Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis

Courtney W. Stairs; Laura Eme; Sergio A. Muñoz-Gómez; Alejandro Cohen; Graham Dellaire; Jennifer N. Shepherd; James P. Fawcett; Andrew J. Roger

doi:10.7554/eLife.34292

Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis

Courtney W. Stairs, Laura Eme, Sergio A. Muñoz-Gómez, Alejandro Cohen, Graham Dellaire, Jennifer N. Shepherd, James P. Fawcett, Andrew J. Roger

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

49 Citations (Scopus)

Abstract

Under hypoxic conditions, some organisms use an electron transport chain consisting of only complex I and II (CII) to generate the proton gradient essential for ATP production. In these cases, CII functions as a fumarate reductase that accepts electrons from a low electron potential quinol, rhodoquinol (RQ). To clarify the origins of RQ-mediated fumarate reduction in eukaryotes, we investigated the origin and function of rquA, a gene encoding an RQ biosynthetic enzyme. RquA is very patchily distributed across eukaryotes and bacteria adapted to hypoxia. Phylogenetic analyses suggest lateral gene transfer (LGT) of rquA from bacteria to eukaryotes occurred at least twice and the gene was transferred multiple times amongst protists. We demonstrate that RquA functions in the mitochondrion-related organelles of the anaerobic protist Pygsuia and is correlated with the presence of RQ. These analyses reveal the role of gene transfer in the evolutionary remodeling of mitochondria in adaptation to hypoxia.

Original language	English
Article number	e34292
Journal	eLife
Volume	7
DOIs	https://doi.org/10.7554/eLife.34292
Publication status	Published - Apr 26 2018

Bibliographical note

Funding Information:
This research, and CWS and LE, were supported by a grant from the Canadian Institutes of Health Research (CIHR) MOP 142349 awarded to AJR. CWS was also supported by the Natural Sciences and Engineering Council of Canada Canadian Graduate Studentship (NSERC-CGS-D) and the Killiam Trusts (Level 2). JNS was supported by the National Institutes of Health (award no. 1R15GM096398-01). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Institutes of Health. Work in the GD laboratory was supported by an NSERC Discovery Grant (RGPIN 05616). Work from JPF laboratory was supported by a CIHR (MOP 341174). The authors would also like to acknowledge Dr. Dale Corkery for assistance in microscopy; and Drs. Eleni Gentekaki (Mae Fah Luang University), Denis Lynn (University of Guelf), and Matthew Brown (Mississippi State University) for providing sequences; Dr. Barbara Karten (Dalhousie University) for providing equipment and expertise in lipid extractions; Dr. Melanie Dobson (Dalhousie University) for providing pGEX plasmids; and Dr. Joran Martijn for discussion on alphaproteobacterial phylogeny.

Funding Information:
This research, and CWS and LE, were supported by a grant from the Canadian Institutes of Health Research (CIHR) MOP 142349 awarded to AJR. CWS was also supported by the Natural Sciences and Engineering Council of Canada Canadian Graduate Studentship (NSERC-CGS-D) and the Killiam Trusts (Level 2). JNS was supported by the National Institutes of Health (award no. 1R15GM096398-01). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Institutes of Health. Work in the GD laboratory was supported by an NSERC Discovery Grant (RGPIN 05616). Work from JPF laboratory was supported by a CIHR (MOP 341174). The authors would also like to acknowledge Dr. Dale Corkery for assistance in microscopy; and Drs. Eleni Gentekaki (Mae Fah Luang University), Denis Lynn (University of Guelf), and Matthew Brown (Mississippi State University) for providing sequences; Dr. Barbara Karten (Dalhousie University) for providing equipment and expertise in lipid extractions; Dr. Melanie Dobson (Dalhousie University) for providing pGEX plasmids; and Dr. Joran Martijn for discussion on alphaproteobacterial phylogeny. Canadian Institutes of Health Research MOP 142349 Andrew J Roger National Institutes of Health 1R15GM096398-01 Jennifer N Shepherd Natural Sciences and Engineering Research Council of Canada NSERC-CGS-D Courtney W Stairs Killam Trusts Courtney W Stairs Courtney W Stairs Natural Sciences and Engineering Research Council of Canada RGPIN 05616 Graham Dellaire Canadian Institutes of Health MOP 341174 James P Fawcett Research.

Publisher Copyright:
© Stairs et al.

ASJC Scopus Subject Areas

General Neuroscience
General Biochemistry,Genetics and Molecular Biology
General Immunology and Microbiology

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

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10.7554/eLife.34292

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title = "Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis",

abstract = "Under hypoxic conditions, some organisms use an electron transport chain consisting of only complex I and II (CII) to generate the proton gradient essential for ATP production. In these cases, CII functions as a fumarate reductase that accepts electrons from a low electron potential quinol, rhodoquinol (RQ). To clarify the origins of RQ-mediated fumarate reduction in eukaryotes, we investigated the origin and function of rquA, a gene encoding an RQ biosynthetic enzyme. RquA is very patchily distributed across eukaryotes and bacteria adapted to hypoxia. Phylogenetic analyses suggest lateral gene transfer (LGT) of rquA from bacteria to eukaryotes occurred at least twice and the gene was transferred multiple times amongst protists. We demonstrate that RquA functions in the mitochondrion-related organelles of the anaerobic protist Pygsuia and is correlated with the presence of RQ. These analyses reveal the role of gene transfer in the evolutionary remodeling of mitochondria in adaptation to hypoxia.",

author = "Stairs, {Courtney W.} and Laura Eme and Mu{\~n}oz-G{\'o}mez, {Sergio A.} and Alejandro Cohen and Graham Dellaire and Shepherd, {Jennifer N.} and Fawcett, {James P.} and Roger, {Andrew J.}",

note = "Funding Information: This research, and CWS and LE, were supported by a grant from the Canadian Institutes of Health Research (CIHR) MOP 142349 awarded to AJR. CWS was also supported by the Natural Sciences and Engineering Council of Canada Canadian Graduate Studentship (NSERC-CGS-D) and the Killiam Trusts (Level 2). JNS was supported by the National Institutes of Health (award no. 1R15GM096398-01). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Institutes of Health. Work in the GD laboratory was supported by an NSERC Discovery Grant (RGPIN 05616). Work from JPF laboratory was supported by a CIHR (MOP 341174). The authors would also like to acknowledge Dr. Dale Corkery for assistance in microscopy; and Drs. Eleni Gentekaki (Mae Fah Luang University), Denis Lynn (University of Guelf), and Matthew Brown (Mississippi State University) for providing sequences; Dr. Barbara Karten (Dalhousie University) for providing equipment and expertise in lipid extractions; Dr. Melanie Dobson (Dalhousie University) for providing pGEX plasmids; and Dr. Joran Martijn for discussion on alphaproteobacterial phylogeny. Funding Information: This research, and CWS and LE, were supported by a grant from the Canadian Institutes of Health Research (CIHR) MOP 142349 awarded to AJR. CWS was also supported by the Natural Sciences and Engineering Council of Canada Canadian Graduate Studentship (NSERC-CGS-D) and the Killiam Trusts (Level 2). JNS was supported by the National Institutes of Health (award no. 1R15GM096398-01). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Institutes of Health. Work in the GD laboratory was supported by an NSERC Discovery Grant (RGPIN 05616). Work from JPF laboratory was supported by a CIHR (MOP 341174). The authors would also like to acknowledge Dr. Dale Corkery for assistance in microscopy; and Drs. Eleni Gentekaki (Mae Fah Luang University), Denis Lynn (University of Guelf), and Matthew Brown (Mississippi State University) for providing sequences; Dr. Barbara Karten (Dalhousie University) for providing equipment and expertise in lipid extractions; Dr. Melanie Dobson (Dalhousie University) for providing pGEX plasmids; and Dr. Joran Martijn for discussion on alphaproteobacterial phylogeny. Canadian Institutes of Health Research MOP 142349 Andrew J Roger National Institutes of Health 1R15GM096398-01 Jennifer N Shepherd Natural Sciences and Engineering Research Council of Canada NSERC-CGS-D Courtney W Stairs Killam Trusts Courtney W Stairs Courtney W Stairs Natural Sciences and Engineering Research Council of Canada RGPIN 05616 Graham Dellaire Canadian Institutes of Health MOP 341174 James P Fawcett Research. Publisher Copyright: {\textcopyright} Stairs et al.",

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AU - Stairs, Courtney W.

AU - Eme, Laura

AU - Muñoz-Gómez, Sergio A.

AU - Cohen, Alejandro

AU - Dellaire, Graham

AU - Shepherd, Jennifer N.

AU - Fawcett, James P.

AU - Roger, Andrew J.

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N2 - Under hypoxic conditions, some organisms use an electron transport chain consisting of only complex I and II (CII) to generate the proton gradient essential for ATP production. In these cases, CII functions as a fumarate reductase that accepts electrons from a low electron potential quinol, rhodoquinol (RQ). To clarify the origins of RQ-mediated fumarate reduction in eukaryotes, we investigated the origin and function of rquA, a gene encoding an RQ biosynthetic enzyme. RquA is very patchily distributed across eukaryotes and bacteria adapted to hypoxia. Phylogenetic analyses suggest lateral gene transfer (LGT) of rquA from bacteria to eukaryotes occurred at least twice and the gene was transferred multiple times amongst protists. We demonstrate that RquA functions in the mitochondrion-related organelles of the anaerobic protist Pygsuia and is correlated with the presence of RQ. These analyses reveal the role of gene transfer in the evolutionary remodeling of mitochondria in adaptation to hypoxia.

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Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis

Abstract

Bibliographical note

ASJC Scopus Subject Areas

PubMed: MeSH publication types

Access to Document

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