Peroxisome diversity and evolution

Abstract

Peroxisomes are organelles bounded by a single membrane that can be found in all major groups of eukaryotes. A single evolutionary origin of this cellular compartment is supported by the presence, in diverse organisms, of a common set of proteins implicated in peroxisome biogenesis and maintenance. Their enzymatic content, however, can vary substantially across species, indicating a high level of evolutionary plasticity. Proteomic analyses have greatly expanded our knowledge on peroxisomes in some model organisms, including plants, mammals and yeasts. However, we still have a limited knowledge about the distribution and functionalities of peroxisomes in the vast majority of groups of microbial eukaryotes. Here, I review recent advances in our understanding of peroxisome diversity and evolution, with a special emphasis on peroxisomes in microbial eukaryotes.

Figure 1.

Our state of knowledge on peroxisome diversity across the eukaryotic tree of life is represented. The level of information of peroxisomes is based on literature searches for each taxa and their major representatives. Circles next to the different taxa indicate the type of information that is available on peroxisomes. Red circles indicates that for this group, extensive biochemical data as well as comprehensive proteomics and bioinformatics surveys are available. Orange circles indicate an intermediate level of information on peroxisomal composition, mostly based on biochemical studies of individual proteins or pathways coupled with comprehensive sequence analyses to predict peroxisomal localization. Yellow circles indicate that the presence of peroxisomes in that group is well established but that the level of the characterization of their function and diversity within this group is very scarce. White circles indicate that the presence of peroxisomes has been studied in this group revealing an apparent absence of these organelles in all the members studied (only a white circle is associated with the group) or in some of them (circles with different colours are associated with the group). Absence of a circle next to the group indicates that the presence or absence of peroxisomes or their enzymatic content in this group remains to be clearly established. (Adapted from a modified version of fig. 1 of Keeling et al. (2005).)

Figure 2.

A schematic view of the peroxisome. The biogenesis and maintenance processes (full-line boxes), which comprise the proteins involved in protein import and organelle division, are present in all types of peroxisomes. The enzymatic content of the peroxisome (dashed-line boxes) is highly variable, with different enzymatic sets being present in different species. Enzymes involved in fatty acid metabolism and reactive oxygen species detoxification are widespread. Other additional pathways (in blue) might be restricted to certain groups of eukaryotes. The text at the right-hand side of the figure provides some important remarks about the diversity and evolution of each depicted process.

Figure 3.

A schematic view of mammalian peroxisomes. (a) Micrograph shows part of a rat liver cell, where peroxisomes (P), can be seen surrounded by other cellular compartments such as the nucleus (N), the rough endoplasmic reticulum (ER) and mitochondria (M). Note the crystalline lattice formed inside peroxisomes, which results from tightly bound enzymatic material. Picture kindly provided by Douglas F. Bray (University of Lethbridge). (b) A reconstruction of the peroxisomal proteome and metabolism as inferred from proteomics data is shown. Colour codes indicate the likely evolutionary origins of the proteins as follows: green, alphaproteobacterial; yellow, eukaryotic; red, actinomycetales; blue, cyanobacterial; and white, undetermined. (Adapted from a modified version of fig. 5 of Gabaldón et al. (2006).)

Figure 4.

Saccharomyces cerevisiae peroxisomal proteome and metabolism as inferred from proteomics data. Colour codes as in figure 3. (Adapted from a modified version of fig. 5 of Gabaldón et al. (2006).)