The distinctive flagellar proteome of Euglena gracilis illuminates the complexities of protistan flagella adaptation

Michael Hammond; Martin Zoltner; Jack Garrigan; Erin Butterfield; Vladimir Varga; Julius Lukeš; Mark C. Field

doi:10.1111/nph.17638

The distinctive flagellar proteome of Euglena gracilis illuminates the complexities of protistan flagella adaptation

Michael Hammond, Martin Zoltner, Jack Garrigan, Erin Butterfield, Vladimir Varga, Julius Lukeš, Mark C. Field (Lead / Corresponding author)

Biological Chemistry and Drug Discovery

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

14 Citations (Scopus)

305 Downloads (Pure)

Abstract

• The eukaryotic flagellum/cilium is a prominent organelle with conserved structure and diverse functions. Euglena gracilis, a photosynthetic and highly adaptable protist, employs its flagella for both locomotion and environmental sensing.

• Using proteomics of isolated E. gracilis flagella we identify nearly 1700 protein groups, which challenges previous estimates of the protein complexity of motile eukaryotic flagella.

• We identified several unexpected similarities shared with mammalian flagella, including an entire glycolytic pathway and proteasome but also document a vast array of flagella-based signal transduction components that coordinate gravitaxis and phototactic motility. By contrast the pellicle was found to consist of over 900 protein groups, containing additional structural and signaling components.

• Our data identify significant adaptations within the E. gracilis flagellum, many of which are clearly linked to the highly flexible lifestyle.

Original language	English
Pages (from-to)	1323-1336
Number of pages	14
Journal	New Phytologist
Volume	232
Issue number	3
Early online date	22 Jul 2021
DOIs	https://doi.org/10.1111/nph.17638
Publication status	Published - Nov 2021

Keywords

cilia
Euglena
evolution
flagella
pellicle
proteomics

ASJC Scopus subject areas

Physiology
Plant Science

Access to Document

10.1111/nph.17638Licence: CC BY

Final Published VersionFinal published version, 2.29 MBLicence: CC BY

A Systems Approach for Understanding Cell Surface Dynamics in Trypanosomes (Investigator Award)
Field, M. (Investigator)
1/10/17 → 31/03/24
Project: Research
Global Mechanisms for Control of the Trypanosome Proteome: Defining the Composition, Origins and Roles of Cullin E3 Ligases
Field, M. (Investigator)
Medical Research Council
1/01/17 → 31/12/19
Project: Research

Fingerprints Proteomics Facility
Centre for Advanced Scientific Technologies
Facility/equipment: Facility

Cite this

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title = "The distinctive flagellar proteome of Euglena gracilis illuminates the complexities of protistan flagella adaptation",

abstract = "• The eukaryotic flagellum/cilium is a prominent organelle with conserved structure and diverse functions. Euglena gracilis, a photosynthetic and highly adaptable protist, employs its flagella for both locomotion and environmental sensing.• Using proteomics of isolated E. gracilis flagella we identify nearly 1700 protein groups, which challenges previous estimates of the protein complexity of motile eukaryotic flagella.• We identified several unexpected similarities shared with mammalian flagella, including an entire glycolytic pathway and proteasome but also document a vast array of flagella-based signal transduction components that coordinate gravitaxis and phototactic motility. By contrast the pellicle was found to consist of over 900 protein groups, containing additional structural and signaling components.• Our data identify significant adaptations within the E. gracilis flagellum, many of which are clearly linked to the highly flexible lifestyle.",

keywords = "cilia, Euglena, evolution, flagella, pellicle, proteomics",

author = "Michael Hammond and Martin Zoltner and Jack Garrigan and Erin Butterfield and Vladimir Varga and Julius Luke{\v s} and Field, {Mark C.}",

note = "This work was supported by grants from the Wellcome Trust (204697/Z/16/Z to MCF), the Medical Research Council (MR/P009018/1 to MCF), the Czech Science Foundation (18-15962S to JL), ERC CZ LL1601 (to JL), the ERD project OPVVV 16_019/0000759 (to JL and MZ), and the Gordon and Betty Moore Foundation (to JL). We thank Eva Lacov{\'a} Dob{\'a}kov{\'a} for provision of Euglena gracilis images shown in Fig. 6, as well as ThankGod Ebenezer (EBI, Cambridge) for early contributions towards sequence analysis of the flagellum fraction, Lael Barlow (University of Dundee) for phylogenetic advice, Alan Prescott (University of Dundee) for his support with electron microscopy and also Douglas Lamont and the Fingerprints team in Dundee for excellent proteomic support.",

year = "2021",

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doi = "10.1111/nph.17638",

language = "English",

volume = "232",

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journal = "New Phytologist",

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AU - Zoltner, Martin

AU - Garrigan, Jack

AU - Butterfield, Erin

AU - Varga, Vladimir

AU - Lukeš, Julius

AU - Field, Mark C.

N1 - This work was supported by grants from the Wellcome Trust (204697/Z/16/Z to MCF), the Medical Research Council (MR/P009018/1 to MCF), the Czech Science Foundation (18-15962S to JL), ERC CZ LL1601 (to JL), the ERD project OPVVV 16_019/0000759 (to JL and MZ), and the Gordon and Betty Moore Foundation (to JL). We thank Eva Lacová Dobáková for provision of Euglena gracilis images shown in Fig. 6, as well as ThankGod Ebenezer (EBI, Cambridge) for early contributions towards sequence analysis of the flagellum fraction, Lael Barlow (University of Dundee) for phylogenetic advice, Alan Prescott (University of Dundee) for his support with electron microscopy and also Douglas Lamont and the Fingerprints team in Dundee for excellent proteomic support.

PY - 2021/11

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N2 - • The eukaryotic flagellum/cilium is a prominent organelle with conserved structure and diverse functions. Euglena gracilis, a photosynthetic and highly adaptable protist, employs its flagella for both locomotion and environmental sensing.• Using proteomics of isolated E. gracilis flagella we identify nearly 1700 protein groups, which challenges previous estimates of the protein complexity of motile eukaryotic flagella.• We identified several unexpected similarities shared with mammalian flagella, including an entire glycolytic pathway and proteasome but also document a vast array of flagella-based signal transduction components that coordinate gravitaxis and phototactic motility. By contrast the pellicle was found to consist of over 900 protein groups, containing additional structural and signaling components.• Our data identify significant adaptations within the E. gracilis flagellum, many of which are clearly linked to the highly flexible lifestyle.

AB - • The eukaryotic flagellum/cilium is a prominent organelle with conserved structure and diverse functions. Euglena gracilis, a photosynthetic and highly adaptable protist, employs its flagella for both locomotion and environmental sensing.• Using proteomics of isolated E. gracilis flagella we identify nearly 1700 protein groups, which challenges previous estimates of the protein complexity of motile eukaryotic flagella.• We identified several unexpected similarities shared with mammalian flagella, including an entire glycolytic pathway and proteasome but also document a vast array of flagella-based signal transduction components that coordinate gravitaxis and phototactic motility. By contrast the pellicle was found to consist of over 900 protein groups, containing additional structural and signaling components.• Our data identify significant adaptations within the E. gracilis flagellum, many of which are clearly linked to the highly flexible lifestyle.

KW - cilia

KW - Euglena

KW - evolution

KW - flagella

KW - pellicle

KW - proteomics

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DO - 10.1111/nph.17638

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The distinctive flagellar proteome of Euglena gracilis illuminates the complexities of protistan flagella adaptation

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Fingerprint

Projects

A Systems Approach for Understanding Cell Surface Dynamics in Trypanosomes (Investigator Award)

Global Mechanisms for Control of the Trypanosome Proteome: Defining the Composition, Origins and Roles of Cullin E3 Ligases

Equipment

Fingerprints Proteomics Facility

Cite this