex is discussed

Draft Genome Sequence of Ardenticatena maritime 110S, a Thermophilic Nitrate- and Iron-Reducing Member of the Chloroflexi Class Ardenticatenia

We report here the draft genome sequence of Ardenticatena maritima 110S, the first sequenced member of class Ardenticatenia of the phylum Chloroflexi. This thermophilic organism is capable of a range of physiologies, including aerobic respiration and iron reduction. It also encodes a complete denitrification pathway with a novel nitric oxide reductase

Draft Genome Sequence of Ornatilinea apprima P3M-1, an Anaerobic Member of the Chloroflexi Class Anaerolineae

We report the draft genome sequence of Ornatilinea apprima P3M-1, a strictly anaerobic member of the Chloroflexi class Anaerolineae. This genome provides insight into the diversity of metabolism within the Anaerolineae, and the evolution of respiration within the Chloroflexi

Draft Genome of Thermanaerothrix daxensis GNS-1, a Thermophilic Facultative Anaerobe from the Chloroflexi Class Anaerolineae

We present the draft genome of Thermanaerothrix daxensis GNS-1, a thermophilic member of the Chloroflexi phylum. This organism was initially characterized as a nonmotile, strictly anaerobic fermenter; however, genome analysis demonstrates that it encodes genes for a flagellum and multiple pathways for aerobic and anaerobic respiration

Draft Genome Sequence of Herpetosiphon geysericola GC-42, a Nonphototrophic Member of the Chloroflexi Class Chloroflexia

We report here the draft genome sequence of Herpetosiphon geysericola GC-42, a predatory nonphototrophic member of the class Chloroflexia in the phylum Chloroflexi. This genome provides insight into the evolution of phototrophy and aerobic respiration within the Chloroflexi

Draft Genome Sequence of Levilinea saccharolytica KIBI-1, a Member of the Chloroflexi Class Anaerolineae

We report the draft genome sequence of Levilinea saccharolytica KIBI-1, a facultative anaerobic member of the Chloroflexi class Anaerolineae. While L. saccharolytica was characterized as an obligate anaerobe, genome analysis provides evidence for the presence of both aerobic respiration and partial denitrification pathways

On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria

The origin of oxygenic photosynthesis in Cyanobacteria led to the rise of oxygen on Earth ~2.3 billion years ago, profoundly altering the course of evolution by facilitating the development of aerobic respiration and complex multicellular life. Here we report the genomes of 41 uncultured organisms related to the photosynthetic Cyanobacteria (class Oxyphotobacteria), including members of the class Melainabacteria and a new class of Cyanobacteria (class Sericytochromatia) that is basal to the Melainabacteria and Oxyphotobacteria. All members of the Melainabacteria and Sericytochromatia lack photosynthetic machinery, indicating that phototrophy was not an ancestral feature of the Cyanobacteria and that Oxyphotobacteria acquired the genes for photosynthesis relatively late in cyanobacterial evolution. We show that all three classes independently acquired aerobic respiratory complexes, supporting the hypothesis that aerobic respiration evolved after oxygenic photosynthesis