Evolutionary loss of peroxisomes--not limited to parasites.

Vojtěch Žárský,Jan Tachezy

doi:10.1186/s13062-015-0101-6

Abstract

BackgroundPeroxisomes are ubiquitous eukaryotic organelles that compartmentalize a variety of metabolic pathways that are primarily related to the oxidative metabolism of lipids and the detoxification of reactive oxygen species. The importance of peroxisomes is underscored by serious human diseases, which are caused by disorders in peroxisomal functions. Some eukaryotic lineages, however, lost peroxisomes. These organisms are mainly anaerobic protists and some parasitic lineages including Plasmodium and parasitic platyhelminths. Here we performed a systematic in-silico analysis of peroxisomal markers among metazoans to assess presence of peroxisomes and peroxisomal enzymes.ResultsOur analyses reveal an obvious loss of peroxisomes in all tested flukes, tapeworms, and parasitic roundworms of the order Trichocephalida. Intriguingly, peroxisomal markers are absent from the genome of the free-living tunicate Oikopleura dioica, which inhabits oxygen-containing niches of sea waters. We further map the presence and predicted subcellular localization of putative peroxisomal enzymes, showing that in organisms without the peroxisomal markers the set of these enzymes is highly reduced and none of them contains a predicted peroxisomal targeting signal.ConclusionsWe have shown that several lineages of metazoans independently lost peroxisomes and that the loss of peroxisomes was not exclusively associated with adaptation to anaerobic habitats and a parasitic lifestyle. Although the reason for the loss of peroxisomes from O. dioica is unclear, organisms lacking peroxisomes, including the free-living O. dioica, share certain typical r-selected traits: high fecundity, limited ontogenesis and relatively low complexity of the gene content. We hypothesize that peroxisomes are generally the first compartment to be lost during evolutionary reductions of the eukaryotic cell.ReviewersThis article was reviewed by Michael Gray and Nick Lane.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-015-0101-6) contains supplementary material, which is available to authorized users.

Highlights

Peroxisomes are ubiquitous eukaryotic organelles that compartmentalize a variety of metabolic pathways that are primarily related to the oxidative metabolism of lipids and the detoxification of reactive oxygen species
We assessed the presence or absence of 14 peroxins conserved in metazoans [21] by assigning the protein sequences to the evolutionary genealogy of genes: Non-supervised Orthologous Groups database of orthologous groups, which was constructed from representative metazoan sequences [27]
We observed the loss of the PTS2binding protein Pex7 in all nematodes which is in agreement with lack of the PTS2 pathway in Caenorhabditis elegas and other lineages [29,30,31]

Summary

Introduction

Peroxisomes are ubiquitous eukaryotic organelles that compartmentalize a variety of metabolic pathways that are primarily related to the oxidative metabolism of lipids and the detoxification of reactive oxygen species. Peroxisomes participate in a variety of metabolic functions, such as the reactive oxygen species detoxification, long-chain fatty acid beta-oxidation, plasmalogen synthesis, amino acid degradation, and purine. A unique group of proteins referred to as peroxins (Pexs) is required for peroxisome biogenesis and protein import. Peroxins mediate the post-translational import of folded proteins bound to cofactors or even of protein complexes [5]. Pex recognizes the peroxisomal targeting signal 1 (PTS1), which is composed of a canonical Ser-Lys-Leu tripeptide at the extreme C-terminus with common deviations of the canonical sequence [6]. Some other proteins carry a nonapeptide motif near the Nterminus termed PTS2, which is recognized by Pex7 [7]

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Conclusion