Letter | Published:

Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry

Nature volume 531, pages 101104 (03 March 2016) | Download Citation

Abstract

The origin of eukaryotes stands as a major conundrum in biology1. Current evidence indicates that the last eukaryotic common ancestor already possessed many eukaryotic hallmarks, including a complex subcellular organization1,2,3. In addition, the lack of evolutionary intermediates challenges the elucidation of the relative order of emergence of eukaryotic traits. Mitochondria are ubiquitous organelles derived from an alphaproteobacterial endosymbiont4. Different hypotheses disagree on whether mitochondria were acquired early or late during eukaryogenesis5. Similarly, the nature and complexity of the receiving host are debated, with models ranging from a simple prokaryotic host to an already complex proto-eukaryote1,3,6,7. Most competing scenarios can be roughly grouped into either mito-early, which consider the driving force of eukaryogenesis to be mitochondrial endosymbiosis into a simple host, or mito-late, which postulate that a significant complexity predated mitochondrial endosymbiosis3. Here we provide evidence for late mitochondrial endosymbiosis. We use phylogenomics to directly test whether proto-mitochondrial proteins were acquired earlier or later than other proteins of the last eukaryotic common ancestor. We find that last eukaryotic common ancestor protein families of alphaproteobacterial ancestry and of mitochondrial localization show the shortest phylogenetic distances to their closest prokaryotic relatives, compared with proteins of different prokaryotic origin or cellular localization. Altogether, our results shed new light on a long-standing question and provide compelling support for the late acquisition of mitochondria into a host that already had a proteome of chimaeric phylogenetic origin. We argue that mitochondrial endosymbiosis was one of the ultimate steps in eukaryogenesis and that it provided the definitive selective advantage to mitochondria-bearing eukaryotes over less complex forms.

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Acknowledgements

T.G. group research is funded in part by a grant from the Spanish Ministry of Economy and Competitiveness (BIO2012-37161), a grant from the European Union FP7 FP7-PEOPLE-2013-ITN-606786 and a grant from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC (Grant Agreement number ERC-2012-StG-310325).

Author information

Affiliations

  1. Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Carrer del Dr Aiguader, 88, 08003 Barcelona, Spain

    • Alexandros A. Pittis
    •  & Toni Gabaldón
  2. Departament of Ciències Experimentals I de La Salut, Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain

    • Alexandros A. Pittis
    •  & Toni Gabaldón
  3. Institució Catalana de Recerca i Estudis Avançats (ICREA), Passeig de Lluís Companys 23, 08010 Barcelona, Spain

    • Toni Gabaldón

Authors

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Contributions

A.A.P. and T.G. conceived the study. A.A.P. performed the computational analyses. A.A.P. and T.G. analysed and interpreted the data. A.A.P. and T.G. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Toni Gabaldón.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Notes, which comprise alternative methods and tests, and additional references.

Excel files

  1. 1.

    Supplementary Table 1

    The selected 37 eukaryotic species and the 692 prokaryotic taxonomic levels used for sub-sampling the eggNOG v4 orthologous groups.

  2. 2.

    Supplementary Table 2

    The file contains information on the protein families assigned to LECA, on which the subsequent analysis was performed. This includes information based on the phylogenetic inference (sister group, component assignment, branch length estimations) and the corresponding annotations, as provided by eggNOG v4 or as defined by the family's members.

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DOI

https://doi.org/10.1038/nature16941

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