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Endosymbiotic origin and differential loss of eukaryotic genes

Author

Listed:
  • Chuan Ku

    (Institute of Molecular Evolution, Heinrich-Heine University)

  • Shijulal Nelson-Sathi

    (Institute of Molecular Evolution, Heinrich-Heine University)

  • Mayo Roettger

    (Institute of Molecular Evolution, Heinrich-Heine University)

  • Filipa L. Sousa

    (Institute of Molecular Evolution, Heinrich-Heine University)

  • Peter J. Lockhart

    (Institute of Fundamental Sciences, Massey University)

  • David Bryant

    (University of Otago)

  • Einat Hazkani-Covo

    (The Open University of Israel)

  • James O. McInerney

    (National University of Ireland
    Michael Smith Building, The University of Manchester)

  • Giddy Landan

    (Genomic Microbiology Group, Institute of Microbiology, Christian-Albrechts-University of Kiel)

  • William F. Martin

    (Institute of Molecular Evolution, Heinrich-Heine University
    Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa)

Abstract

Chloroplasts arose from cyanobacteria, mitochondria arose from proteobacteria. Both organelles have conserved their prokaryotic biochemistry, but their genomes are reduced, and most organelle proteins are encoded in the nucleus. Endosymbiotic theory posits that bacterial genes in eukaryotic genomes entered the eukaryotic lineage via organelle ancestors. It predicts episodic influx of prokaryotic genes into the eukaryotic lineage, with acquisition corresponding to endosymbiotic events. Eukaryotic genome sequences, however, increasingly implicate lateral gene transfer, both from prokaryotes to eukaryotes and among eukaryotes, as a source of gene content variation in eukaryotic genomes, which predicts continuous, lineage-specific acquisition of prokaryotic genes in divergent eukaryotic groups. Here we discriminate between these two alternatives by clustering and phylogenetic analysis of eukaryotic gene families having prokaryotic homologues. Our results indicate (1) that gene transfer from bacteria to eukaryotes is episodic, as revealed by gene distributions, and coincides with major evolutionary transitions at the origin of chloroplasts and mitochondria; (2) that gene inheritance in eukaryotes is vertical, as revealed by extensive topological comparison, sparse gene distributions stemming from differential loss; and (3) that continuous, lineage-specific lateral gene transfer, although it sometimes occurs, does not contribute to long-term gene content evolution in eukaryotic genomes.

Suggested Citation

  • Chuan Ku & Shijulal Nelson-Sathi & Mayo Roettger & Filipa L. Sousa & Peter J. Lockhart & David Bryant & Einat Hazkani-Covo & James O. McInerney & Giddy Landan & William F. Martin, 2015. "Endosymbiotic origin and differential loss of eukaryotic genes," Nature, Nature, vol. 524(7566), pages 427-432, August.
  • Handle: RePEc:nat:nature:v:524:y:2015:i:7566:d:10.1038_nature14963
    DOI: 10.1038/nature14963
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    Cited by:

    1. Fernando Rodriguez & Irina A. Yushenova & Daniel DiCorpo & Irina R. Arkhipova, 2022. "Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Ezequiel Monteforte, 2018. "Las Bases Técnicas como expresión del desarrollo del conocimiento humano: medios de producción, materialidad del trabajo y formas de conciencia," Ensayos de Economía 16780, Universidad Nacional de Colombia Sede Medellín.
    3. Shivam Yadav & Martin Centola & Mathilda Glaesmann & Denys Pogoryelov & Roman Ladig & Mike Heilemann & L. C. Rai & Özkan Yildiz & Enrico Schleiff, 2022. "Cyclophilin anaCyp40 regulates photosystem assembly and phycobilisome association in a cyanobacterium," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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