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An Alternative Root for the Eukaryote Tree of Life
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
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2014 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 24, no 4, 465-470 p.Article in journal (Refereed) Published
Abstract [en]

The root of the eukaryote tree of life defines some of the most fundamental relationships among species. It is also critical for defining the last eukaryote common ancestor (LECA), the shared heritage of all extant species. The unikont-bikont root has been the reigning paradigm for eukaryotes for more than 10 years but is becoming increasingly controversial. We developed a carefully vetted data set, consisting of 37 nuclear-encoded proteins of close bacterial ancestry (euBacs) and their closest bacterial relatives, augmented by deep sequencing of the Acrasis kona (Heterolobosea, Discoba) transcriptome. Phylogenetic analysis of these data produces a highly robust, fully resolved global phy- logeny of eukaryotes. The tree sorts all examined eukaryotes into three megagroups and identifies the Discoba, and potentially its parent taxon Excavata, as the sister group to the bulk of known eukaryote diversity, the proposed Neozoa (Amorphea + Stramenopila+Alveolata+Rhizaria+ Plantae [SARP]). All major alternative hypotheses are rejected with as little as w50% of the data, and this resolu- tion is unaffected by the presence of fast-evolving alignment positions or distant outgroup sequences. This ‘‘neozoan- excavate’’ root revises hypotheses of early eukaryote evolution and highlights the importance of the poorly stud- ied Discoba for understanding the evolution of eukaryotic diversity and basic cellular processes. 

Place, publisher, year, edition, pages
2014. Vol. 24, no 4, 465-470 p.
Keyword [en]
Eukaryote root, molecular phylogenetics, phylogenetics
National Category
Biological Systematics Evolutionary Biology Bioinformatics (Computational Biology)
Research subject
Biology with specialization in Evolutionary Organismal Biology; Biology with specialization in Molecular Evolution; Biology with specialization in Systematics
Identifiers
URN: urn:nbn:se:uu:diva-218740DOI: 10.1016/j.cub.2014.01.036ISI: 000331718900032OAI: oai:DiVA.org:uu-218740DiVA: diva2:696886
Funder
Swedish Research Council
Available from: 2014-02-16 Created: 2014-02-16 Last updated: 2017-12-06Bibliographically approved
In thesis
1. Inferring Ancestry: Mitochondrial Origins and Other Deep Branches in the Eukaryote Tree of Life
Open this publication in new window or tab >>Inferring Ancestry: Mitochondrial Origins and Other Deep Branches in the Eukaryote Tree of Life
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

There are ~12 supergroups of complex-celled organisms (eukaryotes), but relationships among them (including the root) remain elusive. For Paper I, I developed a dataset of 37 eukaryotic proteins of bacterial origin (euBac), representing the conservative protein core of the proto-mitochondrion. This gives a relatively short distance between ingroup (eukaryotes) and outgroup (mitochondrial progenitor), which is important for accurate rooting. The resulting phylogeny reconstructs three eukaryote megagroups and places one, Discoba (Excavata), as sister group to the other two (neozoa). This rejects the reigning “Unikont-Bikont” root and highlights the evolutionary importance of Excavata.

For Paper II, I developed a 150-gene dataset to test relationships in supergroup SAR (Stramenopila, Alveolata, Rhizaria). Analyses of all 150-genes give different trees with different methods, but also reveal artifactual signal due to extremely long rhizarian branches and illegitimate sequences due to horizontal gene transfer (HGT) or contamination. Removing these artifacts leads to strong consistent support for Rhizaria+Alveolata. This breaks up the core of the chromalveolate hypothesis (Stramenopila+Alveolata), adding support to theories of multiple secondary endosymbiosis of chloroplasts.

For Paper III, I studied the evolution of cox15, which encodes the essential mitochondrial protein Heme A synthase (HAS). HAS is nuclear encoded (nc-cox15) in all aerobic eukaryotes except Andalucia godoyi (Jakobida, Excavata), which encodes it in mitochondrial DNA (mtDNA) (mt-cox15). Thus the jakobid gene was postulated to represent the ancestral gene, which gave rise to nc-cox15 by endosymbiotic gene transfer. However, our phylogenetic and structure analyses demonstrate an independent origin of mt-cox15, providing the first strong evidence of bacteria to mtDNA HGT.

Rickettsiales or SAR11 often appear as sister group to modern mitochondria. However these bacteria and mitochondria also have independently evolved AT-rich genomes. For Paper IV, I assembled a dataset of 55 mitochondrial proteins of clear α-proteobacterial origin (including 30 euBacs). Phylogenies from these data support mitochondria+Rickettsiales but disagree on the placement of SAR11. Reducing amino-acid compositional heterogeneity (resulting from AT-bias) stabilizes SAR11 but moves mitochondria to the base of α-proteobacteria. Signal heterogeneity supporting other alternative hypotheses is also detected using real and simulated data. This suggests a complex scenario for the origin of mitochondria.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. 48 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1176
Keyword
Molecular Phylogeny; Phylogenomics; Mitochondria; Eukaryote tree of life
National Category
Biological Systematics Evolutionary Biology
Research subject
Biology with specialization in Systematics; Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-231670 (URN)978-91-554-9031-7 (ISBN)
Public defence
2014-10-24, Fries salen, Evolutionsbiologiskt centrum, Norbyvägen 18, 752 36, Uppsala, 10:30 (English)
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Supervisors
Available from: 2014-10-02 Created: 2014-09-09 Last updated: 2015-01-23

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He, DingFu, Cheng-JieBaldauf, Sandra L.

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