Transcriptome, proteome and draft genome of Euglena gracilis

Thankgod Ebenezer; Martin Zoltner; Alana Burrell; Anna Nenarokova; Anna M. G. Novák Vanclová; Binod Prasad; Petr Soukal; Carlos Santana-Molina; Ellis O'Neill; Nerissa N. Nankissoor; Nithya Vadakedath; Viktor Daiker; Samson Obado; Sara Silva-Pereira; Andrew P. Jackson; Damien P. Devos; Julius Lukeš; Michael Lebert; Sue Vaughan; Vladimir Hampl; Mark Carrington; Michael L. Ginger; Joel B. Dacks; Steven Kelly; Mark Field

doi:10.1186/s12915-019-0626-8

Transcriptome, proteome and draft genome of Euglena gracilis

Thankgod Ebenezer, Martin Zoltner, Alana Burrell, Anna Nenarokova, Anna M. G. Novák Vanclová, Binod Prasad, Petr Soukal, Carlos Santana-Molina, Ellis O'Neill, Nerissa N. Nankissoor, Nithya Vadakedath, Viktor Daiker, Samson Obado, Sara Silva-Pereira, Andrew P. Jackson, Damien P. Devos, Julius Lukeš, Michael Lebert, Sue Vaughan, Vladimir HamplMark Carrington, Michael L. Ginger, Joel B. Dacks (Lead / Corresponding author), Steven Kelly (Lead / Corresponding author), Mark Field (Lead / Corresponding author)

Biological Chemistry and Drug Discovery

Research output: Contribution to journal › Article › peer-review

95 Citations (Scopus)

226 Downloads (Pure)

Abstract

Background: Photosynthetic euglenids are major contributors to fresh water ecosystems. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue has
hampered both basic research and translational efforts.

Results: We report a detailed transcriptome and partial genome for E. gracilis Z1. The nuclear genome is estimated to be around 500 Mb in size, and the transcriptome encodes over 36,000 proteins and the genome possesses less than 1% coding sequence. Annotation of coding sequences indicates a highly sophisticated endomembrane system, RNA
processing mechanisms and nuclear genome contributions from several photosynthetic lineages. Multiple gene families, including likely signal transduction components, have been massively expanded. Alterations in protein abundance are controlled post-transcriptionally between light and dark conditions, surprisingly similar to trypanosomatids.

Conclusions: Our data provide evidence that a range of photosynthetic eukaryotes contributed to the Euglena nuclear genome, evidence in support of the ‘shopping bag’ hypothesis for plastid acquisition. We also suggest that euglenids possess unique regulatory mechanisms for achieving extreme adaptability, through mechanisms of paralog expansion and gene acquisition.

Original language	English
Article number	11
Pages (from-to)	1-23
Number of pages	23
Journal	BMC Biology
Volume	17
DOIs	https://doi.org/10.1186/s12915-019-0626-8
Publication status	Published - 7 Feb 2019

Keywords

Cellular evolution
Euglena gracilis
Excavata
Gene architecture
Horizontal gene transfer
Plastid
Secondary endosymbiosis
Splicing
Transcriptome

ASJC Scopus subject areas

Biotechnology
Structural Biology
Ecology, Evolution, Behavior and Systematics
Physiology
General Biochemistry,Genetics and Molecular Biology
General Agricultural and Biological Sciences
Plant Science
Developmental Biology
Cell Biology

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10.1186/s12915-019-0626-8Licence: CC BY

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© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Final published version, 2.65 MBLicence: CC BY

Cite this

Ebenezer, T., Zoltner, M., Burrell, A., Nenarokova, A., Novák Vanclová, A. M. G., Prasad, B., Soukal, P., Santana-Molina, C., O'Neill, E., Nankissoor, N. N., Vadakedath, N., Daiker, V., Obado, S., Silva-Pereira, S., Jackson, A. P., Devos, D. P., Lukeš, J., Lebert, M., Vaughan, S., ... Field, M. (2019). Transcriptome, proteome and draft genome of Euglena gracilis. BMC Biology, 17, 1-23. Article 11. https://doi.org/10.1186/s12915-019-0626-8

@article{39643b8fbdde4902aef35418e34ab4af,

title = "Transcriptome, proteome and draft genome of Euglena gracilis",

abstract = "Background: Photosynthetic euglenids are major contributors to fresh water ecosystems. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue hashampered both basic research and translational efforts.Results: We report a detailed transcriptome and partial genome for E. gracilis Z1. The nuclear genome is estimated to be around 500 Mb in size, and the transcriptome encodes over 36,000 proteins and the genome possesses less than 1% coding sequence. Annotation of coding sequences indicates a highly sophisticated endomembrane system, RNAprocessing mechanisms and nuclear genome contributions from several photosynthetic lineages. Multiple gene families, including likely signal transduction components, have been massively expanded. Alterations in protein abundance are controlled post-transcriptionally between light and dark conditions, surprisingly similar to trypanosomatids.Conclusions: Our data provide evidence that a range of photosynthetic eukaryotes contributed to the Euglena nuclear genome, evidence in support of the {\textquoteleft}shopping bag{\textquoteright} hypothesis for plastid acquisition. We also suggest that euglenids possess unique regulatory mechanisms for achieving extreme adaptability, through mechanisms of paralog expansion and gene acquisition.",

keywords = "Cellular evolution, Euglena gracilis, Excavata, Gene architecture, Horizontal gene transfer, Plastid, Secondary endosymbiosis, Splicing, Transcriptome",

author = "Thankgod Ebenezer and Martin Zoltner and Alana Burrell and Anna Nenarokova and {Nov{\'a}k Vanclov{\'a}}, {Anna M. G.} and Binod Prasad and Petr Soukal and Carlos Santana-Molina and Ellis O'Neill and Nankissoor, {Nerissa N.} and Nithya Vadakedath and Viktor Daiker and Samson Obado and Sara Silva-Pereira and Jackson, {Andrew P.} and Devos, {Damien P.} and Julius Luke{\v s} and Michael Lebert and Sue Vaughan and Vladimir Hampl and Mark Carrington and Ginger, {Michael L.} and Dacks, {Joel B.} and Steven Kelly and Mark Field",

note = "This work was supported by the Yousef Jameel Academic Program (through the Yousef Jameel PhD Scholarship), the Cambridge Commonwealth, European and International Trust, the Cambridge University Student Registry, the Cambridge Philosophical Society (all to TEE), the Medical Research Council (Grant #: P009018/1 to MCF), and German Aerospace Center - DLR, Cologne, on the behalf of Federal Ministry of Education and Research (BMBF), Germany (Grant no: 50WB1128 and 50WB1528 to ML), the European Research Council CZ LL1601 BFU2013-40866-P (to DPD) and the Czech Ministry of Education, Youth and Sports - National Sustainability Program II (Project BIOCEV-FAR) LQ 1604, by the project BIOCEV (CZ.1.05/1.1.00/02.0109), by the Centre for research of pathogenicity and virulence of parasites CZ.02.1.01/0.0/0.0/16_019/0000759 and by the Czech Science Foundation project nr. 16-25280S (to VH, AV and PS). ",

year = "2019",

month = feb,

day = "7",

doi = "10.1186/s12915-019-0626-8",

language = "English",

volume = "17",

pages = "1--23",

journal = "BMC Biology",

issn = "1741-7007",

publisher = "Springer Verlag",

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Ebenezer, T, Zoltner, M, Burrell, A, Nenarokova, A, Novák Vanclová, AMG, Prasad, B, Soukal, P, Santana-Molina, C, O'Neill, E, Nankissoor, NN, Vadakedath, N, Daiker, V, Obado, S, Silva-Pereira, S, Jackson, AP, Devos, DP, Lukeš, J, Lebert, M, Vaughan, S, Hampl, V, Carrington, M, Ginger, ML, Dacks, JB, Kelly, S & Field, M 2019, 'Transcriptome, proteome and draft genome of Euglena gracilis', BMC Biology, vol. 17, 11, pp. 1-23. https://doi.org/10.1186/s12915-019-0626-8

TY - JOUR

T1 - Transcriptome, proteome and draft genome of Euglena gracilis

AU - Ebenezer, Thankgod

AU - Zoltner, Martin

AU - Burrell, Alana

AU - Nenarokova, Anna

AU - Novák Vanclová, Anna M. G.

AU - Prasad, Binod

AU - Soukal, Petr

AU - Santana-Molina, Carlos

AU - O'Neill, Ellis

AU - Nankissoor, Nerissa N.

AU - Vadakedath, Nithya

AU - Daiker, Viktor

AU - Obado, Samson

AU - Silva-Pereira, Sara

AU - Jackson, Andrew P.

AU - Devos, Damien P.

AU - Lukeš, Julius

AU - Lebert, Michael

AU - Vaughan, Sue

AU - Hampl, Vladimir

AU - Carrington, Mark

AU - Ginger, Michael L.

AU - Dacks, Joel B.

AU - Kelly, Steven

AU - Field, Mark

N1 - This work was supported by the Yousef Jameel Academic Program (through the Yousef Jameel PhD Scholarship), the Cambridge Commonwealth, European and International Trust, the Cambridge University Student Registry, the Cambridge Philosophical Society (all to TEE), the Medical Research Council (Grant #: P009018/1 to MCF), and German Aerospace Center - DLR, Cologne, on the behalf of Federal Ministry of Education and Research (BMBF), Germany (Grant no: 50WB1128 and 50WB1528 to ML), the European Research Council CZ LL1601 BFU2013-40866-P (to DPD) and the Czech Ministry of Education, Youth and Sports - National Sustainability Program II (Project BIOCEV-FAR) LQ 1604, by the project BIOCEV (CZ.1.05/1.1.00/02.0109), by the Centre for research of pathogenicity and virulence of parasites CZ.02.1.01/0.0/0.0/16_019/0000759 and by the Czech Science Foundation project nr. 16-25280S (to VH, AV and PS).

PY - 2019/2/7

Y1 - 2019/2/7

N2 - Background: Photosynthetic euglenids are major contributors to fresh water ecosystems. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue hashampered both basic research and translational efforts.Results: We report a detailed transcriptome and partial genome for E. gracilis Z1. The nuclear genome is estimated to be around 500 Mb in size, and the transcriptome encodes over 36,000 proteins and the genome possesses less than 1% coding sequence. Annotation of coding sequences indicates a highly sophisticated endomembrane system, RNAprocessing mechanisms and nuclear genome contributions from several photosynthetic lineages. Multiple gene families, including likely signal transduction components, have been massively expanded. Alterations in protein abundance are controlled post-transcriptionally between light and dark conditions, surprisingly similar to trypanosomatids.Conclusions: Our data provide evidence that a range of photosynthetic eukaryotes contributed to the Euglena nuclear genome, evidence in support of the ‘shopping bag’ hypothesis for plastid acquisition. We also suggest that euglenids possess unique regulatory mechanisms for achieving extreme adaptability, through mechanisms of paralog expansion and gene acquisition.

AB - Background: Photosynthetic euglenids are major contributors to fresh water ecosystems. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue hashampered both basic research and translational efforts.Results: We report a detailed transcriptome and partial genome for E. gracilis Z1. The nuclear genome is estimated to be around 500 Mb in size, and the transcriptome encodes over 36,000 proteins and the genome possesses less than 1% coding sequence. Annotation of coding sequences indicates a highly sophisticated endomembrane system, RNAprocessing mechanisms and nuclear genome contributions from several photosynthetic lineages. Multiple gene families, including likely signal transduction components, have been massively expanded. Alterations in protein abundance are controlled post-transcriptionally between light and dark conditions, surprisingly similar to trypanosomatids.Conclusions: Our data provide evidence that a range of photosynthetic eukaryotes contributed to the Euglena nuclear genome, evidence in support of the ‘shopping bag’ hypothesis for plastid acquisition. We also suggest that euglenids possess unique regulatory mechanisms for achieving extreme adaptability, through mechanisms of paralog expansion and gene acquisition.

KW - Cellular evolution

KW - Euglena gracilis

KW - Excavata

KW - Gene architecture

KW - Horizontal gene transfer

KW - Plastid

KW - Secondary endosymbiosis

KW - Splicing

KW - Transcriptome

UR - http://www.scopus.com/inward/record.url?scp=85061200138&partnerID=8YFLogxK

U2 - 10.1186/s12915-019-0626-8

DO - 10.1186/s12915-019-0626-8

M3 - Article

C2 - 30732613

SN - 1741-7007

VL - 17

SP - 1

EP - 23

JO - BMC Biology

JF - BMC Biology

M1 - 11

ER -

Transcriptome, proteome and draft genome of Euglena gracilis

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Transcriptome, proteome and draft genome of Euglena gracilis

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