Cargando…

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 re...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4053784/
https://www.ncbi.nlm.nih.gov/pubmed/23375108
http://dx.doi.org/10.1186/gb-2013-14-2-r11
_version_ 1782320438956785664
author 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
author_facet 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
author_sort Clarke, Michael
collection PubMed
description 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.
format Online
Article
Text
id pubmed-4053784
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-40537842014-06-12 Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling 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 Genome Biol Research 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. BioMed Central 2013 2013-02-01 /pmc/articles/PMC4053784/ /pubmed/23375108 http://dx.doi.org/10.1186/gb-2013-14-2-r11 Text en Copyright © 2013 Clarke et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
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
Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title_full Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title_fullStr Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title_full_unstemmed Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title_short Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
title_sort genome of acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4053784/
https://www.ncbi.nlm.nih.gov/pubmed/23375108
http://dx.doi.org/10.1186/gb-2013-14-2-r11
work_keys_str_mv AT clarkemichael genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT lohanamandaj genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT liubernard genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT lagkouvardosilias genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT royscott genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT zafarnikhat genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT bertelliclaire genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT schildechristina genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT kianianmomeniarash genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT burglinthomasr genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT frechchristian genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT turcottebernard genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT kopecklauso genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT synnottjohnm genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT choocaleb genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT paponovivan genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT finkleraliza genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT hengtanchrissoon genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT hutchinsandrewp genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT weinmeierthomas genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT ratteithomas genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT chujefferysc genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT gimenezgregory genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT irimiamanuel genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT rigdendanielj genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT fitzpatrickdavida genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT lorenzomoralesjacob genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT batemanalex genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT chiuchenghsun genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT tangpetrus genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT hegemannpeter genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT frommhillel genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT raoultdidier genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT greubgilbert genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT mirandasaavedradiego genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT chennansheng genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT nashpiers genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT gingermichaell genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT hornmatthias genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT schaappauline genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT calerlis genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling
AT loftusbrendanj genomeofacanthamoebacastellaniihighlightsextensivelateralgenetransferandearlyevolutionoftyrosinekinasesignaling