Complex evolution of two types of cardiolipin synthase in the eukaryotic lineage stramenopiles

• Published in: Molecular phylogenetics and evolution 2016-08, Vol.101, p.133-141
• Main Authors: Noguchi, Fumiya, Tanifuji, Goro, Brown, Matthew W., Fujikura, Katsunori, Takishita, Kiyotaka
• Format: Article
• Language: English
• Subjects: Cardiolipin synthase; Differential gene loss; DNA, Complementary - chemistry; DNA, Complementary - metabolism; Eukaryotes; Evolution, Molecular; Labyrinthulomycetes; Membrane Proteins - classification; Membrane Proteins - genetics; Membrane Proteins - metabolism; Mitochondria; Phylogenomics; Phylogeny; RNA - isolation & purification; RNA - metabolism; Sequence Analysis, DNA; Stramenopiles; Stramenopiles - enzymology; Transferases (Other Substituted Phosphate Groups) - classification; Transferases (Other Substituted Phosphate Groups) - genetics; Transferases (Other Substituted Phosphate Groups) - metabolism
• ISSN: 1055-7903; 1095-9513
• DOI: 10.1016/j.ympev.2016.05.011

[Display omitted] •Cardiolipin synthase (CLS)_pld as well as CLS_cap was found among stramenopiles.•CLS_pld-bearing species is in the most basal lineage of the stramenopile phylogeny.•A common ancestor of stramenopiles possibly had both CLS_pld and CLS_cap.•CLS_pld and CLS_cap may have been differentially lost in the stramenopile evolution. The phospholipid cardiolipin is indispensable for eukaryotes to activate mitochondria, and it was previously reported that two phylogenetically distinct types of enzyme synthesizing cardiolipin, one with two phospholipase D domains (CLS_pld) and the other with a CDP-alcohol phosphatidyltransferase domain (CLS_cap), are patchily and complementarily distributed at higher taxonomic (e.g., supergroup) levels of eukaryotes. Stramenopiles, one of the major eukaryotic clades, were considered to exclusively possess CLS_cap. However, through our present surveys with genome or transcriptome data from a broad range of stramenopile taxa, species with both CLS_cap and CLS_pld and species with only CLS_pld or CLS_cap were discovered among this group. Because these homologues of CLS_cap and CLS_pld retrieved from stramenopiles were likely inherited from the last eukaryotic common ancestor, it is reasonable to assume that a common ancestor of all stramenopiles harbored both CLS_cap and CLS_pld. Furthermore, based on the robust organismal phylogeny of stramenopiles unveiled with large-scale phylogenetic analyses, the earliest diverging lineage of stramenopiles (including bicosoecids, placidids, etc.) was found to comprise species with both CLS_cap and CLS_pld along with species with only either CLS_cap or CLS_pld. These findings suggest that a common ancestor of the most basal stramenopile lineage retained these two vertically inherited enzymes and that differential losses of either CLS_cap or CLS_pld occurred in this lineage. On the other hand, in the other stramenopile lineage composed of Ochrophyta, Pseudofungi, and Labyrinthulomycetes (to the exclusion of the most basal lineage), only CLS_cap was found, and therefore a common ancestor of these three groups likely lost CLS_pld. Based on our findings, the evolution of CLS_cap/CLS_pld in stramenopiles appears to be more complex than previously thought.