Downloaded from NCBI Under Ancestral Mirnas

Total Page:16

File Type:pdf, Size:1020Kb

Downloaded from NCBI Under Ancestral Mirnas bioRxiv preprint doi: https://doi.org/10.1101/076190; this version posted September 28, 2016. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Bråte et al., 20 09 2016 – preprint copy - BioRxiv Pre-metazoan origin of animal miRNAs Jon Bråtea,1, Ralf S. Neumanna,b,1, Bastian Frommc, Arthur A. B. Haraldsena, Paul E. Grinia, Kamran Shalchian-Tabrizia,2 a Centre for Epigenetics, Development and Evolution (CEDE) and Centre for Integrative Microbial Evolution (CIME), Section for Genetics and Evolutionary Biology (EVOGENE), University of Oslo, Norway. b Institute of Clinical Medicine, Department of Immunology, University of Oslo, Norway. c Department of Tumor Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, Norway. 1 Contributed equally 2 Corresponding author: [email protected] Abstract microRNAs (miRNAs) are integrated parts of the developmental toolkit in animals. The evolutionary history and origins of animal miRNAs is however unclear, and it is not known when they evolved and on how many occasions. We have therefore investigated the presence of miRNAs and the necessary miRNA biogenesis machinery in a large group of unicellular relatives of animals, Ichthyosporea. By small RNA sequencing we find evidence for at least four genes in the genus Sphaeroforma that satisfy the criteria for the annotation of animal miRNA genes. Three of these miRNAs are conserved and expressed across sphaeroformid species. Furthermore, we identify homologues of the animal miRNA biogenesis genes across a wide range of ichthyosporeans, including Drosha and Pasha which make up the animal specific Microprocessor complex. Taken together we report the first evidence for bona fide miRNA genes and the presence of the miRNA-processing pathway in unicellular Choanozoa, implying that the origin of animal miRNAs and the Microprocessor complex predates multicellular animals. Keywords: miRNA, animal evolution, Sphaeroforma, Ichthyosporea, Holozoa Introduction induced silencing complex (RISC), while the other strand (the microRNAs (miRNAs) are short (20-26 nucleotides) RNA molecules passenger, or star strand) is degraded. Gene regulation takes place via that are involved in gene regulation (Fromm, 2016). They are found in a the RISC and the central component, the Argonaute (AGO) protein that wide variety of organisms including plants, viruses and animals but binds the mature miRNA. Target messenger RNAs (mRNAs) are current evidence does not support a common evolutionary history identified by basepairing between the loaded miRNAs and the mRNA, (Tarver et al., 2012; Cerutti and Casas-Mollano, 2006; Shabalina and and translation of the mRNA is either fully blocked or down regulated. Koonin, 2016). In animals, miRNAs are essential components of the In animals, miRNA genes have been found even in the early gene regulatory machinery and highly important for processes like cell diverging animal lineages such as sponges (Grimson et al., 2008; differentiation and development (Mello and Conte, 2004). Furthermore, Robinson et al., 2013; Liew et al., 2016; Wheeler et al., 2009). In fact, because of the increase of distinct miRNA families during animal only two animal lineages are known to be missing miRNAs, the evolution (combined with lineage specific expansions and rare losses), ctenophores and Placozoa (Maxwell et al. 2012; Grimson et al. 2008; miRNAs have been linked to the evolution of morphological Moroz et al. 2014). However, due to the lack of homologous miRNA complexity in animals (Berezikov, 2011; Wheeler et al., 2009; Kosik, sequences in the basal branching animals, it has been hypothesized that 2010; Fromm et al., 2013; Erwin et al., 2011; Philippe et al., 2011). miRNA genes in animals arose several times independently (Tarver et Mainly based on the absence of miRNAs in single-celled ancestors, it al., 2012). Although, except from one study sequencing the small RNA has even been proposed that miRNAs were one of the key factors that content of the choanoflagellate Monosiga brevicollis (Grimson et al. allowed multicellular animals to evolve (Grimson et al., 2008; Wheeler 2008), almost nothing is known about the presence of miRNA genes, or et al., 2009; Mattick, 2004). the biogenesis machinery, in the unicellular relatives of animals. Generally, the primary transcripts of miRNA genes (pri- Here, we therefore investigate whether miRNA genes miRNA) can be very long RNA molecules that contain hairpin coevolved with animal multicellularity or if these genes were present structures (Axtell et al. 2011; Ameres & Zamore 2013; Chang et al. already in the unicellular ancestors of animals, the choanozoans. We 2015). In animals, the so-called Microprocessor complex (Han et al., address this question by deep sequencing of smallRNAs from species 2006), comprising the RNase III enzyme Drosha and the double- belonging to Ichthyosporea; a basal group at the split between animals stranded RNA (dsRNA) -binding protein Pasha (known as DGCR8 in and fungi, and search for the animal miRNA biogenesis machinery in humans), subsequently excises the hairpin structures (creating the pre- all unicellular relatives of animals. Our results show the existence of six miRNA). In contrast, plants do not possess Drosha or Pasha proteins; miRNA genes in Sphaeroforma that fulfill all criteria for the annotation here, several copies of the nuclear RNase III protein Dicer fulfills the of metazoan miRNAs (Fromm et al., 2015). Three of the miRNAs are role of the Microprocessor. In both animals and plants, the loop region highly conserved and expressed across three species, which strongly of the hairpin pre-miRNA is subsequently removed by Dicer proteins, indicate that the genes have important and similar function. In addition, albeit dicing takes place in the cytoplasm and nucleus, respectively, we show that the genomes of several species of Ichthyosporea, covering resulting in a 20-26 nt dsRNA molecule. Typically, only one of these the genera Sphaeroforma, Creolimax, Pirum, Abeoforma and strands (known as the mature strand) is then loaded into the RNA- 1 bioRxiv preprint doi: https://doi.org/10.1101/076190; this version posted September 28, 2016. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Bråte et al., 20 09 2016 – preprint copy - BioRxiv Amoebidium contain homologs of the animal Pasha and Drosha genes additional miRNAs were found in S. sirkka. Because there is no genome as well as Dicer, Exportin 5 and AGO. available for S. napiecek we could not run the miRNA prediction tools Altogether we present an evolutionary scenario where the as for the other species. But we could identify five of the S. arctica pre- common ancestor of Choanozoa and animals (Holozoan ancestor) miRNAs among the expressed mRNAs (even though the pri-miRNA is already possessed the animal miRNA biogenesis pathway, including transcribed by RNA polymerase II, and hence is poly-adenylated, it Drosha and Pasha, as well as bona fide miRNAs. This implies that both might not be present among the mRNAs because of rapid processing by the animal miRNAs and the Microprocessor pre-date the origin of Drosha and Dicer). These pre-miRNAs also had small RNA reads animals and that the last common ancestor of animals likely used mapping to the same locations as the mature and star strands in S. miRNAs for gene regulation. arctica, except for the star region of Sar-Mir-Nov-3 and 5. The pre- miRNAs were highly conserved between the three species with most Results mutations in the loop region which does not affect the gene targeting. But there were also a few minor differences in the mature and star Sphaeroforma species have bona fide miRNA genes strands, most notably in Sar-Mir-Nov-2. None of the novel miRNAs had any detectable homologs outside of Ichthyosporea. Initially, our small RNA sequencing and bioinformatics pipeline The miRNA genes are either located in intergenic regions or identified six miRNA genes in Sphaeroforma arctica (Figure 1 and in the introns and UTRs of protein-coding genes (Figure S1). In S. Supplementary File 1). Five of the miRNAs fulfilled all of the recently arctica Sar-Mir-Nov-1, 3, 5 and 6 are encoded in intergenic regions and proposed criteria for the annotation of miRNA genes (Fromm et al., transcribed as > 1kb unspliced pri-miRNA fragments with a well- 2015); at least two 20-26 nt RNA strands are expressed from each of the defined TSS, except for Sar-Mir-Nov-3 which is lacking a TSS but this two arms that are derived from a hairpin precursor with 2-nt offsets is probably an artifact of the genome assembly. Interestingly, the region (note that the 1nt Drosha-offset of Sar-Mir-Nov-3 and the 1nt Dicer- covering the Sar-Mir-Nov-5 pri-miRNA is transcribed also from the offset of Sar-Mir-Nov-5 are both likely due to the low number of reads opposite strand which could represent a potential novel long non-coding in general and correspondingly lower read-counts of the star sequence). RNA with binding capacity to the miRNA (an miRNA sponge) as no Further, the reads on both arms show no or very little variation of their protein-coding gene is annotated in the region. Sar-Mir-Nov-2 and Sar- 5’ start positions (5’ homogeneity) and we observe at least 16 Mir-Nov-4 are encoded within protein coding genes, in the intron and complementary nucleotides between the two arms. We include here Sar- the 3’-UTR respectively (Figure S1). These miRNAs are not transcribed Mir-Nov-6, although the star strand is not expressed and thus Dicer or from a separate TSS, but instead co-transcribed with the protein-coding Drosha offsets cannot be assessed because it shows high expression, a gene and subsequently processed into the mature miRNAs.
Recommended publications
  • Multigene Eukaryote Phylogeny Reveals the Likely Protozoan Ancestors of Opis- Thokonts (Animals, Fungi, Choanozoans) and Amoebozoa
    Accepted Manuscript Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opis- thokonts (animals, fungi, choanozoans) and Amoebozoa Thomas Cavalier-Smith, Ema E. Chao, Elizabeth A. Snell, Cédric Berney, Anna Maria Fiore-Donno, Rhodri Lewis PII: S1055-7903(14)00279-6 DOI: http://dx.doi.org/10.1016/j.ympev.2014.08.012 Reference: YMPEV 4996 To appear in: Molecular Phylogenetics and Evolution Received Date: 24 January 2014 Revised Date: 2 August 2014 Accepted Date: 11 August 2014 Please cite this article as: Cavalier-Smith, T., Chao, E.E., Snell, E.A., Berney, C., Fiore-Donno, A.M., Lewis, R., Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa, Molecular Phylogenetics and Evolution (2014), doi: http://dx.doi.org/10.1016/ j.ympev.2014.08.012 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. 1 1 Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts 2 (animals, fungi, choanozoans) and Amoebozoa 3 4 Thomas Cavalier-Smith1, Ema E. Chao1, Elizabeth A. Snell1, Cédric Berney1,2, Anna Maria 5 Fiore-Donno1,3, and Rhodri Lewis1 6 7 1Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
    [Show full text]
  • Protist Phylogeny and the High-Level Classification of Protozoa
    Europ. J. Protistol. 39, 338–348 (2003) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/ejp Protist phylogeny and the high-level classification of Protozoa Thomas Cavalier-Smith Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK; E-mail: [email protected] Received 1 September 2003; 29 September 2003. Accepted: 29 September 2003 Protist large-scale phylogeny is briefly reviewed and a revised higher classification of the kingdom Pro- tozoa into 11 phyla presented. Complementary gene fusions reveal a fundamental bifurcation among eu- karyotes between two major clades: the ancestrally uniciliate (often unicentriolar) unikonts and the an- cestrally biciliate bikonts, which undergo ciliary transformation by converting a younger anterior cilium into a dissimilar older posterior cilium. Unikonts comprise the ancestrally unikont protozoan phylum Amoebozoa and the opisthokonts (kingdom Animalia, phylum Choanozoa, their sisters or ancestors; and kingdom Fungi). They share a derived triple-gene fusion, absent from bikonts. Bikonts contrastingly share a derived gene fusion between dihydrofolate reductase and thymidylate synthase and include plants and all other protists, comprising the protozoan infrakingdoms Rhizaria [phyla Cercozoa and Re- taria (Radiozoa, Foraminifera)] and Excavata (phyla Loukozoa, Metamonada, Euglenozoa, Percolozoa), plus the kingdom Plantae [Viridaeplantae, Rhodophyta (sisters); Glaucophyta], the chromalveolate clade, and the protozoan phylum Apusozoa (Thecomonadea, Diphylleida). Chromalveolates comprise kingdom Chromista (Cryptista, Heterokonta, Haptophyta) and the protozoan infrakingdom Alveolata [phyla Cilio- phora and Miozoa (= Protalveolata, Dinozoa, Apicomplexa)], which diverged from a common ancestor that enslaved a red alga and evolved novel plastid protein-targeting machinery via the host rough ER and the enslaved algal plasma membrane (periplastid membrane).
    [Show full text]
  • The Evolution of Multicellularity and Early Animal Genomes Nina M Brooke and Peter WH Hollandã
    599 The evolution of multicellularity and early animal genomes Nina M Brooke and Peter WH Hollandà Several independent molecular datasets, including complete although some expressed sequence tag screens have mtDNA sequence, indicate that Choanozoa are most closely commenced (Hydra EST Database: http://hampson- related to multicellular animals. There is still confusion pc2.ics.uci.edu/blast/jf/; [1,2]) and gene-expression data concerning basal animal phylogeny, although recent data are accumulating (for cnidarians, these are being indicate that Placozoa are not degenerate cnidarians and hence assembled into a web-accessible database [3]). (along with sponges) occupy a pivotal position. The transition in evolution from diploblast to bilaterian animals is becoming better Models and mechanisms understood, with gene expression data arguing that cnidarians Some organisational principles are shared by different have forerunners of the anteroposterior and dorsoventral body groups of multicellular organisms, such as division of axes, and even a putative homologue of mesoderm. The labour, differentiation and cell communication. Wolpert homeobox and kinase gene families have been further analysed and Szathmary [4] propose that development from a single in basal animals, although more data are required to enable cell is an additional feature shared by all those multicellular detailed comparison with Bilateria. organisms that evolved complexity and diversity. Their reasoning is that an egg creates a genetic bottleneck in Addresses development, removing the potential for conflict between Department of Zoology, University of Oxford, South Parks Road, somatic cells, and allowing coordination to evolve. Oxford OX1 3PS, UK Ãe-mail: [email protected] When we consider molecular mechanisms responsible for that coordination, however, there is no reason to Current Opinion in Genetics & Development 2003, 13:599–603 suspect there will be much similarity between different multicellular lineages.
    [Show full text]
  • Phylogenomics Invokes the Clade Housing Cryptista, Archaeplastida, and Microheliella Maris
    bioRxiv preprint doi: https://doi.org/10.1101/2021.08.29.458128; this version posted August 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Phylogenomics invokes the clade housing Cryptista, 2 Archaeplastida, and Microheliella maris. 3 4 Euki Yazaki1, †, *, Akinori Yabuki2, †, *, Ayaka Imaizumi3, Keitaro Kume4, Tetsuo Hashimoto5,6, 5 and Yuji Inagaki6,7 6 7 1: RIKEN iTHEMS, Wako, Saitama 351-0198, Japan 8 2: Japan Agency for Marine-Earth Science and Technology, Yokosuka, Kanagawa 236-0001, 9 Japan 10 3: College of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan. 11 4: Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki, 305-8575, Japan 12 5: Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305- 13 8572, Japan 14 6: Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 15 Ibaraki, 305-8572, Japan 16 7: Center for Computational Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, 17 Japan 18 19 †EY and AY equally contributed to this work. 20 *Correspondence addressed to Euki Yazaki: [email protected] and Akinori Yabuki: 21 [email protected] 22 23 Running title: The clade housing Cryptista, Archaeplastida, and Microheliella maris. 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.29.458128; this version posted August 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
    [Show full text]
  • Evaluating Evidence from Fossils and Molecular Clocks
    Downloaded from http://cshperspectives.cshlp.org/ on August 1, 2014 - Published by Cold Spring Harbor Laboratory Press On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks Laura Eme, Susan C. Sharpe, Matthew W. Brown and Andrew J. Roger Cold Spring Harb Perspect Biol 2014; doi: 10.1101/cshperspect.a016139 Subject Collection The Origin and Evolution of Eukaryotes On the Age of Eukaryotes: Evaluating Evidence Protein Targeting and Transport as a Necessary from Fossils and Molecular Clocks Consequence of Increased Cellular Complexity Laura Eme, Susan C. Sharpe, Matthew W. Brown, Maik S. Sommer and Enrico Schleiff et al. The Persistent Contributions of RNA to Eukaryotic Origins: How and When Was the Eukaryotic Gen(om)e Architecture and Cellular Mitochondrion Acquired? Function Anthony M. Poole and Simonetta Gribaldo Jürgen Brosius The Archaeal Legacy of Eukaryotes: A Origin of Spliceosomal Introns and Alternative Phylogenomic Perspective Splicing Lionel Guy, Jimmy H. Saw and Thijs J.G. Ettema Manuel Irimia and Scott William Roy How Natural a Kind Is ''Eukaryote?'' Protein and DNA Modifications: Evolutionary W. Ford Doolittle Imprints of Bacterial Biochemical Diversification and Geochemistry on the Provenance of Eukaryotic Epigenetics L. Aravind, A. Maxwell Burroughs, Dapeng Zhang, et al. What Was the Real Contribution of The Eukaryotic Tree of Life from a Global Endosymbionts to the Eukaryotic Nucleus? Phylogenomic Perspective Insights from Photosynthetic Eukaryotes Fabien Burki David Moreira and Philippe Deschamps Bioenergetic Constraints on the Evolution of The Dispersed Archaeal Eukaryome and the Complex Life Complex Archaeal Ancestor of Eukaryotes Nick Lane Eugene V. Koonin and Natalya Yutin Origin and Evolution of Plastids and Origins of Eukaryotic Sexual Reproduction Photosynthesis in Eukaryotes Ursula Goodenough and Joseph Heitman Geoffrey I.
    [Show full text]
  • Molecular Phylogeny of Choanoflagellates, the Sister Group to Metazoa
    Molecular phylogeny of choanoflagellates, the sister group to Metazoa M. Carr*†, B. S. C. Leadbeater*‡, R. Hassan‡§, M. Nelson†, and S. L. Baldauf†¶ʈ †Department of Biology, University of York, Heslington, York, YO10 5YW, United Kingdom; and ‡School of Biosciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, United Kingdom Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved August 28, 2008 (received for review February 28, 2008) Choanoflagellates are single-celled aquatic flagellates with a unique family. Members of the Acanthoecidae family (Norris 1965) are morphology consisting of a cell with a single flagellum surrounded by characterized by the most distinct periplast morphology. This a ‘‘collar’’ of microvilli. They have long interested evolutionary biol- consists of a complex basket-like lorica constructed in a precise and ogists because of their striking resemblance to the collared cells highly reproducible manner from ribs (costae) composed of rod- (choanocytes) of sponges. Molecular phylogeny has confirmed a close shaped silica strips (Fig. 1 E and F) (13). The Acanthoecidae family relationship between choanoflagellates and Metazoa, and the first is further subdivided into nudiform (Fig. 1E) and tectiform (Fig. 1F) choanoflagellate genome sequence has recently been published. species, based on the morphology of the lorica, the stage in the cell However, molecular phylogenetic studies within choanoflagellates cycle when the silica strips are produced, the location at which the are still extremely limited. Thus, little is known about choanoflagel- strips are stored, and the mode of cell division [supporting infor- late evolution or the exact nature of the relationship between mation (SI) Text] (14).
    [Show full text]
  • Multigene Phylogeny of Choanozoa and the Origin of Animals
    Multigene Phylogeny of Choanozoa and the Origin of Animals Kamran Shalchian-Tabrizi1*, Marianne A. Minge2, Mari Espelund2, Russell Orr1, Torgeir Ruden3, Kjetill S. Jakobsen2, Thomas Cavalier-Smith4 1 Microbial Evolution Research Group, Department of Biology, University of Oslo, Oslo, Norway, 2 Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, Norway, 3 Scientific Computer Group, Center for Information Technology Services, University of Oslo, Oslo, Norway, 4 Department of Zoology, University of Oxford, Oxford, United Kingdom Abstract Animals are evolutionarily related to fungi and to the predominantly unicellular protozoan phylum Choanozoa, together known as opisthokonts. To establish the sequence of events when animals evolved from unicellular ancestors, and understand those key evolutionary transitions, we need to establish which choanozoans are most closely related to animals and also the evolutionary position of each choanozoan group within the opisthokont phylogenetic tree. Here we focus on Ministeria vibrans, a minute bacteria-eating cell with slender radiating tentacles. Single-gene trees suggested that it is either the closest unicellular relative of animals or else sister to choanoflagellates, traditionally considered likely animal ancestors. Sequencing thousands of Ministeria protein genes now reveals about 14 with domains of key significance for animal cell biology, including several previously unknown from deeply diverging Choanozoa, e.g. domains involved in hedgehog, Notch and tyrosine kinase signaling
    [Show full text]
  • David López Escardó
    Unveiling new molecular Opisthokonta diversity: A perspective from evolutionary genomics David López Escardó TESI DOCTORAL UPF / ANY 2017 DIRECTOR DE LA TESI Dr. Iñaki Ruiz Trillo DEPARTAMENT DE CIÈNCIES EXPERIMENTALS I DE LA SALUT ii Acknowledgements: Aquesta tesi va començar el dia que, mirant grups on poguer fer el projecte de màster, vaig trobar la web d'un grup de recerca que treballaven amb uns microorganismes, desconeguts per mi en aquell moment, per entendre l'origen dels animals. Tres o quatre assignatures de micro a la carrera, i cap d'elles tractava a fons amb protistes i menys els parents unicel·lulars dels animals. En fi, "Bitxos" raros, origen dels animals... em va semblar interessant. Així que em vaig presentar al despatx del Iñaki vestit amb el tratge de comercial de Tecnocasa, per veure si podia fer les pràctiques del Màster amb ells. El primer que vaig volguer remarcar durant l'entrevista és que no pretenia anar amb tratge a la feina, que no es pensés que jo de normal vaig tan seriós... Sigui com sigui, després de rumiar-s'ho, em va dir que endavant i em va emplaçar a fer una posterior entrevista amb els diferents membres del lab perquè tries un projecte de màster. Per tant, aquí el meu primer agraïment i molt gran, al Iñaki, per permetre'm, no només fer el màster, sinó també permetre'm fer aquesta tesis al seu laboratori. També per la llibertat alhora de triar projectes i per donar-li al MCG un ambient cordial on hi dóna gust treballar. Gràcies, doncs, per deixar-me entrar al món científic per la porta de la protistologia, la genòmica i l'evolució, que de ben segur m'acompanyaran sempre.
    [Show full text]
  • Intracellular Infection of Diverse Diatoms by an Evolutionary Distinct Relative of the Fungi
    Current Biology, Volume 29 Supplemental Information Intracellular Infection of Diverse Diatoms by an Evolutionary Distinct Relative of the Fungi Aurélie Chambouvet, Adam Monier, Finlay Maguire, Sarah Itoïz, Javier del Campo, Philippe Elies, Bente Edvardsen, Wenche Eikreim, and Thomas A. Richards 89/0.98 4 Apusozoa AY835680 (IAFDv24) uncultured ‘fungus’ 81/0.98 8 Choanoflagellida 63/0.81 34/0.86 MF190551 Syssomonas multiformis L42528 Corallochytrium limacisporum 78/0.98 KX420739 Ministeria vibrans 29/0.76 AF349564 Capsaspora owczarzaki 37/0.5 MF190553 Pigoraptor chileana Opisthokonta 100/0.99 MF190552 Pigoraptor vietnamica 25/- incertae sedis 100/1 AY692319 Amphibiocystidium ranae 50/- AF118851 Rhinosporidium seeberi AF192386 Pseudoperkinsus tapetis 100/1 Y19155 Amoebidium parasiticum 53/- 100/0.8 AY336711 Enterobryus sp. CMJ-2003 60/- 11 Nucleariidae/Fonticula group 47/0.99 111 Blastocladio-/Chytridio-/Mucoro-/Zoopagomycota/Dikarya 100/1 KU983765 Amoeboaphelidium sp. WZ01 72/- JX507298 Amoeboaphelidium protococcarum 32/- 78/- FJ157332 (kor-110904-24) uncultured eukaryote 87/1 JX967274 Amoeboaphelidium sp. PML-2014 98/0.99 KC315807 (KRL03E06) uncultured eukaryote 82/0.99 KX465218 (OL48) uncultured ‘fungus’ KJ566931 Aphelidium aff. melosirae P-1 Chy_NCLC1_01 Chy_445_01 Chy_445_02 99/0.99 KY129663 Aphelidium tribonemae Aphelidea 80/0.99 0 1 2 3 0 1 2 3 0 1 2 3 AB468642 (S08B08) uncultured ‘fungus’ EU154992 (KD14-BASS) uncultured ‘fungus’ AB468595 (S04B04) uncultured ‘fungus’ AB468654 (S08B20) uncultured ‘fungus’ AB468643 (S08B09) uncultured
    [Show full text]
  • The Evolution of the GPCR Signaling System in Eukaryotes: Modularity, Conservation, and the Transition to Metazoan Multicellularity
    GBE The Evolution of the GPCR Signaling System in Eukaryotes: Modularity, Conservation, and the Transition to Metazoan Multicellularity Alex de Mendoza1,2, Arnau Sebe´-Pedro´ s1,2,andIn˜ aki Ruiz-Trillo1,2,3,* 1Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra) Passeig Marı´tim de la Barceloneta, Barcelona, Spain 2Departament de Gene`tica, Universitat de Barcelona, Spain Downloaded from 3Institucio´ Catalana de Recerca i Estudis Avanc¸ats (ICREA) Passeig Lluı´s Companys, Barcelona, Spain *Corresponding author: E-mail: [email protected], [email protected]. Accepted: February 19, 2014 http://gbe.oxfordjournals.org/ Abstract The G-protein-coupled receptor (GPCR) signaling system is one of the main signaling pathways in eukaryotes. Here, we analyze the evolutionary history of all its components, from receptors to regulators, to gain a broad picture of its system-level evolution. Using eukaryotic genomes covering most lineages sampled to date, we find that the various components of the GPCR signaling pathway evolved independently, highlighting the modular nature of this system. Our data show that some GPCR families, G proteins, and regulators of G proteins diversified through lineage-specific diversifications and recurrent domain shuffling. Moreover, most of the at Centro de Información y Documentación Científica on May 25, 2015 gene families involved in the GPCR signaling system were already present in the last common ancestor of eukaryotes. Furthermore, we show that the unicellular ancestor of Metazoa already had most of the cytoplasmic components of the GPCR signaling system, including, remarkably, all the G protein alpha subunits, which are typical of metazoans.
    [Show full text]
  • Marine Biological Laboratory) Data Are All from EST Analyses
    TABLE S1. Data characterized for this study. rDNA 3 - - Culture 3 - etK sp70cyt rc5 f1a f2 ps22a ps23a Lineage Taxon accession # Lab sec61 SSU 14 40S Actin Atub Btub E E G H Hsp90 M R R T SUM Cercomonadida Heteromita globosa 50780 Katz 1 1 Cercomonadida Bodomorpha minima 50339 Katz 1 1 Euglyphida Capsellina sp. 50039 Katz 1 1 1 1 4 Gymnophrea Gymnophrys sp. 50923 Katz 1 1 2 Cercomonadida Massisteria marina 50266 Katz 1 1 1 1 4 Foraminifera Ammonia sp. T7 Katz 1 1 2 Foraminifera Ovammina opaca Katz 1 1 1 1 4 Gromia Gromia sp. Antarctica Katz 1 1 Proleptomonas Proleptomonas faecicola 50735 Katz 1 1 1 1 4 Theratromyxa Theratromyxa weberi 50200 Katz 1 1 Ministeria Ministeria vibrans 50519 Katz 1 1 Fornicata Trepomonas agilis 50286 Katz 1 1 Soginia “Soginia anisocystis” 50646 Katz 1 1 1 1 1 5 Stephanopogon Stephanopogon apogon 50096 Katz 1 1 Carolina Tubulinea Arcella hemisphaerica 13-1310 Katz 1 1 2 Cercomonadida Heteromita sp. PRA-74 MBL 1 1 1 1 1 1 1 7 Rhizaria Corallomyxa tenera 50975 MBL 1 1 1 3 Euglenozoa Diplonema papillatum 50162 MBL 1 1 1 1 1 1 1 1 8 Euglenozoa Bodo saltans CCAP1907 MBL 1 1 1 1 1 5 Alveolates Chilodonella uncinata 50194 MBL 1 1 1 1 4 Amoebozoa Arachnula sp. 50593 MBL 1 1 2 Katz lab work based on genomic PCRs and MBL (Marine Biological Laboratory) data are all from EST analyses. Culture accession number is ATTC unless noted. GenBank accession numbers for new sequences (including paralogs) are GQ377645-GQ377715 and HM244866-HM244878.
    [Show full text]
  • On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks
    Downloaded from http://cshperspectives.cshlp.org/ on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks Laura Eme, Susan C. Sharpe, Matthew W. Brown1, and Andrew J. Roger Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax B3H 4R2, Canada Correspondence: [email protected] Our understanding of the phylogenetic relationships among eukaryotic lineages has im- proved dramatically over the few past decades thanks to the development of sophisticated phylogenetic methods and models of evolution, in combination with the increasing avail- ability of sequence data for a variety of eukaryotic lineages. Concurrently, efforts have been made to infer the age of major evolutionary events along the tree of eukaryotes using fossil- calibrated molecular clock-based methods. Here, we review the progress and pitfalls in estimating the age of the last eukaryotic common ancestor (LECA) and major lineages. After reviewing previous attempts to date deep eukaryote divergences, we present the results of a Bayesian relaxed-molecular clock analysis of a large dataset (159 proteins, 85 taxa) using 19 fossil calibrations. We show that for major eukaryote groups estimated dates of divergence, as well as their credible intervals, are heavily influenced by the relaxed molec- ular clock models and methods used, and by the nature and treatment of fossil calibrations. Whereas the estimated age of LECA varied widely, ranging from 1007 (943–1102) Ma to 1898 (1655–2094) Ma, all analyses suggested that the eukaryotic supergroups subsequently diverged rapidly (i.e., within 300 Ma of LECA).
    [Show full text]