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Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling

Michael Clarke1, Amanda J Lohan1, Bernard Liu2, Ilias Lagkouvardos3, Scott Roy4, Nikhat Zafar5, Claire Bertelli6, Christina Schilde7, Arash Kianianmomeni8, Thomas R Bürglin9, Christian Frech10, Bernard Turcotte11, Klaus O Kopec12, John M Synnott1, Caleb Choo10, Ivan Paponov13, Aliza Finkler14, Chris Soon Heng Tan15, Andrew P Hutchins16, Thomas Weinmeier17, Thomas Rattei17, Jeffery SC Chu18, Gregory Gimenez19, Manuel Irimia20, Daniel J Rigden21, David A Fitzpatrick22, Jacob Lorenzo-Morales23, Alex Bateman24, Cheng-Hsun Chiu25, Petrus Tang26, Peter Hegemann8, Hillel Fromm14, Didier Raoult19, Gilbert Greub6, Diego Miranda-Saavedra16, Nansheng Chen10, Piers Nash27, Michael L Ginger28, Matthias Horn3, Pauline Schaap7, Lis Caler5 and Brendan J Loftus1*

Author affiliations

1 Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland

2 Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Ave, Room 1081 Toronto, Ontario M5G 1X5, Canada

3 Department für Mikrobielle Ökologie, Universität Wien, Althanstr. 14, A-1090 Wien, Austria

4 Department of Biology, San Francisco State University, 1600 Holloway Ave, San Francisco, CA 94132, USA

5 Bioinformatics Department, J Craig Venter Institute, Inc., 9704 Medical Center DriveRockville, MD 20850, USA

6 Center for Research on Intracellular Bacteria, Institute of Microbiology, Institute of Microbiology, Rue du Bugnon 48, 1011 Lausanne, Switzerland

7 College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK

8 Institute of Biology, Experimental Biophysics, Humboldt-Universität zu Berlin, Invalidenstrasse 42, D-10115 Berlin, Germany

9 Department of Biosciences and Nutrition and Center for Biosciences, Karolinska Institutet, Hälsovägen 7, Novum, SE 141 83 Huddinge, Sweden

10 Department of Molecular Biology and Biochemistry, Simon Fraser University, 8888 University Drive, Burnaby, BC V5A 1S6, Canada

11 Department of Medicine, McGill University, McIntyre Medical Building, 3655 Sir William Osler, Montreal, Quebec H3G 1Y6, Canada

12 Max Planck Institute for Developmental Biology, Spemannstr. 35 - 39, 72076 Tübingen, Germany

13 Institut für Biologie II/Molecular Plant Physiology, Faculty of Biology, Albert-Ludwigs University of Freiburg, Freiburg, Germany

14 Department of Plant Sciences, Britannia 04, Tel-Aviv University, Tel-Aviv 69978, Israel

15 CeMM-Research Center for Molecular Medicine of the Austrian Academy of Sciences, Lazarettgasse 14, AKH BT 25.3, A-1090 Vienna, Austria

16 World Premier International (WPI) Immunology Frontier Research Center (IFReC), Osaka University, 3-1 Yamadaoka, Suita, 565-0871 Osaka, Japan

17 Department für Computational Systems Biology, Universität Wien, Althanstraße 14, 1090 Wien, Austria

18 Department of Medical Genetics, Medical Genetics, C201 - 4500 Oak Street, Vancouver, BC, V6H 3N1, Canada

19 Unité des rickettsies, IFR 48, CNRS-IRD UMR 6236, Faculté de médecine, Université de la Méditerranée, Marseille, France

20 Banting and Best Department of Medical Research, Donnelly Centre, University of Toronto, 160 College Street, Room 230,Toronto, Ontario M5S 3E1, Canada

21 Institute of Integrative Biology, Biosciences Building, University of Liverpool, Crown Street, Liverpool L69 7ZB, UK

22 Department of Biology, NUI Maynooth, Co Kildare, Ireland

23 University Institute of Tropical Diseases and Public Health of the Canary Islands, University of La Laguna, Avda. Astrofísico Fco. Sánchez, S/N 38203 La Laguna, Tenerife, Canary Islands, Spain

24 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK

25 Divisions of Pediatric Infectious Diseases, Department of Pediatrics, Chang Gung Children's Hospital and Chang Gung Memorial Hospital, Taoyuan, Taiwan

26 Department of Parasitology, Chang Gung University, Taoyuan, Taiwan

27 Ben May Department for Cancer Research and Committee on Cancer Biology, The University of Chicago, Chicago, IL 60637, USA

28 Faculty of Health and Medicine, Division of Biomedical and Life Sciences, Lancaster University, Lancaster, LA1 4YQ, UK

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Citation and License

Genome Biology 2013, 14:R11  doi:10.1186/gb-2013-14-2-r11

Published: 1 February 2013

Abstract

Background

The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its genomic diversity remains largely unsampled. Here we present an analysis of a whole genome assembly of Acanthamoeba castellanii (Ac) the first representative from a solitary free-living amoebozoan.

Results

Ac encodes 15,455 compact intron-rich genes, a significant number of which are predicted to have arisen through inter-kingdom lateral gene transfer (LGT). A majority of the LGT candidates have undergone a substantial degree of intronization and Ac appears to have incorporated them into established transcriptional programs. Ac manifests a complex signaling and cell communication repertoire, including a complete tyrosine kinase signaling toolkit and a comparable diversity of predicted extracellular receptors to that found in the facultatively multicellular dictyostelids. An important environmental host of a diverse range of bacteria and viruses, Ac utilizes a diverse repertoire of predicted pattern recognition receptors, many with predicted orthologous functions in the innate immune systems of higher organisms.

Conclusions

Our analysis highlights the important role of LGT in the biology of Ac and in the diversification of microbial eukaryotes. The early evolution of a key signaling facility implicated in the evolution of metazoan multicellularity strongly argues for its emergence early in the Unikont lineage. Overall, the availability of an Ac genome should aid in deciphering the biology of the Amoebozoa and facilitate functional genomic studies in this important model organism and environmental host.