Abstract
BackgroundPeroxisomes are ubiquitous eukaryotic organelles involved in various oxidative reactions. Their enzymatic content varies between species, but the presence of common protein import and organelle biogenesis systems support a single evolutionary origin. The precise scenario for this origin remains however to be established. The ability of peroxisomes to divide and import proteins post-translationally, just like mitochondria and chloroplasts, supports an endosymbiotic origin. However, this view has been challenged by recent discoveries that mutant, peroxisome-less cells restore peroxisomes upon introduction of the wild-type gene, and that peroxisomes are formed from the Endoplasmic Reticulum. The lack of a peroxisomal genome precludes the use of classical analyses, as those performed with mitochondria or chloroplasts, to settle the debate. We therefore conducted large-scale phylogenetic analyses of the yeast and rat peroxisomal proteomes.ResultsOur results show that most peroxisomal proteins (39–58%) are of eukaryotic origin, comprising all proteins involved in organelle biogenesis or maintenance. A significant fraction (13–18%), consisting mainly of enzymes, has an alpha-proteobacterial origin and appears to be the result of the recruitment of proteins originally targeted to mitochondria. Consistent with the findings that peroxisomes are formed in the Endoplasmic Reticulum, we find that the most universally conserved Peroxisome biogenesis and maintenance proteins are homologous to proteins from the Endoplasmic Reticulum Assisted Decay pathway.ConclusionAltogether our results indicate that the peroxisome does not have an endosymbiotic origin and that its proteins were recruited from pools existing within the primitive eukaryote. Moreover the reconstruction of primitive peroxisomal proteomes suggests that ontogenetically as well as phylogenetically, peroxisomes stem from the Endoplasmic Reticulum.ReviewersThis article was reviewed by Arcady Mushegian, Gáspár Jékely and John LogsdonOpen peer reviewReviewed by Arcady Mushegian, Gáspar Jékely and John Logsdon. For the full reviews, please go to the Reviewers' comments section.
Highlights
Peroxisomes are ubiquitous eukaryotic organelles involved in various oxidative reactions
Strong arguments support the view of peroxisomes as autonomous organelles with an endosymbiotic origin: i) matrix enzymes are synthesized on free polyribosomes and post-translationally imported into the organelles, ii) peroxisomes have their own protein import machinery, like mitochondria and chloroplasts, and iii) peroxisomes have been shown to divide [4]
Pex1 and Pex6, AAA cassette containing proteins, have evolved from Cdc48/p97 [13] (Figure 1a), a protein central to the ERAD pathway which is involved in Golgi vesicle fusion and spindle body disassembly after mitosis; Pex2 and Pex10, ubiquitin ligase domain (RING domain) containing proteins, contain homology to the ERAD ubiquitin ligase Hrd1; the TPR repeats of Pex5 are homologous to the SEL1 repeats of the Hrd1 interacting protein Hrd3; Pex4 contains an E2 ubiquitin conjugating enzyme domain and is homologous to the ERAD ubiquitin conjugating enzymes Ubc1, Ubc6 and Ubc7
Summary
Peroxisomes are ubiquitous eukaryotic organelles involved in various oxidative reactions Their enzymatic content varies between species, but the presence of common protein import and organelle biogenesis systems support a single evolutionary origin. The ability of peroxisomes to divide and import proteins post-translationally, just like mitochondria and chloroplasts, supports an endosymbiotic origin. This view has been challenged by recent discoveries that mutant, peroxisome-less cells restore peroxisomes upon introduction of the wild-type gene, and that peroxisomes are formed from the Endoplasmic Reticulum. Photorespiration is typical for plant peroxisomes while peroxisomes of various yeasts can oxidize alkanes or methanol Despite this diversity all these organelles belong to the same microbody family. Strong arguments support the view of peroxisomes as autonomous organelles with an endosymbiotic origin: i) matrix enzymes are synthesized on free polyribosomes and post-translationally imported into the organelles, ii) peroxisomes have their own protein import machinery, like mitochondria and chloroplasts, and iii) peroxisomes have been shown to divide [4]
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