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  • 1.
    Cenci, Ugo
    et al.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Sibbald, Shannon J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Curtis, Bruce A.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Kamikawa, Ryoma
    Kyoto Univ, Grad Sch Human & Environm Studies, Kyoto, Kyoto 6068501, Japan.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Moog, Daniel
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada;Philipps Univ Marburg, Cell Biol Lab, Karl von Frisch Str 8, D-35043 Marburg, Germany.
    Henrissat, Bernard
    Univ Aix Marseille, CNRS, AFMB, 163 Ave Luminy, F-13288 Marseille, France;INRA, USC AFMB 1408, F-13288 Marseille, France;King Abdulaziz Univ, Dept Biol Sci, Jeddah 21589, Saudi Arabia.
    Marechal, Eric
    Univ Grenoble Alpes, Lab Physiol Cellulaire & Vegetale, CNRS, CEA,INRA,Inst Biosci & Biotechnol Grenoble,CEA Gr, 17 Rue Martyrs, F-38000 Grenoble, France.
    Chabi, Malika
    Univ Lille 1, UMR 8576, Unite Glycobiol Struct & Fonct, F-59650 Villeneuve Dascq, France.
    Djemiel, Christophe
    Univ Lille 1, UMR 8576, Unite Glycobiol Struct & Fonct, F-59650 Villeneuve Dascq, France.
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada;Canadian Inst Adv Res, Program Integrated Microbial Biodivers, Toronto, ON, Canada.
    Kim, Eunsoo
    Amer Museum Nat Hist, Div Invertebrate Zool, Cent Pk West & 79 St, New York, NY 10024 USA;Amer Museum Nat Hist, Sackler Inst Comparat Genom, Cent Pk West & 79 St, New York, NY 10024 USA.
    Archibald, John M.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS B3H 4R2, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada;Canadian Inst Adv Res, Program Integrated Microbial Biodivers, Toronto, ON, Canada.
    Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids2018In: BMC Biology, ISSN 1741-7007, E-ISSN 1741-7007, Vol. 16, article id 137Article in journal (Refereed)
    Abstract [en]

    Background: The evolution of photosynthesis has been a major driver in eukaryotic diversification. Eukaryotes have acquired plastids (chloroplasts) either directly via the engulfment and integration of a photosynthetic cyanobacterium (primary endosymbiosis) or indirectly by engulfing a photosynthetic eukaryote (secondary or tertiary endosymbiosis). The timing and frequency of secondary endosymbiosis during eukaryotic evolution is currently unclear but may be resolved in part by studying cryptomonads, a group of single-celled eukaryotes comprised of both photosynthetic and non-photosynthetic species. While cryptomonads such as Guillardia theta harbor a red algal-derived plastid of secondary endosymbiotic origin, members of the sister group Goniomonadea lack plastids. Here, we present the genome of Goniomonas avonlea-the first for any goniomonad-to address whether Goniomonadea are ancestrally non-photosynthetic or whether they lost a plastid secondarily. Results: We sequenced the nuclear and mitochondrial genomes of Goniomonas avonlea and carried out a comparative analysis of Go. avonlea, Gu. theta, and other cryptomonads. The Go. avonlea genome assembly is similar to 92 Mbp in size, with 33,470 predicted protein-coding genes. Interestingly, some metabolic pathways (e.g., fatty acid biosynthesis) predicted to occur in the plastid and periplastidal compartment of Gu. theta appear to operate in the cytoplasm of Go. avonlea, suggesting that metabolic redundancies were generated during the course of secondary plastid integration. Other cytosolic pathways found in Go. avonlea are not found in Gu. theta, suggesting secondary loss in Gu. theta and other plastid-bearing cryptomonads. Phylogenetic analyses revealed no evidence for algal endosymbiont-derived genes in the Go. avonlea genome. Phylogenomic analyses point to a specific relationship between Cryptista (to which cryptomonads belong) and Archaeplastida. Conclusion: We found no convincing genomic or phylogenomic evidence that Go. avonlea evolved from a secondary red algal plastid-bearing ancestor, consistent with goniomonads being ancestrally non-photosynthetic eukaryotes. The Go. avonlea genome sheds light on the physiology of heterotrophic cryptomonads and serves as an important reference point for studying the metabolic "rewiring" that took place during secondary plastid integration in the ancestor of modern-day Cryptophyceae.

  • 2.
    Eme, Laura
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    The eukaryotic ancestor shapes up2018In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 562, no 7727, p. 352-354Article in journal (Other academic)
    Abstract [en]

    Asgard archaea are the closest known relatives of nucleus-bearing organisms called eukaryotes. A study indicates that these archaea have a dynamic network of actin protein - a trait thought of as eukaryote-specific.

  • 3.
    Eme, Laura
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Spang, Anja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Lombard, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Archaea and the origin of eukaryotes2017In: Nature Reviews Microbiology, ISSN 1740-1526, E-ISSN 1740-1534, Vol. 15, no 12, p. 711-723Article, review/survey (Refereed)
    Abstract [en]

    Woese and Fox's 1977 paper on the discovery of the Archaea triggered a revolution in the field of evolutionary biology by showing that life was divided into not only prokaryotes and eukaryotes. Rather, they revealed that prokaryotes comprise two distinct types of organisms, the Bacteria and the Archaea. In subsequent years, molecular phylogenetic analyses indicated that eukaryotes and the Archaea represent sister groups in the tree of life. During the genomic era, it became evident that eukaryotic cells possess a mixture of archaeal and bacterial features in addition to eukaryotic-specific features. Although it has been generally accepted for some time that mitochondria descend from endosymbiotic alphaproteobacteria, the precise evolutionary relationship between eukaryotes and archaea has continued to be a subject of debate. In this Review, we outline a brief history of the changing shape of the tree of life and examine how the recent discovery of a myriad of diverse archaeal lineages has changed our understanding of the evolutionary relationships between the three domains of life and the origin of eukaryotes. Furthermore, we revisit central questions regarding the process of eukaryogenesis and discuss what can currently be inferred about the evolutionary transition from the first to the last eukaryotic common ancestor.

  • 4.
    Gentekaki, Eleni
    et al.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.;Mae Fah Luang Univ, Sch Sci, Chiang Rai, Thailand.;Mae Fah Luang Univ, Human Gut Microbiome Hlth Res Unit, Chiang Rai, Thailand..
    Curtis, Bruce A.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada..
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada..
    Klimes, Vladimir
    Univ Ostrava, Dept Biol & Ecol, Fac Sci, Ostrava, Czech Republic..
    Elias, Marek
    Univ Ostrava, Dept Biol & Ecol, Fac Sci, Ostrava, Czech Republic..
    Salas-Leiva, Dayana E.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada..
    Herman, Emily K.
    Univ Alberta, Dept Cell Biol, Edmonton, AB, Canada..
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada..
    Arias, Maria C.
    Univ Sci & Technol Lille, Unite Glycobiol Struct & Fonct, CNRS, UMR8576,Cite Sci, Villeneuve Dascq, France..
    Henrissat, Bernard
    Aix Marseille Univ, CNRS, UMR 7257, Marseille, France.;NRA, USC 1408, AFMB, Marseille, France.;King Abdulaziz Univ, Dept Biol Sci, Jeddah, Saudi Arabia..
    Hilliou, Frederique
    Univ Cote Azur, NRA, ISA, Sophia Antipolis, France..
    Klute, Mary J.
    Univ Alberta, Dept Cell Biol, Edmonton, AB, Canada..
    Suga, Hiroshi
    Prefectural Univ Hiroshima, Fac Life & Environm Sci, Nanatsuka 562, Shobara, Hiroshima, Japan..
    Malik, Shehre-Banoo
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada..
    Pightling, Arthur W.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;US FDA, Ctr Food Safety & Appl Nutr, College Pk, MD USA..
    Kolisko, Martin
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.;Czech Acad Sci, Inst Parasitol, Ctr Biol, Ceske Budejovice, Czech Republic..
    Rachubinski, Richard A.
    Schlacht, Alexander
    Soanes, Darren M.
    Univ Exeter, Coll Life & Environm Sci, Exeter, Devon, England..
    Tsaousis, Anastasios D.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.;Univ Kent, Lab Mol & Evolutionary Parasitol, RAPID Grp, Sch Biosci, Canterbury, Kent, England..
    Archibald, John M.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.;Canadian Inst Adv Res, CIFAR Program Integrated Microbial Biodivers, Toronto, ON, Canada..
    Ball, Steven G.
    Dacks, Joel B.
    Univ Alberta, Dept Cell Biol, Edmonton, AB, Canada..
    Clark, C. Graham
    London Sch Hyg & Trop Med, Fac Infect & Trop Dis, London, England..
    van der Giezen, Mark
    Univ Exeter, Biosci, Exeter, Devon, England..
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.;Canadian Inst Adv Res, CIFAR Program Integrated Microbial Biodivers, Toronto, ON, Canada..
    Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis2017In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 15, no 9, article id e2003769Article in journal (Refereed)
    Abstract [en]

    Blastocystis is the most prevalent eukaryotic microbe colonizing the human gut, infecting approximately 1 billion individuals worldwide. Although Blastocystis has been linked to intestinal disorders, its pathogenicity remains controversial because most carriers are asymptomatic. Here, the genome sequence of Blastocystis subtype (ST) 1 is presented and compared to previously published sequences for ST4 and ST7. Despite a conserved core of genes, there is unexpected diversity between these STs in terms of their genome sizes, guanine-cytosine (GC) content, intron numbers, and gene content. ST1 has 6,544 protein-coding genes, which is several hundred more than reported for ST4 and ST7. The percentage of proteins unique to each ST ranges from 6.2% to 20.5%, greatly exceeding the differences observed within parasite genera. Orthologous proteins also display extreme divergence in amino acid sequence identity between STs (i.e., 59%-61% median identity), on par with observations of the most distantly related species pairs of parasite genera. The STs also display substantial variation in gene family distributions and sizes, especially for protein kinase and protease gene families, which could reflect differences in virulence. It remains to be seen to what extent these inter-ST differences persist at the intra-ST level. A full 26% of genes in ST1 have stop codons that are created on the mRNA level by a novel polyadenylation mechanism found only in Blastocystis. Reconstructions of pathways and organellar systems revealed that ST1 has a relatively complete membrane-trafficking system and a near-complete meiotic toolkit, possibly indicating a sexual cycle. Unlike some intestinal protistan parasites, Blastocystis ST1 has near-complete de novo pyrimidine, purine, and thiamine biosynthesis pathways and is unique amongst studied stramenopiles in being able to metabolize alpha-glucans rather than beta-glucans. It lacks all genes encoding heme-containing cytochrome P450 proteins. Predictions of the mitochondrion-related organelle (MRO) proteome reveal an expanded repertoire of functions, including lipid, cofactor, and vitamin biosynthesis, as well as proteins that may be involved in regulating mitochondrial morphology and MRO/endoplasmic reticulum (ER) interactions. In sharp contrast, genes for peroxisome-associated functions are absent, suggesting Blastocystis STs lack this organelle. Overall, this study provides an important window into the biology of Blastocystis, showcasing significant differences between STs that can guide future experimental investigations into differences in their virulence and clarifying the roles of these organisms in gut health and disease.

  • 5.
    Hess, Sebastian
    et al.
    Dalhousie Univ, Dept Biochem & Mol Biol, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada;Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada;Univ Cologne, Inst Zool, Cologne, Germany.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Dalhousie Univ, Dept Biochem & Mol Biol, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Simpson, Alastair G. B.
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada.
    A natural toroidal microswimmer with a rotary eukaryotic flagellum2019In: Nature Microbiology, E-ISSN 2058-5276, Vol. 4, no 10, p. 1620-1626Article in journal (Refereed)
    Abstract [en]

    We describe Idionectes vortex gen. nov., sp. nov., a unicellular microeukaryote that swims by continuous inversion of its surface, similar to a vortex ring. This previously unreported mode of motility approximates a hypothetical concept called the 'toroidal swimmer', in which a doughnut-shaped object rotates around its circular axis and travels in the opposite direction to its outer surface motion. During swimming, the flagellum of Idionectes rotates relative to its cell body, which is normally a hallmark of prokaryotic rather than eukaryotic flagella.

  • 6.
    Karnkowska, Anna
    et al.
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic;Univ Warsaw, Fac Biol, Biol & Chem Res Ctr, Dept Mol Phylogenet & Evolut, Warsaw, Poland.
    Treitli, Sebastian C.
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    Brzon, Ondrej
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    Novak, Lukas
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    Vacek, Vojtech
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    Soukal, Petr
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    Barlow, Lael D.
    Univ Alberta, Dept Med, Div Infect Dis, Edmonton, AB, Canada.
    Herman, Emily K.
    Univ Alberta, Dept Med, Div Infect Dis, Edmonton, AB, Canada.
    Pipaliya, Shweta, V
    Univ Alberta, Dept Med, Div Infect Dis, Edmonton, AB, Canada.
    Panek, Tomas
    Univ Ostrava, Fac Sci, Dept Biol & Ecol, Ostrava, Czech Republic.
    Zihala, David
    Univ Ostrava, Fac Sci, Dept Biol & Ecol, Ostrava, Czech Republic.
    Petrzelkova, Romana
    Univ Ostrava, Fac Sci, Dept Biol & Ecol, Ostrava, Czech Republic.
    Butenko, Anzhelika
    Univ Ostrava, Fac Sci, Dept Biol & Ecol, Ostrava, Czech Republic.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology. Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.
    Elias, Marek
    Univ Ostrava, Fac Sci, Dept Biol & Ecol, Ostrava, Czech Republic;Univ Ostrava, Fac Sci, Inst Environm Technol, Ostrava, Czech Republic.
    Dacks, Joel B.
    Univ Alberta, Dept Med, Div Infect Dis, Edmonton, AB, Canada.
    Hampl, Vladimir
    Charles Univ Prague, Fac Sci, Dept Parasitol, BIOCEV, Vestec, Czech Republic.
    The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion2019In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 10, p. 2292-2312Article in journal (Refereed)
    Abstract [en]

    The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here, we report an extensive analysis of the M. exilis genome to address this question. Unexpectedly, we find that M. exilis genome structure and content is similar in complexity to other eukaryotes and less "reduced" than genomes of some other protists from the Metamonada group to which it belongs. Furthermore, the predicted cytoskeletal systems, the organization of endomembrane systems, and biosynthetic pathways also display canonical eukaryotic complexity. The only apparent preadaptation that permitted the loss of mitochondria was the acquisition of the SUF system for Fe-S cluster assembly and the loss of glycine cleavage system. Changes in other systems, including in amino acid metabolism and oxidative stress response, were coincident with the loss of mitochondria but are likely adaptations to the microaerophilic and endobiotic niche rather than the mitochondrial loss per se. Apart from the lack of mitochondria and peroxisomes, we show that M. exilis is a fully elaborated eukaryotic cell that is a promising model system in which eukaryotic cell biology can be investigated in the absence of mitochondria.

  • 7.
    Lax, Gordon
    et al.
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada.
    Eglit, Yana
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Dalhousie Univ, Dept Biochem & Mol Biol, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Bertrand, Erin M.
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada.
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, Ctr Comparat Genom & Evolutionary Bioinformat, Halifax, NS, Canada.
    Simpson, Alastair G. B.
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biol, Halifax, NS, Canada.
    Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes2018In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 564, no 7736, p. 410-414Article in journal (Refereed)
    Abstract [en]

    Almost all eukaryote life forms have now been placed within one of five to eight supra-kingdom-level groups using molecular phylogenetics(1-4). The 'phylum' Hemimastigophora is probably the most distinctive morphologically defined lineage that still awaits such a phylogenetic assignment. First observed in the nineteenth century, hemimastigotes are free-living predatory protists with two rows of flagella and a unique cell architecture(5-7); to our knowledge, no molecular sequence data or cultures are currently available for this group. Here we report phylogenomic analyses based on high-coverage, cultivation-independent transcriptomics that place Hemimastigophora outside of all established eukaryote supergroups. They instead comprise an independent supra-kingdom-level lineage that most likely forms a sister clade to the 'Diaphoretickes' half of eukaryote diversity (that is, the 'stramenopiles, alveolates and Rhizaria' supergroup (Sar), Archaeplastida and Cryptista, as well as other major groups). The previous ranking of Hemimastigophora as a phylum understates the evolutionary distinctiveness of this group, which has considerable importance for investigations into the deep-level evolutionary history of eukaryotic life-ranging from understanding the origins of fundamental cell systems to placing the root of the tree. We have also established the first culture of a hemimastigote (Hemimastix kukwesjijk sp. nov.), which will facilitate future genomic and cellbiological investigations into eukaryote evolution and the last eukaryotic common ancestor.

  • 8.
    Leger, Michelle M.
    et al.
    UPF, CSIC, Inst Evolutionary Biol, Barcelona, Spain.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Roger, Andrew J.
    Dalhousie Univ, Ctr Comparat Genom & Evolutionary Bioinformat, Dept Biochem & Mol Biol, Halifax, NS, Canada.
    Demystifying Eukaryote Lateral Gene Transfer2018In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 40, no 5, article id 1700242Article in journal (Refereed)
    Abstract [en]

    In a recent BioEssays paper [W. F. Martin, BioEssays 2017, 39, 1700115], William Martin sharply criticizes evolutionary interpretations that involve lateral gene transfer (LGT) into eukaryotic genomes. Most published examples of LGTs in eukaryotes, he suggests, are in fact contaminants, ancestral genes that have been lost from other extant lineages, or the result of artefactual phylogenetic inferences. Martin argues that, except for transfers that occurred from endosymbiotic organelles, eukaryote LGT is insignificant. Here, in reviewing this field, we seek to correct some of the misconceptions presented therein with regard to the evidence for LGT in eukaryotes.

  • 9.
    Leger, Michelle M.
    et al.
    Dalhousie Univ, Dept Biochem & Mol Biol, 5850 Coll St,POB 15000, Halifax, NS B3H 4R2, Canada.;Univ Pompeu Fabra, CSIC, Inst Evolutionary Biol, Passeig Maritim de la Barceloneta 37-49, Barcelona 08003, Spain..
    Kolisko, Martin
    Dalhousie Univ, Dept Biochem & Mol Biol, 5850 Coll St,POB 15000, Halifax, NS B3H 4R2, Canada.;Czech Acad Sci, Biol Ctr, Inst Parasitol, Branisovska 1160-31, Ceske Budejovice 37005, Czech Republic..
    Kamikawa, Ryoma
    Kyoto Univ, Grad Sch Global Environm Studies, Grad Sch Human & Environm Studies, Sakyo Ku, Yoshida Honmachi, Kyoto 6068501, Japan..
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Dalhousie Univ, Dept Biochem & Mol Biol, 5850 Coll St,POB 15000, Halifax, NS B3H 4R2, Canada.
    Kume, Keitaro
    Univ Tsukuba, Ctr Computat Sci, Grad Sch Life & Environm Sci, 1-1-1 Tennodai, Tsukuba, Ibaraki 3058572, Japan..
    Cepicka, Ivan
    Charles Univ Prague, Fac Sci, Dept Zool, Vinicna 7, CR-12844 Prague 2, Czech Republic..
    Silberman, Jeffrey D.
    Univ Arkansas, Dept Biol Sci, Fayetteville, AR 72701 USA..
    Andersson, Jan O.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Xu, Feifei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Yabuki, Akinori
    Japan Agcy Marine Earth Sci & Technol JAMSTEC, 2-15 Natsushima Cho, Yokosuka, Kanagawa 2370061, Japan..
    Eme, Laura
    Dalhousie Univ, Dept Biochem & Mol Biol, 5850 Coll St,POB 15000, Halifax, NS B3H 4R2, Canada.
    Zhang, Qianqian
    Chinese Acad Sci, Yantai Inst Coastal Zone Res, 17 Chunhui Rd, Yantai 264003, Shandong, Peoples R China..
    Takishita, Kiyotaka
    Japan Agcy Marine Earth Sci & Technol JAMSTEC, 2-15 Natsushima Cho, Yokosuka, Kanagawa 2370061, Japan..
    Inagaki, Yuji
    Univ Tsukuba, Ctr Computat Sci, Grad Sch Life & Environm Sci, 1-1-1 Tennodai, Tsukuba, Ibaraki 3058572, Japan.;Univ Tsukuba, Ctr Computat Sci, 1-1-1 Tennodai, Tsukuba, Ibaraki 3058577, Japan..
    Simpson, Alastair G. B.
    Dalhousie Univ, Dept Biol, 1355 Oxford St,POB 15000, Halifax, NS B3H 4R2, Canada..
    Hashimoto, Tetsuo
    Univ Tsukuba, Ctr Computat Sci, Grad Sch Life & Environm Sci, 1-1-1 Tennodai, Tsukuba, Ibaraki 3058572, Japan.;Univ Tsukuba, Ctr Computat Sci, 1-1-1 Tennodai, Tsukuba, Ibaraki 3058577, Japan..
    Roger, Andrew J.
    Dalhousie Univ, Dept Biochem & Mol Biol, 5850 Coll St,POB 15000, Halifax, NS B3H 4R2, Canada..
    Organelles that illuminate the origins of Trichomonas hydrogenosomes and Giardia mitosomes2017In: NATURE ECOLOGY & EVOLUTION, ISSN 2397-334X, Vol. 1, no 4, article id UNSP 0092Article in journal (Refereed)
    Abstract [en]

    Many anaerobic microbial parasites possess highly modified mitochondria known as mitochondrion-related organelles (MROs). The best-studied of these are the hydrogenosomes of Trichomonas vaginalis and Spironucleus salmonicida, which produce ATP anaerobically through substrate-level phosphorylation with concomitant hydrogen production; and the mitosomes of Giardia intestinalis, which are functionally reduced and lack any role in ATP production. Howewer, to understand the metabolic specializations that these MROs underwent in adaptation to parasitism, data from their free-living relatives are needed. Here, we present a large-scale comparative transcriptomic study of MROs across a major eukaryotic group, Metamonada, examining lineage-specific gain and loss of metabolic functions in the MROs of Trichomonas, Giardia, Spironucleus and their free-living relatives. Our analyses uncover a complex history of ATP production machinery in diplomonads such as Giardia, and their closest relative, Dysnectes; and a correlation between the glycine cleavage machinery and lifestyles. Our data further suggest the existence of a previously undescribed biochemical class of MRO that generates hydrogen but is incapable of ATP synthesis.

  • 10.
    Raina, Jean-Baptiste
    et al.
    Univ Technol Sydney, Climate Change Cluster, Ultimo, NSW, Australia.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Pollock, F. Joseph
    Penn State Univ, Dept Biol, Eberly Coll Sci, University Pk, PA USA.
    Spang, Anja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. NIOZ, Royal Netherlands Inst Sea Res, Dept Marine Microbiol & Biogeochem, Netherlands; Univ Utrecht, Netherlands.
    Archibald, John M.
    Dalhousie Univ, Dept Biochem & Mol Biol, Halifax, NS, Canada.
    Williams, Tom A.
    Univ Bristol, Sch Biol Sci, Bristol, Avon, England.
    Symbiosis in the microbial world: from ecology to genome evolution2018In: BIOLOGY OPEN, ISSN 2046-6390, Vol. 7, no 2, article id UNSP bio032524Article, review/survey (Refereed)
    Abstract [en]

    The concept of symbiosis - defined in 1879 by de Bary as 'the living together of unlike organisms' - has a rich and convoluted history in biology. In part, because it questioned the concept of the individual, symbiosis fell largely outside mainstream science and has traditionally received less attention than other research disciplines. This is gradually changing. In nature organisms do not live in isolation but rather interact with, and are impacted by, diverse beings throughout their life histories. Symbiosis is now recognized as a central driver of evolution across the entire tree of life, including, for example, bacterial endosymbionts that provide insects with vital nutrients and the mitochondria that power our own cells. Symbioses between microbes and their multicellular hosts also underpin the ecological success of some of the most productive ecosystems on the planet, including hydrothermal vents and coral reefs. In November 2017, scientists working in fields spanning the life sciences came together at a Company of Biologists' workshop to discuss the origin, maintenance, and long-term implications of symbiosis from the complementary perspectives of cell biology, ecology, evolution and genomics, taking into account both model and non-model organisms. Here, we provide a brief synthesis of the fruitful discussions that transpired.

  • 11.
    Seitz, Kiley W.
    et al.
    Univ Texas Austin, Dept Marine Sci, Port Aransas, TX 78373 USA.
    Dombrowski, Nina
    Univ Texas Austin, Dept Marine Sci, Port Aransas, TX 78373 USA;Royal Netherlands Inst Sea Res, NIOZ, NL-1797 SZ Den Burg, Netherlands;Univ Utrecht, NL-1797 SZ Den Burg, Netherlands.
    Eme, Laura
    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 Paris Sud, Unite Ecol Systemat & Evolut, CNRS, F-91400 Orsay, France.
    Spang, Anja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Royal Netherlands Inst Sea Res, NIOZ, NL-1797 SZ Den Burg, Netherlands;Univ Utrecht, NL-1797 SZ Den Burg, Netherlands.
    Lombard, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Sieber, Jessica R.
    Univ Minnesota, Duluth, MN 55812 USA.
    Teske, Andreas P.
    Univ N Carolina, Dept Marine Sci, Chapel Hill, NC 27599 USA.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Wageningen Univ, Dept Agrotechnol & Food Sci, Lab Microbiol, NL-6708 WE Wageningen, Netherlands.
    Baker, Brett J.
    Univ Texas Austin, Dept Marine Sci, Port Aransas, TX 78373 USA.
    Asgard archaea capable of anaerobic hydrocarbon cycling2019In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 10, article id 1822Article in journal (Refereed)
    Abstract [en]

    Large reservoirs of natural gas in the oceanic subsurface sustain complex communities of anaerobic microbes, including archaeal lineages with potential to mediate oxidation of hydrocarbons such as methane and butane. Here we describe a previously unknown archaeal phylum, Helarchaeota, belonging to the Asgard superphylum and with the potential for hydrocarbon oxidation. We reconstruct Helarchaeota genomes from metagenomic data derived from hydrothermal deep-sea sediments in the hydrocarbon-rich Guaymas Basin. The genomes encode methyl-CoM reductase-like enzymes that are similar to those found in butane-oxidizing archaea, as well as several enzymes potentially involved in alkyl-CoA oxidation and the Wood-Ljungdahl pathway. We suggest that members of the Helarchaeota have the potential to activate and subsequently anaerobically oxidize hydrothermally generated short-chain hydrocarbons.

  • 12.
    Spang, Anja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Royal Netherlands Inst Sea Res, Dept Marine Microbiol & Biogeochem, NIOZ, Den Burg, Netherlands.; Univ Utrecht, Den Burg, Netherlands.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Saw, Jimmy H.
    Oregon State Univ, Dept Microbiol, Corvallis, OR USA.
    Fernández Cáceres, Eva
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Zaremba-Niedzwiedzka, Katarzyna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Lombard, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Guy, Lionel
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Asgard archaea are the closest prokaryotic relatives of eukaryotes2018In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 3, article id e1007080Article in journal (Other academic)
  • 13.
    Spang, Anja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Stairs, Courtney W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Dombrowski, Nina
    NIOZ, Royal Netherlands Inst Sea Res, Dept Marine Microbiol & Biogeochem, Ab Den Burg, Netherlands;Univ Utrecht, Ab Den Burg, Netherlands;Univ Texas Austin, Inst Marine Sci, Dept Marine Sci, Port Aransas, TX USA.
    Eme, Laura
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Lombard, Jonathan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Caceres, Eva F.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Greening, Chris
    Monash Univ, Sch Biol Sci, Clayton, Vic, Australia.
    Baker, BrettJ
    Univ Texas Austin, Inst Marine Sci, Dept Marine Sci, Port Aransas, TX USA.
    Ettema, Thijs J. G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism2019In: Nature Microbiology, E-ISSN 2058-5276, Vol. 4, no 7, p. 1138-1148Article in journal (Refereed)
    Abstract [en]

    The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. Current research suggests that eukaryotes evolved from a merger between a host of archaeal descent and an alphaproteobacterial endosymbiont. The discovery of the Asgard archaea, a proposed archaeal superphylum that includes Lokiarchaeota, Thorarchaeota, Odinarchaeota and Heimdallarchaeota suggested to comprise the closest archaeal relatives of eukaryotes, has helped to elucidate the identity of the putative archaeal host. Whereas Lokiarchaeota are assumed to employ a hydrogen-dependent metabolism, little is known about the metabolic potential of other members of the Asgard superphylum. We infer the central metabolic pathways of Asgard archaea using comparative genomics and phylogenetics to be able to refine current models for the origin of eukaryotes. Our analyses indicate that Thorarchaeota and Lokiarchaeota encode proteins necessary for carbon fixation via the Wood-Ljungdahl pathway and for obtaining reducing equivalents from organic substrates. By contrast, Heimdallarchaeum LC2 and LC3 genomes encode enzymes potentially enabling the oxidation of organic substrates using nitrate or oxygen as electron acceptors. The gene repertoire of Heimdallarchaeum AB125 and Odinarchaeum indicates that these organisms can ferment organic substrates and conserve energy by coupling ferredoxin reoxidation to respiratory proton reduction. Altogether, our genome analyses suggest that Asgard representatives are primarily organoheterotrophs with variable capacity for hydrogen consumption and production. On this basis, we propose the 'reverse flow model', an updated symbiogenetic model for the origin of eukaryotes that involves electron or hydrogen flow from an organoheterotrophic archaeal host to a bacterial symbiont.

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