Evolutionary loss of peroxisomes – not limited to parasites

Vojtěch Žárský, Jan Tachezy

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. 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. Our 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. We 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. This article was reviewed by Michael Gray and Nick Lane.