Abstract
BackgroundCardiolipin (CL) is an important component in mitochondrial inner and bacterial membranes. Its appearance in these two biomembranes has been considered as evidence of the endosymbiotic origin of mitochondria. But CL was reported to be synthesized through two distinct enzymes--CLS_cap and CLS_pld in eukaryotes and bacteria. Therefore, how the CL biosynthesis pathway evolved is an interesting question.ResultsPhylogenetic distribution investigation of CL synthase (CLS) showed: most bacteria have CLS_pld pathway, but in partial bacteria including proteobacteria and actinobacteria CLS_cap pathway has already appeared; in eukaryotes, Supergroup Opisthokonta and Archaeplastida, and Subgroup Stramenopiles, which all contain multicellular organisms, possess CLS_cap pathway, while Supergroup Amoebozoa and Excavata and Subgroup Alveolata, which all consist exclusively of unicellular eukaryotes, bear CLS_pld pathway; amitochondriate protists in any supergroups have neither. Phylogenetic analysis indicated the CLS_cap in eukaryotes have the closest relationship with those of alpha proteobacteria, while the CLS_pld in eukaryotes share a common ancestor but have no close correlation with those of any particular bacteria.ConclusionsThe first eukaryote common ancestor (FECA) inherited the CLS_pld from its bacterial ancestor (e. g. the bacterial partner according to any of the hypotheses about eukaryote evolution); later, when the FECA evolved into the last eukaryote common ancestor (LECA), the endosymbiotic mitochondria (alpha proteobacteria) brought in CLS_cap, and then in some LECA individuals the CLS_cap substituted the CLS_pld, and these LECAs would evolve into the protist lineages from which multicellular eukaryotes could arise, while in the other LECAs the CLS_pld was retained and the CLS_cap was lost, and these LECAs would evolve into the protist lineages possessing CLS_pld. Besides, our work indicated CL maturation pathway arose after the emergence of eukaryotes probably through mechanisms such as duplication of other genes, and gene duplication and loss occurred frequently at different lineage levels, increasing the pathway diversity probably to fit the complicated cellular process in various cells. Our work also implies the classification putting Stramenopiles and Alveolata together to form Chromalveolata may be unreasonable; the absence of CL synthesis and maturation pathways in amitochondriate protists is most probably due to secondary loss.
Highlights
Cardiolipin (CL) is an important component in mitochondrial inner and bacterial membranes
The biosynthesis reaction is a reversible transesterification catalyzed by a kind of cardiolipin synthase (CLS) containing two phospholipase D (PLDc_2) domains– CLS_pld, while in eukaryotes, the reaction is not a reversible one catalyzed by another kind of CL synthase (CLS) containing one CDP-alcohol phosphatidyltransferase (CAP) domain–CLS_cap
The indispensable eukaryotic CL maturation process and enzymes are as follows: nascent CL is deacylated to form monolysocardiolipin (MLCL), which is catalyzed by either of the two kinds of enzymes–CL-specific phospholipase (CLD1, YGR110W) identified in yeast [17] and calcium-independent phospholipase A2 beta or gamma reported in Drosophila and rat [18,19]; MLCL is reacylated by CoA-independent tafazzin (TAZ) [20] or acylCoA:lysocardiolipin acyltransferase 1 (ALCAT1) [21] to become mature CL
Summary
Cardiolipin (CL) is an important component in mitochondrial inner and bacterial membranes. The indispensable eukaryotic CL maturation process and enzymes are as follows: nascent CL is deacylated to form monolysocardiolipin (MLCL), which is catalyzed by either of the two kinds of enzymes–CL-specific phospholipase (CLD1, YGR110W) identified in yeast [17] and calcium-independent phospholipase A2 (iPLA2) beta or gamma reported in Drosophila and rat [18,19]; MLCL is reacylated by CoA-independent tafazzin (TAZ) [20] or acylCoA:lysocardiolipin acyltransferase 1 (ALCAT1) [21] to become mature CL. There is not such a maturation process at all
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