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

Michael Clarke, Amanda J. Lohan, Bernard Liu, Ilias Lagkouvardos, Scott Roy, Nikhat Zafar, Claire Bertelli, Christina Schilde, Arash Kianianmomeni, Thomas R. Bürglin, Christian Frech, Bernard Turcotte, Klaus O. Kopec, John M. Synnott, Caleb Choo, Ivan Paponov, Aliza Finkler, Chris Soon Heng Tan, Andrew P. Hutchins, Thomas Weinmeier & 22 others Thomas Rattei, Jeffery S.C. Chu, Gregory Gimenez, Manuel Irimia, Daniel J. Rigden, David A. Fitzpatrick, Jacob Lorenzo-Morales, Alex Bateman, Cheng Hsun Chiu, Petrus Tang, Peter Hegemann, Hillel Fromm, Didier Raoult, Gilbert Greub, Diego Miranda-Saavedra, Nansheng Chen, Piers Nash, Michael L. Ginger, Matthias Horn, Pauline Schaap, Lis Caler, Brendan J. Loftus

Research output: Contribution to journalArticle

151 Citations (Scopus)

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.

LanguageEnglish
Article numberR11
JournalGenome Biology
Volume14
Issue number2
DOIs
Publication statusPublished - 1 Feb 2013
Externally publishedYes

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Acanthamoeba castellanii
Horizontal Gene Transfer
gene transfer
Protein-Tyrosine Kinases
tyrosine
phosphotransferases (kinases)
genome
Genome
eukaryote
genomics
Amoebozoa
metazoan
pattern recognition
immune system
Eukaryota
virus
eukaryotic cells
communication
bacterium
gene

Cite this

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 S.C. ; 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. In: Genome Biology. 2013 ; Vol. 14, No. 2.
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title = "Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling",
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.",
author = "Michael Clarke and Lohan, {Amanda J.} and Bernard Liu and Ilias Lagkouvardos and Scott Roy and Nikhat Zafar and Claire Bertelli and Christina Schilde and Arash Kianianmomeni and B{\"u}rglin, {Thomas R.} and Christian Frech and Bernard Turcotte and Kopec, {Klaus O.} and Synnott, {John M.} and Caleb Choo and Ivan Paponov and Aliza Finkler and {Heng Tan}, {Chris Soon} and Hutchins, {Andrew P.} and Thomas Weinmeier and Thomas Rattei and Chu, {Jeffery S.C.} and Gregory Gimenez and Manuel Irimia and Rigden, {Daniel J.} and Fitzpatrick, {David A.} and Jacob Lorenzo-Morales and Alex Bateman and Chiu, {Cheng Hsun} and Petrus Tang and Peter Hegemann and Hillel Fromm and Didier Raoult and Gilbert Greub and Diego Miranda-Saavedra and Nansheng Chen and Piers Nash and Ginger, {Michael L.} and Matthias Horn and Pauline Schaap and Lis Caler and Loftus, {Brendan J.}",
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Clarke, M, Lohan, AJ, Liu, B, Lagkouvardos, I, Roy, S, Zafar, N, Bertelli, C, Schilde, C, Kianianmomeni, A, Bürglin, TR, Frech, C, Turcotte, B, Kopec, KO, Synnott, JM, Choo, C, Paponov, I, Finkler, A, Heng Tan, CS, Hutchins, AP, Weinmeier, T, Rattei, T, Chu, JSC, Gimenez, G, Irimia, M, Rigden, DJ, Fitzpatrick, DA, Lorenzo-Morales, J, Bateman, A, Chiu, CH, Tang, P, Hegemann, P, Fromm, H, Raoult, D, Greub, G, Miranda-Saavedra, D, Chen, N, Nash, P, Ginger, ML, Horn, M, Schaap, P, Caler, L & Loftus, BJ 2013, 'Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling', Genome Biology, vol. 14, no. 2, R11. https://doi.org/10.1186/gb-2013-14-2-r11

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 S.C.; 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.

In: Genome Biology, Vol. 14, No. 2, R11, 01.02.2013.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling

AU - Clarke, Michael

AU - Lohan, Amanda J.

AU - Liu, Bernard

AU - Lagkouvardos, Ilias

AU - Roy, Scott

AU - Zafar, Nikhat

AU - Bertelli, Claire

AU - Schilde, Christina

AU - Kianianmomeni, Arash

AU - Bürglin, Thomas R.

AU - Frech, Christian

AU - Turcotte, Bernard

AU - Kopec, Klaus O.

AU - Synnott, John M.

AU - Choo, Caleb

AU - Paponov, Ivan

AU - Finkler, Aliza

AU - Heng Tan, Chris Soon

AU - Hutchins, Andrew P.

AU - Weinmeier, Thomas

AU - Rattei, Thomas

AU - Chu, Jeffery S.C.

AU - Gimenez, Gregory

AU - Irimia, Manuel

AU - Rigden, Daniel J.

AU - Fitzpatrick, David A.

AU - Lorenzo-Morales, Jacob

AU - Bateman, Alex

AU - Chiu, Cheng Hsun

AU - Tang, Petrus

AU - Hegemann, Peter

AU - Fromm, Hillel

AU - Raoult, Didier

AU - Greub, Gilbert

AU - Miranda-Saavedra, Diego

AU - Chen, Nansheng

AU - Nash, Piers

AU - Ginger, Michael L.

AU - Horn, Matthias

AU - Schaap, Pauline

AU - Caler, Lis

AU - Loftus, Brendan J.

PY - 2013/2/1

Y1 - 2013/2/1

N2 - 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.

AB - 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.

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DO - 10.1186/gb-2013-14-2-r11

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