Evolutionary loss of peroxisomes--not limited to parasites

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

Fig. 1

Distribution of peroxins (A), and possible peroxisomal enzymes (B) in metazoan genomes. Organisms lacking peroxins are highlighted in red. a Identification of peroxins. The green squares indicate identification with high confidence. The identification of Pex10 in the Oikopleura dioica genome with lower confidence (marked by an asterisk) was rejected as a false-positive based on phylogenetic analysis (Figure S1). b Identification of putative peroxisomal enzymes and enyzmes of mitochondrial beta-oxidation. Predicted subcellular localization is indicated in the following colors: grey, no targeting signal detected; red, peroxisomal targeting sequence type 1 or 2 (pts); blue, mitochondrial localization signal (mito); and yellow, secretory pathway signal peptide (sec). Combinations of several different localization signals are shown as follows: violet, pts and mito; orange, pts and sec; green, sec and mito; and black, pts, mito and sec. (Acox1 - Acyl-CoA oxidase1, Acox3 - Acyl-CoA oxidase 3, Lbp - L-bifunctional protein, Dbp - D-bifunctional protein, Acaa1 - Peroxisomal beta-ketothiolase 1, Scp2 - Peroxisomal beta-ketothiolase 2, Amacr - Alpha-methylacyl-CoA racemase, Crat - Carnitine acetyltransferase, Crot - Carnitine octanoyltransferase, Ech1 - Enoyl Coenzyme A hydratase 1, Decr - Peroxisomal 2,4-dienoyl-CoA reductase 2, Pec1 - Peroxisomal 3,2-trans-enoyl-CoA isomerase, Vlcs - Very-long-chain acyl-CoA synthetase, Pte1 - Acyl-CoA thioesterase 2, Pte2 - Acyl-CoA thioesterase 1B, Phyh - Phytanoyl-CoA 2-hydroxylase, Hpcl2 - 2-Hydroxyphytanoyl-CoA lyase, Gnpat - Dihydroxyacetone phosphate acyltransferase, Agps - Alkyldihydroxyacetone phosphate synthase, Far - Fatty acyl-CoA reductase 2, Agxt - Alanine:glyoxylate aminotransferase, Pipox - Peroxisomal sarcosine oxidase/L-pipecolate oxidase, Cat - Catalase, Prdx5 - Peroxiredoxin V, Dao - d-amino acid oxidase, Hao1 - Hydroxyacid oxidase 1, Ephx2 - Epoxide hydrolase, Gstk1 - Glutathione S-transferase class Kappa, Paox - N1-acetylspermine/spermidine oxidase, Xdh - Xanthine dehydrogenase, Uox - Uricase, Allc – Allantoicase)

Fig. 2

Number of unique orthologous groups in the metazoan eggNOG database that were assigned to genomes. Organisms were sorted into crude taxonomic groups. For a complete list, see Table S1. Organisms lacking peroxins are shown in red. Parasitic nematodes harboring peroxisomes are represented by yellow circles.