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Endosymbiotic origin and differential loss of eukaryotic genes

Nature volume 524, pages 427432 (27 August 2015) | Download Citation

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.

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Acknowledgements

We thank the following funding agencies: the European Research Council grants 232975, 666053 (W.F.M.) and 281357 (G.L.; to T. Dagan); the Templeton Foundation grant 48177 (J.O.M.); the Open University of Israel Research Fund (E.H.-C.); the German-Israeli Foundation grant I-1321-203.13/2015 (E.H.-C., W.F.M.), the New Zealand BioProtection CoRE (P.J.L.); the German Academic Exchange Service PhD stipend 57076385 (C.K.); an Alexander von Humboldt Foundation fellowship (D.B.). Computational support of the Zentrum für Informations- und Medientechnologie at the Heinrich-Heine University is acknowledged.

Author information

Affiliations

  1. Institute of Molecular Evolution, Heinrich-Heine University, 40225 Düsseldorf, Germany

    • Chuan Ku
    • , Shijulal Nelson-Sathi
    • , Mayo Roettger
    • , Filipa L. Sousa
    •  & William F. Martin
  2. Institute of Fundamental Sciences, Massey University, Palmerston North 4474, New Zealand

    • Peter J. Lockhart
  3. Department of Mathematics and Statistics, University of Otago, Dunedin 9054, New Zealand

    • David Bryant
  4. Department of Natural and Life Sciences, The Open University of Israel, Ra’anana 43107, Israel

    • Einat Hazkani-Covo
  5. Department of Biology, National University of Ireland, Maynooth, County Kildare, Ireland

    • James O. McInerney
  6. Michael Smith Building, The University of Manchester, Oxford Rd, Manchester M13 9PL, UK

    • James O. McInerney
  7. Genomic Microbiology Group, Institute of Microbiology, Christian-Albrechts-University of Kiel, 24118 Kiel, Germany

    • Giddy Landan
  8. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, 2780-157 Oeiras, Portugal

    • William F. Martin

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Contributions

C.K., G.L., S.N.-S., E.H.-C., D.B., M.R., P.J.L., J.O.M., and W.F.M. designed experiments. C.K., G.L., S.N.-S., M.R., F.L.S., and E.H.-C. performed analyses. C.K., S.N.S., F.L.S., P.J.L., D.B., E.H.-C., J.O.M., G.L., and W.F.M. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to William F. Martin.

Extended data

Supplementary information

Excel files

  1. 1.

    Supplementary Table 1

    List of 55 eukaryote genomes organized by six eukaryotic supergroups, sources of genome sequences, 28,702 eukaryotic protein clusters with at least two sequences and maximum-likelihood trees of eukaryote-specific clusters (ESCs) with at least four sequences.

  2. 2.

    Supplementary Table 2

    List of 956,053 eukaryotic protein sequences in the sequence abbreviations used in this study and the original headers in the downloaded files.

  3. 3.

    Supplementary Table 3

    List of 1,847 bacterial genomes, their taxonomical groupings and 102,089 clusters with at least five sequences, as well as a maximum likelihood reference tree based on 32 nearly universal single-copy genes.

  4. 4.

    Supplementary Table 4

    List of 134 archaeal genomes, their taxonomical groupings and 11,992 clusters with at least five sequences.

  5. 5.

    Supplementary Table 5

    List of 2,585 eukaryote-prokaryote clusters (EPCs).

  6. 6.

    Supplementary Table 6

    Annotations of the functions of the 28,702 eukaryotic clusters and eukaryote monophyly in EPC trees.

  7. 7.

    Supplementary Table 8

    Frequency of occurrence of prokaryotic taxa in the sister group to eukaryotes and a two-sided Wilcoxon signed rank test comparing the original frequencies and those after randomizations.

Text files

  1. 1.

    Supplementary Table 7

    Maximum-likelihood trees with at least four sequences reconstructed from eukaryote-prokaryote clusters (EPCs).

PDF files

  1. 1.

    Supplementary Table 9

    BLAST analysis of bacterial, mitochondrial and plastid genomes against the nuclear genomes.

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https://doi.org/10.1038/nature14963

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