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

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 r...

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Vydané v:	Genome biology Ročník 14; číslo 2; s. R11
Hlavní autori:	Clarke, Michael, Lohan, Amanda J, Liu, Bernard, Lagkouvardos, Ilias, Roy, Scott, Zafar, Nikhat, Bertelli, Claire, Schilde, Christina, Kianianmomeni, Arash, Bürglin, Thomas R, Frech, Christian, Turcotte, Bernard, Kopec, Klaus O, Synnott, John M, Choo, Caleb, Paponov, Ivan, Finkler, Aliza, Heng Tan, Chris Soon, Hutchins, Andrew P, Weinmeier, Thomas, Rattei, Thomas, Chu, Jeffery SC, Gimenez, Gregory, Irimia, Manuel, Rigden, Daniel J, Fitzpatrick, David A, Lorenzo-Morales, Jacob, Bateman, Alex, Chiu, Cheng-Hsun, Tang, Petrus, Hegemann, Peter, Fromm, Hillel, Raoult, Didier, Greub, Gilbert, Miranda-Saavedra, Diego, Chen, Nansheng, Nash, Piers, Ginger, Michael L, Horn, Matthias, Schaap, Pauline, Caler, Lis, Loftus, Brendan J
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	London BioMed Central 01.02.2013
Predmet:	Acanthamoeba castellanii Acanthamoeba castellanii - genetics Amoebozoa Animal Genetics and Genomics Animalia bacteria Bioinformatics Biomedical and Life Sciences cell communication eukaryotic cells evolution Evolution, Molecular Evolutionary Biology Gene Transfer, Horizontal genes genetic variation genome assembly Genome, Protozoan genomics horizontal gene transfer Human Genetics immune system Introns Life Sciences Metazoa Microbial Genetics and Genomics Plant Genetics and Genomics Protein-Tyrosine Kinases - genetics Protein-Tyrosine Kinases - metabolism Protozoan Proteins - genetics Protozoan Proteins - metabolism receptors Signal Transduction transcription (genetics) viruses Mannose Binding Protein Acanthamoeba Castellanii Lateral Gene Transfer Tyrosine Kinase Signaling Intron Gain
ISSN:	1474-760X, 1465-6906, 1474-760X, 1465-6914
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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.
AbstractList	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. 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. 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. 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. 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. 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.BACKGROUNDThe 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.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.RESULTSAc 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.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.CONCLUSIONSOur 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.
ArticleNumber	R11
Author	Roy, Scott Lagkouvardos, Ilias Horn, Matthias Frech, Christian Fromm, Hillel Chiu, Cheng-Hsun Weinmeier, Thomas Rattei, Thomas Chen, Nansheng Nash, Piers Zafar, Nikhat Kopec, Klaus O Irimia, Manuel Choo, Caleb Rigden, Daniel J Liu, Bernard Turcotte, Bernard Heng Tan, Chris Soon Finkler, Aliza Ginger, Michael L Gimenez, Gregory Kianianmomeni, Arash Tang, Petrus Lohan, Amanda J Bürglin, Thomas R Fitzpatrick, David A Hegemann, Peter Schaap, Pauline Synnott, John M Chu, Jeffery SC Bateman, Alex Greub, Gilbert Hutchins, Andrew P Clarke, Michael Loftus, Brendan J Caler, Lis Miranda-Saavedra, Diego Bertelli, Claire Raoult, Didier Schilde, Christina Lorenzo-Morales, Jacob Paponov, Ivan
AuthorAffiliation	19 Unité des rickettsies, IFR 48, CNRS-IRD UMR 6236, Faculté de médecine, Université de la Méditerranée, Marseille, France 1 Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland 9 Department of Biosciences and Nutrition and Center for Biosciences, Karolinska Institutet, Hälsovägen 7, Novum, SE 141 83 Huddinge, Sweden 25 Divisions of Pediatric Infectious Diseases, Department of Pediatrics, Chang Gung Children's Hospital and Chang Gung Memorial Hospital, Taoyuan, Taiwan 15 CeMM-Research Center for Molecular Medicine of the Austrian Academy of Sciences, Lazarettgasse 14, AKH BT 25.3, A-1090 Vienna, Austria 6 Center for Research on Intracellular Bacteria, Institute of Microbiology, Institute of Microbiology, Rue du Bugnon 48, 1011 Lausanne, Switzerland 4 Department of Biology, San Francisco State University, 1600 Holloway Ave, San Francisco, CA 94132, USA 13 Institut für Biologie II/Molecular Plant Physiology, Faculty of Biology, Albert-Ludwigs University of Freiburg, Freiburg
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23375108$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:127155912$$DView record from Swedish Publication Index (Karolinska Institutet)
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Snippet	Background The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its... The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its genomic... Background: The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its... BACKGROUND: The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its...
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SubjectTerms	Acanthamoeba castellanii Acanthamoeba castellanii - genetics Amoebozoa Animal Genetics and Genomics Animalia bacteria Bioinformatics Biomedical and Life Sciences cell communication eukaryotic cells evolution Evolution, Molecular Evolutionary Biology Gene Transfer, Horizontal genes genetic variation genome assembly Genome, Protozoan genomics horizontal gene transfer Human Genetics immune system Introns Life Sciences Metazoa Microbial Genetics and Genomics Plant Genetics and Genomics Protein-Tyrosine Kinases - genetics Protein-Tyrosine Kinases - metabolism Protozoan Proteins - genetics Protozoan Proteins - metabolism receptors Signal Transduction transcription (genetics) viruses
Title	Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
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