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Evolution of the Peroxisomal Proteome

  • Toni GabaldónEmail author
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 89)

Abstract

Peroxisomes are single-membrane bound intracellular organelles that can be found in organisms across the tree of eukaryotes, and thus are likely to derive from an ancestral peroxisome in the last eukaryotic common ancestor (LECA). Yet, peroxisomes in different lineages can present a large diversity in terms of their metabolic capabilities, which reflects a highly variable proteomic content. Theories on the evolutionary origin of peroxisomes have shifted in the last decades from scenarios involving an endosymbiotic origin, similar to those of mitochondria and plastids, towards hypotheses purporting an endogenous origin from within the endomembrane system. The peroxisomal proteome is highly dynamic in evolutionary terms, and can evolve via differential loss and gain of proteins, as well as via relocalization of proteins from and to other sub-cellular compartments. Here, I review current knowledge and discussions on the diversity, origin, and evolution of the peroxisomal proteome.

Keywords

Peroxisomes Evolution Peroxisomal proteome Endomembrane system 

Abbreviations

LECA

Last eukaryotic common ancestor

H2O2

Hydrogen peroxide

PEX

Peroxin

ER

Endoplasmic reticulum

ERAD

Endoplasmic reticulum associated decay

AGT

Alanine:glyoxylate aminotransferase

PXA

Peroxisomal ABC transporter

CTA

Catalase

FOX

Fatty acid oxidase

FAA

Fatty acid CoA synthetase

Notes

Acknowledgements

TG acknowledges support of the Spanish Ministry of Economy and Competitiveness grants, ‘Centro de Excelencia Severo Ochoa 2013-2017’ SEV-2012-0208, and BFU2015-67107 cofounded by European Regional Development Fund (ERDF); from the CERCA Programme/Generalitat de Catalunya; from the Catalan Research Agency (AGAUR) SGR857, and grants from the European Union’s Horizon 2020 research and innovation programme under the grant agreement ERC-2016-724173 and the Marie Sklodowska-Curie grant agreement No H2020-MSCA-ITN-642095.

References

  1. Andersen JS, Mann M (2006) Organellar proteomics: turning inventories into insights. EMBO Reports 874–879.  https://doi.org/10.1038/sj.embor.7400780CrossRefGoogle Scholar
  2. Antonenkov VD, Hiltunen JK (2012) Transfer of metabolites across the peroxisomal membrane. Biochim Biophys Acta Mol Basis Dis 1374–1386.  https://doi.org/10.1016/j.bbadis.2011.12.011CrossRefGoogle Scholar
  3. Bowers WE (1998) Christian de Duve and the discovery of lysosomes and peroxisomes. Trends in Cell Biol 330–333.  https://doi.org/10.1016/s0962-8924(98)01314-2CrossRefGoogle Scholar
  4. Breidenbach RW, Kahn A, Beevers H (1968) Characterization of glyoxysomes from castor bean endosperm. Plant Physiol 43(5):705–713.  https://doi.org/10.1104/PP.43.5.705CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cooper TG, Beevers H (1969) Beta oxidation in glyoxysomes from castor bean endosperm. J Biol Chem 244(13):3514–3520PubMedGoogle Scholar
  6. de Duve C (1982) Peroxisomes and related particles in historical perspective. Ann NY Acad Sci 386(1):1–4.  https://doi.org/10.1111/j.1749-6632.1982.tb21402.xCrossRefPubMedGoogle Scholar
  7. De Duve C (1996) ‘The peroxisome in retrospect. Ann NY Acad Sci 1–10.  https://doi.org/10.1111/j.1749-6632.1996.tb18603.xCrossRefGoogle Scholar
  8. De Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 395–403.  https://doi.org/10.1038/nrg2071CrossRefGoogle Scholar
  9. De Duve C, Baudhuin P (1966) Peroxisomes (microbodies and related particles). Physiol Rev 46(2):323–357CrossRefGoogle Scholar
  10. Erdmann R, Schliebs W (2005) Peroxisomal matrix protein import: the transient pore model. Nat Rev Mol Cell Biol 738–742.  https://doi.org/10.1038/nrm1710CrossRefGoogle Scholar
  11. Gabaldón T et al (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 8.  https://doi.org/10.1186/1745-6150-1-8CrossRefGoogle Scholar
  12. Gabaldón T (2010) Peroxisome diversity and evolution. Philosophical Trans Royal Soc Lond Ser B: Biol Sci 365(1541):765–773. Available at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20124343
  13. Gabaldón T (2014a) A metabolic scenario for the evolutionary origin of peroxisomes from the endomembranous system. Cell Mol Life Sci 71(13):2373–2376.  https://doi.org/10.1007/s00018-013-1424-zCrossRefPubMedGoogle Scholar
  14. Gabaldón T (2014b) Evolutionary considerations on the origin of peroxisomes from the endoplasmic reticulum, and their relationships with mitochondria. Cell Mol Life Sci 2379–2382.  https://doi.org/10.1007/s00018-014-1640-1CrossRefGoogle Scholar
  15. Gabaldón T, Ginger ML, Michels PAM (2016) Peroxisomes in parasitic protists. Mol Biochem Parasitol 209(1–2):35–45.  https://doi.org/10.1016/j.molbiopara.2016.02.005CrossRefPubMedGoogle Scholar
  16. Gabaldón T, Pittis AA (2015) Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes. Biochimie 119:262–268.  https://doi.org/10.1016/j.biochi.2015.03.021CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gualdrón-López M et al (2012) When, how and why glycolysis became compartmentalised in the Kinetoplastea. A new look at an ancient organelle. Int J Parasitol 1–20.  https://doi.org/10.1016/j.ijpara.2011.10.007CrossRefGoogle Scholar
  18. Holland HD et al (2006) The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci 361(1470):903–915.  https://doi.org/10.1098/rstb.2006.1838CrossRefPubMedPubMedCentralGoogle Scholar
  19. Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2(4):226–231.  https://doi.org/10.1038/35008652CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lazarow PB, De Duve C (1976) A fatty acyl-CoA oxidizing system in rat liver peroxisomes; enhancement by clofibrate, a hypolipidemic drug. Proc Natl Acad Sci USA 73(6):2043–2046.  https://doi.org/10.1073/pnas.73.6.2043CrossRefPubMedGoogle Scholar
  21. Ludewig-Klingner A-K et al (2018) Distribution and evolution of peroxisomes in alveolates (apicomplexa, dinoflagellates, ciliates). Genome Biol Evol 10(1):1–13.  https://doi.org/10.1093/gbe/evx250CrossRefPubMedGoogle Scholar
  22. Opperdoes FR, Borst P (1977) Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett 80(2):360–364.  https://doi.org/10.1016/0014-5793(77)80476-6CrossRefPubMedGoogle Scholar
  23. Pieuchot L, Jedd G (2012) Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu Rev Microbiol 66(1):237–263.  https://doi.org/10.1146/annurev-micro-092611-150126CrossRefGoogle Scholar
  24. Rhodin JAG (1954) Correlation of ultrastructural organization : and function in normal and experimentally changed proximal convoluted tubule cells of the mouse kidney: an electron microscopic study. Department of Anatomy, Karolinska Institute, SolnaGoogle Scholar
  25. Schlüter A et al (2006) The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol Biol Evol 23(4):838–845.  https://doi.org/10.1093/molbev/msj103CrossRefPubMedGoogle Scholar
  26. Schlüter A et al (2007) PeroxisomeDB: a database for the peroxisomal proteome, functional genomics and disease. Nucleic Acids Res. Oxford University Press 35(Database issue) D815–D822. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1747181&tool=pmcentrez&rendertype=abstract
  27. Smith JJ, Aitchison JD (2013) Peroxisomes take shape. Nat Rev Mol Cell Biol 803–817.  https://doi.org/10.1038/nrm3700CrossRefGoogle Scholar
  28. Speijer D (2011) Oxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it. BioEssays 33(2):88–94.  https://doi.org/10.1002/bies.201000097CrossRefPubMedGoogle Scholar
  29. Speijer D (2017) Evolution of peroxisomes illustrates symbiogenesis. BioEssays 39(9).  https://doi.org/10.1002/bies.201700050CrossRefGoogle Scholar
  30. Szabo AS, Avers CJ (1969) Some aspects of regulation of peroxisomes and mitochondria in yeast. Ann NY Acad Sci 168(2):302–312.  https://doi.org/10.1111/j.1749-6632.1969.tb43117.xCrossRefPubMedGoogle Scholar
  31. Szöör B et al (2014) Evolution, dynamics and specialized functions of glycosomes in metabolism and development of trypanosomatids. Curr Opin Microbiol 79–87.  https://doi.org/10.1016/j.mib.2014.09.006CrossRefGoogle Scholar
  32. Tabak HF et al (2003) Peroxisomes start their life in the endoplasmic reticulum. Traffic (Copenhagen, Denmark) 4(8):512–518. doi:110 [pii]Google Scholar
  33. Taylor SW, Fahy E, Ghosh SS (2003) Global organellar proteomics. Trends in Biotechnol 82–88.  https://doi.org/10.1016/s0167-7799(02)00037-9CrossRefGoogle Scholar
  34. Terlecky SR et al (2009) The role of peroxisomes in the regulation of Podospora anserina sexual development. Res Signpost 37661(2):61–85Google Scholar
  35. Tolbert NE et al (1968) Peroxisomes from spinach leaves containing enzymes related to glycolate metabolism. J Biol Chem 243(19):5179–5184PubMedGoogle Scholar
  36. van der Klei IJ, Veenhuis M (2013) The versatility of peroxisome function in filamentous fungi. Subcell Biochem 69:135–152.  https://doi.org/10.1007/978-94-007-6889-5_8CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology (BIST)BarcelonaSpain
  2. 2.Universitat Pompeu Fabra (UPF)BarcelonaSpain
  3. 3.Institució Catalana de Recerca i Estudis Avançats (ICREA)BarcelonaSpain

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