Molecular Evolution of Cytochrome bd Oxidases across Proteobacterial Genomes

Abstract

This work is aimed to resolve the complex molecular evolution of cytochrome bd ubiquinol oxidase, a nearly ubiquitous bacterial enzyme that is involved in redox balance and bioenergetics. Previous studies have created an unclear picture of bd oxidases phylogenesis without considering the existence of diverse types of bd oxidases. Integrated approaches of genomic and protein analysis focused on proteobacteria have generated a molecular classification of diverse types of bd oxidases, which produces a new scenario for interpreting their evolution. A duplication of the original gene cluster of bd oxidase might have occurred in the ancestors of extant α-proteobacteria of the Rhodospirillales order, such as Acidocella, from which the bd-I type of the oxidase might have diffused to other proteobacterial lineages. In contrast, the Cyanide-Insensitive Oxidase type may have differentiated into recognizable subtypes after another gene cluster duplication. These subtypes are widespread in the genomes of α-, β-, and γ-proteobacteria, with occasional instances of lateral gene transfer. In resolving the evolutionary pattern of proteobacterial bd oxidases, this work sheds new light on the basal taxa of α-proteobacteria from which the γ-proteobacterial lineage probably emerged.

Microbes vs. chemistry in the origin of the anaerobic gut lumen

“…The composition of the gut microbiota is highly variable along the length of the gut as well as across the intestine, and the mechanisms underlying the heterogeneity remain poorly characterized. For example, the taxa belonging to the Proteobacteria and Actinobacteria phyla are much more abundant in the small intestine than in the colon (11,23). Similar observations have been reported for the mucosally adherent rectal microbiota relative to feces (10).…”

“…Herein, we examined the abundance of the four bacterial phyla that account for greater than 98% of the taxa: Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes. The first two phyla are highly enriched in aerotolerant bacteria that are either aerobes or facultative anaerobes (23).…”

Genome Analysis of Structure–Function Relationships in Respiratory Complex I, an Ancient Bioenergetic Enzyme

“…The introduction of the methoxy ring substituents that differentiate ubiquinone (Q) from MQ and PQ has occurred when oxygen levels in the environment became sufficiently high to sustain the three hydroxylation reactions required in ubiquinone biosynthesis ( Aussel et al 2014 ). That time corresponded with the separation of aerobic proteobacteria from other prokaryotes ( Segata et al 2013 ; Degli Esposti et al 2015 ). In contrast with recent speculations ( Welte and Deppenmeier 2014 ), complex I subunits of aerobic proteobacteria do not show evident sequence variation that could be correlated with Q rather than MQ reactivity ( fig.…”

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F ig . 3.— Alignment of NuoD/Nad7/49-kDa subunit sequences of complex I and acquisition of Q reactivity in complex I. Sequences with the accession number identified on the left were first aligned using the COBALT feature of the BLAST program and then manually refined ( Degli Esposti et al 2015 ). ( A ) Alignment blocks of the NuoD/49-kDa subunit showing the four conserved regions that contribute to the architecture of the large Q reaction chamber.

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“…( B ) Phylogenetically wide tree of the NuoD/Nad7/49 kDa subunit. The neighbor-joining (NJ) tree was initially obtained using the deltaBLAST program ( Boratyn et al 2012 ; Degli Esposti et al 2015 ) using NuoD of Nitrospira defluvii (accession number: CBK40385) as the query and was extended to 5,000 sequences from bacteria and archaea possessing simplified Nuo operons. Note that after the early, well-separated branching groups of sulfur-reducing anaerobes (such as Nautiliales) and mbx -like complexes (which appear to be sister groups in trees of other Nuo subunits), as well as that of Fpo complexes, the proteins from other bacterial phyla are not well-resolved from each other, thus forming a semi-comb pattern of clades ( Bapteste et al 2008 ).…”