The evolution of YidC/Oxa/Alb3 family in the three domains of life: A phylogenomic analysis

Abstract

Background: YidC/Oxa/Alb3 family includes a group of conserved translocases that are essential for protein insertion into inner membranes of bacteria and mitochondria, and thylakoid membranes of chloroplasts. Because mitochondria and chloroplasts are of bacterial origin, Oxa and Alb3, like many other mitochondrial/chloroplastic proteins, are hypothetically derived from the pre-existing protein (YidC) of bacterial endosymbionts. Here, we test this hypothesis and investigate the evolutionary history of the whole YidC/Oxa/Alb3 family in the three domains of life. Results: Our comprehensive analyses of the phylogenetic distribution and phylogeny of the YidC/Oxa/Alb3 family lead to the following findings: 1) In archaea, YidC homologs are only sporadically distributed in Euryarchaeota; 2) Most bacteria contain only one YidC gene copy; some species in a few taxa (Bacillus, Lactobacillales, Actinobacteria and Clostridia) have two gene copies; 3) Eukaryotic Oxa and Alb3 have two separate prokaryotic origins, but they might not arise directly from the YidC of proteobacteria and cyanobacteria through the endosymbiosis origins of mitochondrium and chloroplast, respectively; 4) An ancient duplication occurred on both Oxa and Alb3 immediately after their origins, and thus most eukaryotes generally bear two Oxa and two Alb3. However, secondary loss, duplication or acquisition of new domain also occurred on the two genes in some lineages, especially in protists, resulting in a rich diversity or adaptive differentiation of the two translocases in these lineages. Conclusion: YidC is distributed in bacteria and some Euryarchaeota. Although mitochondrial Oxa and chloroplastic Alb3 are derived from the prokaryotic YidC, their origin might be not related to the endosymbiosis events of the two organelles. In some eukaryotic lineages, especially in protists, Oxa and Alb3 have diverse evolutionary histories. Finally, a model for the evolutionary history of the entire YidC/Oxa/Alb3 family in the three domains of life is proposed.