Peroxisome Diversity and Evolution

Downloaded from rstb.royalsocietypublishing.org on January 3, 2011 Peroxisome diversity and evolution Toni Gabaldón Phil. Trans. R. Soc. B 2010 365, 765-773 doi: 10.1098/rstb.2009.0240 References This article cites 63 articles, 20 of which can be accessed free http://rstb.royalsocietypublishing.org/content/365/1541/765.full.html#ref-list-1 Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1541/765 Subject collections Articles on similar topics can be found in the following collections cellular biology (98 articles) evolution (2302 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on January 3, 2011 Phil. Trans. R. Soc. B (2010) 365, 765–773 doi:10.1098/rstb.2009.0240 Review Peroxisome diversity and evolution Toni Gabaldoń* Centre for Genomic Regulation (CRG), Dr Aiguader, 88 08003 Barcelona, Spain 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. Keywords: peroxisomes; glyoxysomes; glycosomes; evolution; proteome 1. INTRODUCTION only be found in a very narrow range of species. This Peroxisomes, initially named microbodies, were first is the case for the fluorescent luciferase in fireflies noted by Rhodin (1954) as part of his PhD thesis on (Gould et al. 1987) or for several key enzymes for the morphology of proximal tubule cells from mouse the production of penicillin, which are restricted to a kidney. However, their initial characterization as a few fungal genera such as Penicillium (Kiel et al. novel type of cellular organelle came years later, 2000). Other peroxisomal pathways, in contrast, when Christian de Duve and his team were able to iso- show a more widespread distribution such as the b oxi- late peroxisomes from rat liver and study their dation of fatty acids or the set of enzymes responsible biochemical properties (de Duve & Baudhuin 1966). for oxidative stress response. Despite displaying such de Duve’s group identified the presence of several high levels of metabolic diversity, all peroxisomes enzymes involved in the production and degradation have in common a similar set of proteins involved in of hydrogen peroxide and hence gave the name peroxi- their biogenesis and maintenance, as well as the use somes to these organelles. Since then, peroxisomes of similar targeting signals for directing the localization have been isolated from a variety of other organisms of proteins to the organelle. The presence of these and it soon became evident that the specific metabolic common traits supports the idea of a single evolution- properties of peroxisomes can differ substantially from ary origin for all peroxisomes, although the exact species to species. Even at the level of a single organ- scenario still remains somewhat controversial ism, peroxisomes can display alternative enzymatic (de Duve 2007). contents depending on the specific tissue or the In recent years, we have witnessed several break- environmental conditions considered. Indeed, some throughs in peroxisome research, including the peroxisomes found in specific groups of organisms or elucidation of the molecular mechanisms involved in tissues are so divergent that they were initially classi- the formation and division of peroxisomes as well as fied as distinct organelles and are still now the finding of novel clues about their possible evol- commonly referred to with alternative names. For utionary origin (van der Zand et al. 2006). While instance, peroxisomes in trypanosomatid species har- such findings have clearly advanced our understanding bour certain glycolytic reactions and are therefore of the function and evolution of these widespread known as glycosomes (Michels et al. 2006), whereas organelles, there is still little information regarding some plant peroxisomes are named glyoxysomes the distribution and diversity of peroxisomes across because they mainly harbour enzymes of the glyoxylate the major groups of eukaryotic organisms. Indeed, cycle (Hayashi et al. 2000). In filamentous fungi, a par- most of our knowledge about peroxisomes comes ticular type of peroxisome, referred to as the Woronin from the characterization of peroxisomal proteins in body, functions in the maintenance of cellular integrity a handful of model species, including the human, by sealing the septal pore in response to wounding rat, mouse, the yeasts Saccharomyces cerevisiae, Pichia (Wu¨rtz et al. 2009). Some peroxisomal enzymes can pastoris, Hansenula polymorpha and Yarrowia lipolytica, and the model plant Arabidopsis thaliana. These model organisms represent only partially two of the *[email protected] five major groups in which eukaryotic diversity is cur- One contribution of 12 to a Theme Issue ‘Evolution of organellar rently classified (Keeling et al. 2005)(figure 1) and, metabolism in unicellular eukaryotes’. with the notable exception of yeast, they represent 765 This journal is # 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on January 3, 2011 766 T. Gabaldoń Review. Peroxisome diversity and evolution Discicristates Plantae Streptophytes Excavates Heterolobosea land plants Kinetoplastids Charophytes green algae Diplonemids Chlorophytes Euglenids Trebouxiophytes Core Jakobids Ulvophytes Trimastix Prasinophytes Oxymonads Mesostigma Trichomonads Hypermastigotes Floridiophytes red algae Carpediemonas Bangiophytes Retortamonads Cyanidiophytes Diplomonads Glaucophytes Malawimonads Cercomonads Euglyphids Cercozoa Apicomplexa Phaeodarea Colpodella Heteromitids Dinoflagellate Thaumatomonads Chlorarachniophytes Alveolates Oxyhrris Perkinsus Phytomyxids Ciliates Haplosporidia Colponema Foraminifera Polycystines Ellobiopsids Acantharia Rhizaria Diatoms Raphidiophytes Ascomycetes Eustigmatophytes Basidiomycetes Chrysophytes Zygomycetes Phaeophytes Microsporidia Bolidophytes Chytrids Blastocystis Nucleariids Actinophryids Animals Stramenopiles Labyrinthulids Choanoflagellate Thraustrochytrids Opisthokonts Oomycetes Capsaspora Opalinids Ichthyosporea Bicosoecids Dictyostelids Haptophytes Myxogastrids Protostelids Cryptomonads Lobosea Chromalveolates Archamoebae ‘Unikonts’ Amoebozoa 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).) complex multicellular organisms. Only recently, the In this review, I will provide an overview of the cur- interest has partially shifted to peroxisomes in rent state of our knowledge on peroxisome diversity microbial eukaryotes. Considering their adaptation to and evolution. For this, I will first focus on the a variety of niches and life styles, it is among these common mechanisms shared by all peroxisomes to organisms, where the highest diversity in terms of then survey what is known to be specific in the major metabolic properties of peroxisomes is expected. groupings of eukaryotic taxa. When discussing this Thanks to the availability of completely sequenced metabolic diversity, and to provide a logical frame- genomes for a growing number of microbial eukar- work, I will follow the classification of eukaryotic yotes, we are now just starting to unveil the existing taxa into five major groups, namely

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