Deep mitochondrial origin outside the sampled alphaproteobacteria

Abstract

Mitochondria are ATP-generating organelles, the endosymbiotic origin of which was a key event in the evolution of eukaryotic cells1. Despite strong phylogenetic evidence that mitochondria had an alphaproteobacterial ancestry2, efforts to pinpoint their closest relatives among sampled alphaproteobacteria have generated conflicting results, complicating detailed inferences about the identity and nature of the mitochondrial ancestor. While most studies support the idea that mitochondria evolved from an ancestor related to Rickettsiales3,4,5,6,7,8,9, an order that includes several host-associated pathogenic and endosymbiotic lineages10,11, others have suggested that mitochondria evolved from a free-living group12,13,14. Here we re-evaluate the phylogenetic placement of mitochondria. We used genome-resolved binning of oceanic metagenome datasets and increased the genomic sampling of Alphaproteobacteria with twelve divergent clades, and one clade representing a sister group to all Alphaproteobacteria. Subsequent phylogenomic analyses that specifically address long branch attraction and compositional bias artefacts suggest that mitochondria did not evolve from Rickettsiales or any other currently recognized alphaproteobacterial lineage. Rather, our analyses indicate that mitochondria evolved from a proteobacterial lineage that branched off before the divergence of all sampled alphaproteobacteria. In light of this new result, previous hypotheses on the nature of the mitochondrial ancestor6,15,16 should be re-evaluated.

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Fig. 1: Metagenomic exploration of oceanic alphaproteobacteria.
Fig. 2: Increased genomic sampling of alphaproteobacterial clades.
Fig. 3: Updated alphaproteobacterial tree.
Fig. 4: An early-branching mitochondrial ancestor.

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Acknowledgements

We thank the Tara Oceans consortium for generating metagenomic datasets and for making these publically available. We thank G. Herndl and C. Schleper for sharing metagenomic datasets before publication, and to M. Wu for sharing the genome of ‘Candidatus Magnetococcus yuandaducum’ before publication; K. Zaremba-Niedzwiedzka, C. Stairs, L. Eme, T. Williams, N. Lartillot, J. Alneberg, B. Quang Minh and H. C. Wang for useful advice, discussions and technical support; the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) at Uppsala University and the Swedish National Infrastructure for Computing (SNIC) at the PDC Center for High-Performance Computing for providing computational resources. This work is supported by grants of the European Research Council (ERC Starting grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (SSF-FFL5) and the Swedish Research Council (VR grant 2015-04959) awarded to T.J.G.E.

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Nature thanks T. Gabaldón, M. Gray and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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T.J.G.E. conceived the study. J.M., J.V. and P.O. screened metagenomic sequence datasets. J.M. and J.V. performed metagenome assemblies and metagenomic binning analyses. J.M. performed comparative genomics and phylogenetics analyses. J.M., L.G. and T.J.G.E. analysed and interpreted results. J.M. and T.J.G.E. wrote, and all authors edited and approved, the manuscript.

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Correspondence to Thijs J. G. Ettema.

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Supplementary Information

This file contains Supplementary Discussions, Supplementary Figures 1-27, Supplementary Tables 1-8 and Supplementary References.

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This source data is a Newick file that contains the result of a test described in Supplementary Discussion 1.1 (Randomization of mitochondrial sequences to assess LBA-related tree artefacts). The Newick file can be opened using general tree-viewing software such as Figtree.

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Martijn, J., Vosseberg, J., Guy, L. et al. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557, 101–105 (2018). https://doi.org/10.1038/s41586-018-0059-5

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