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Deep mitochondrial origin outside the sampled alphaproteobacteria
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Univ Utrecht, Dept Biol, Utrecht, Netherlands.
Uppsala University, Science for Life Laboratory, SciLifeLab. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.ORCID iD: 0000-0001-8354-2398
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2018 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 557, no 7703, p. 101-105Article in journal (Refereed) Published
Abstract [en]

Mitochondria are ATP-generating organelles, the endosymbiotic origin of which was a key event in the evolution of eukaryotic cells(1). Despite strong phylogenetic evidence that mitochondria had an alphaproteobacterial ancestry(2), 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 Rickettsiales(3-9), an order that includes several host-associated pathogenic and endosymbiotic lineages(10,11), others have suggested that mitochondria evolved from a free-living group(12-14). 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 ancestor(6,15,16) should be re-evaluated.

Place, publisher, year, edition, pages
2018. Vol. 557, no 7703, p. 101-105
Keywords [en]
Single-Cell, Evolution, Phylogeny, Sequence, Tree, Rickettsiales, Insights, Tool, Assembler, Selection
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-327305DOI: 10.1038/s41586-018-0059-5ISI: 000431234500038PubMedID: 29695865OAI: oai:DiVA.org:uu-327305DiVA, id: diva2:1130260
Funder
EU, European Research Council, 310039-PUZZLE_CELLSwedish Foundation for Strategic Research , SSF-FFL5Swedish Research Council, 2015-04959Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2018-07-25Bibliographically approved
In thesis
1. Exploration of microbial diversity and evolution through cultivation independent phylogenomics
Open this publication in new window or tab >>Exploration of microbial diversity and evolution through cultivation independent phylogenomics
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Our understanding of microbial evolution is largely dependent on available genomic data of diverse organisms. Yet, genome-sequencing efforts have mostly ignored the diverse uncultivable majority in favor of cultivable and sociologically relevant organisms. In this thesis, I have applied and developed cultivation independent methods to explore microbial diversity and obtain genomic data in an unbiased manner. The obtained genomes were then used to study the evolution of mitochondria, Rickettsiales and Haloarchaea.

Metagenomic binning of oceanic samples recovered draft genomes for thirteen novel Alphaproteobacteria-related lineages. Phylogenomics analyses utilizing the improved taxon sample suggested that mitochondria are not related to Rickettsiales but rather evolved from a proteobacterial lineage closely related to all sampled alphaproteobacteria.

Single-cell genomics and metagenomics of lake and oceanic samples, respectively, identified previously unobserved Rickettsiales-related lineages. They branched early relative to characterized Rickettsiales and encoded flagellar genes, a feature once thought absent in this order. Flagella are most likely an ancestral feature, and were independently lost during Rickettsiales diversification. In addition, preliminary analyses suggest that ATP/ADP translocase, the marker for energy parasitism, was acquired after the acquisition of type IV secretion systems during the emergence of the Rickettsiales.

Further exploration of the oceanic samples yielded the first draft genomes of Marine Group IV archaea, the closest known relatives of the Haloarchaea. The halophilic and generally aerobic Haloarchaea are thought to have evolved from an anaerobic methanogenic ancestor. The MG-IV genomes allowed us to study this enigmatic evolutionary transition. Preliminary ancestral reconstruction analyses suggest a gradual loss of methanogenesis and adaptation to an aerobic lifestyle, respectively.

The thesis further presents a new amplicon sequencing method that captures near full-length 16S and 23S rRNA genes of environmental prokaryotes. The method exploits PacBio's long read technology and the frequent proximity of these genes in prokaryotic genomes. Compared to traditional partial 16S amplicon sequencing, our method classifies environmental lineages that are distantly related to reference taxa more confidently.

In conclusion, this thesis provides new insights into the origins of mitochondria, Rickettsiales and Haloarchaea and illustrates the power of cultivation independent methods with respect to the study of microbial evolution.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. p. 71
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1539
Keywords
cultivation independent genomics, metagenomics, single-cell genomics, metagenomic binning, phylogenetics, phylogenomics, phylogenetic artefacts, comparative genomics, gene tree-species tree reconciliation, rRNA amplicon sequencing, Tara Oceans, origin of mitochondria, Alphaproteobacteria, Rickettsiales, Haloarchaea, endosymbiosis
National Category
Evolutionary Biology Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-327310 (URN)978-91-513-0025-2 (ISBN)
Public defence
2017-09-29, B/B22, Biomedical Center (BMC), Husargatan 3, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2017-09-08 Created: 2017-08-08 Last updated: 2017-10-17

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Martijn, JoranGuy, LionelEttema, Thijs J. G.

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