A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia

Courtney W. Stairs; Laura Eme; Matthew W. Brown; Cornelis Mutsaers; Edward Susko; Graham Dellaire; Darren M. Soanes; Mark Van Der Giezen; Andrew J. Roger

doi:10.1016/j.cub.2014.04.033

A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia

Courtney W. Stairs, Laura Eme, Matthew W. Brown, Cornelis Mutsaers, Edward Susko, Graham Dellaire, Darren M. Soanes, Mark Van Der Giezen, Andrew J. Roger

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

77 Citations (Scopus)

Abstract

Background Many microbial eukaryotes have evolved anaerobic alternatives to mitochondria known as mitochondrion-related organelles (MROs). Yet, only a few of these have been experimentally investigated. Here we report an RNA-seq-based reconstruction of the MRO proteome of Pygsuia biforma, an anaerobic representative of an unexplored deep-branching eukaryotic lineage. Results Pygsuia's MRO has a completely novel suite of functions, defying existing "function-based" organelle classifications. Most notable is the replacement of the mitochondrial iron-sulfur cluster machinery by an archaeal sulfur mobilization (SUF) system acquired via lateral gene transfer (LGT). Using immunolocalization in Pygsuia and heterologous expression in yeast, we show that the SUF system does indeed localize to the MRO. The Pygsuia MRO also possesses a unique assemblage of features, including: cardiolipin, phosphonolipid, amino acid, and fatty acid metabolism; a partial Kreb's cycle; a reduced respiratory chain; and a laterally acquired rhodoquinone (RQ) biosynthesis enzyme. The latter observation suggests that RQ is an electron carrier of a fumarate reductase-type complex II in this MRO. Conclusions The unique functional profile of this MRO underscores the tremendous plasticity of mitochondrial function within eukaryotes and showcases the role of LGT in forging metabolic mosaics of ancestral and newly acquired organellar pathways.

Original language	English
Pages (from-to)	1176-1186
Number of pages	11
Journal	Current Biology
Volume	24
Issue number	11
DOIs	https://doi.org/10.1016/j.cub.2014.04.033
Publication status	Published - Jun 2 2014

Bibliographical note

Funding Information:
C.S. is supported by a Natural Science and Engineering Research Council (NSERC) Alexander Graham Bell Canadian Graduate Scholarship and Killam Graduate Scholarship. L.E. and M.B. were supported by Centre for Comparative Genomics and Evolutionary Bioinformatics postdoctoral fellowships from the Tula Foundation. The majority of this work was supported by a Canadian Institutes of Health Research Grant (CIHR; MOP-82809) awarded to A.J.R. A.J.R. acknowledges the Canadian Institute for Advanced Research Program in Microbial Biodiversity, in which he is a Senior Fellow, and the Canada Research Chairs Program. Work in G.D.’s laboratory was supported by a CIHR Operating Grant (MOP-84260) and a Discovery Grant from the NSERC. G.D. is also a senior scientist of the Beatrice Hunter Cancer Research Institute (BHCRI; Halifax) and a CIHR New Investigator. Work in M.v.d.G.’s laboratory was supported by a CoSyst-BBSRC grant. The authors would also like to thank Melanie Dobson and Barbara Karten for providing reagents and advice for various experiments and A.G.M. Tielens for providing the α-TvASCT antibodies, the Mississippi State University’s High Performance Computing Collaboratory for computational resources, and Dale Corkery for assistance with microscopy.

ASJC Scopus Subject Areas

General Neuroscience
General Biochemistry,Genetics and Molecular Biology
General Agricultural and Biological Sciences

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1016/j.cub.2014.04.033

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title = "A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia",

abstract = "Background Many microbial eukaryotes have evolved anaerobic alternatives to mitochondria known as mitochondrion-related organelles (MROs). Yet, only a few of these have been experimentally investigated. Here we report an RNA-seq-based reconstruction of the MRO proteome of Pygsuia biforma, an anaerobic representative of an unexplored deep-branching eukaryotic lineage. Results Pygsuia's MRO has a completely novel suite of functions, defying existing {"}function-based{"} organelle classifications. Most notable is the replacement of the mitochondrial iron-sulfur cluster machinery by an archaeal sulfur mobilization (SUF) system acquired via lateral gene transfer (LGT). Using immunolocalization in Pygsuia and heterologous expression in yeast, we show that the SUF system does indeed localize to the MRO. The Pygsuia MRO also possesses a unique assemblage of features, including: cardiolipin, phosphonolipid, amino acid, and fatty acid metabolism; a partial Kreb's cycle; a reduced respiratory chain; and a laterally acquired rhodoquinone (RQ) biosynthesis enzyme. The latter observation suggests that RQ is an electron carrier of a fumarate reductase-type complex II in this MRO. Conclusions The unique functional profile of this MRO underscores the tremendous plasticity of mitochondrial function within eukaryotes and showcases the role of LGT in forging metabolic mosaics of ancestral and newly acquired organellar pathways.",

author = "Stairs, {Courtney W.} and Laura Eme and Brown, {Matthew W.} and Cornelis Mutsaers and Edward Susko and Graham Dellaire and Soanes, {Darren M.} and {Van Der Giezen}, Mark and Roger, {Andrew J.}",

note = "Funding Information: C.S. is supported by a Natural Science and Engineering Research Council (NSERC) Alexander Graham Bell Canadian Graduate Scholarship and Killam Graduate Scholarship. L.E. and M.B. were supported by Centre for Comparative Genomics and Evolutionary Bioinformatics postdoctoral fellowships from the Tula Foundation. The majority of this work was supported by a Canadian Institutes of Health Research Grant (CIHR; MOP-82809) awarded to A.J.R. A.J.R. acknowledges the Canadian Institute for Advanced Research Program in Microbial Biodiversity, in which he is a Senior Fellow, and the Canada Research Chairs Program. Work in G.D.{\textquoteright}s laboratory was supported by a CIHR Operating Grant (MOP-84260) and a Discovery Grant from the NSERC. G.D. is also a senior scientist of the Beatrice Hunter Cancer Research Institute (BHCRI; Halifax) and a CIHR New Investigator. Work in M.v.d.G.{\textquoteright}s laboratory was supported by a CoSyst-BBSRC grant. The authors would also like to thank Melanie Dobson and Barbara Karten for providing reagents and advice for various experiments and A.G.M. Tielens for providing the α-TvASCT antibodies, the Mississippi State University{\textquoteright}s High Performance Computing Collaboratory for computational resources, and Dale Corkery for assistance with microscopy. ",

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doi = "10.1016/j.cub.2014.04.033",

language = "English",

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T1 - A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia

AU - Stairs, Courtney W.

AU - Eme, Laura

AU - Brown, Matthew W.

AU - Mutsaers, Cornelis

AU - Susko, Edward

AU - Dellaire, Graham

AU - Soanes, Darren M.

AU - Van Der Giezen, Mark

AU - Roger, Andrew J.

N1 - Funding Information: C.S. is supported by a Natural Science and Engineering Research Council (NSERC) Alexander Graham Bell Canadian Graduate Scholarship and Killam Graduate Scholarship. L.E. and M.B. were supported by Centre for Comparative Genomics and Evolutionary Bioinformatics postdoctoral fellowships from the Tula Foundation. The majority of this work was supported by a Canadian Institutes of Health Research Grant (CIHR; MOP-82809) awarded to A.J.R. A.J.R. acknowledges the Canadian Institute for Advanced Research Program in Microbial Biodiversity, in which he is a Senior Fellow, and the Canada Research Chairs Program. Work in G.D.’s laboratory was supported by a CIHR Operating Grant (MOP-84260) and a Discovery Grant from the NSERC. G.D. is also a senior scientist of the Beatrice Hunter Cancer Research Institute (BHCRI; Halifax) and a CIHR New Investigator. Work in M.v.d.G.’s laboratory was supported by a CoSyst-BBSRC grant. The authors would also like to thank Melanie Dobson and Barbara Karten for providing reagents and advice for various experiments and A.G.M. Tielens for providing the α-TvASCT antibodies, the Mississippi State University’s High Performance Computing Collaboratory for computational resources, and Dale Corkery for assistance with microscopy.

PY - 2014/6/2

Y1 - 2014/6/2

N2 - Background Many microbial eukaryotes have evolved anaerobic alternatives to mitochondria known as mitochondrion-related organelles (MROs). Yet, only a few of these have been experimentally investigated. Here we report an RNA-seq-based reconstruction of the MRO proteome of Pygsuia biforma, an anaerobic representative of an unexplored deep-branching eukaryotic lineage. Results Pygsuia's MRO has a completely novel suite of functions, defying existing "function-based" organelle classifications. Most notable is the replacement of the mitochondrial iron-sulfur cluster machinery by an archaeal sulfur mobilization (SUF) system acquired via lateral gene transfer (LGT). Using immunolocalization in Pygsuia and heterologous expression in yeast, we show that the SUF system does indeed localize to the MRO. The Pygsuia MRO also possesses a unique assemblage of features, including: cardiolipin, phosphonolipid, amino acid, and fatty acid metabolism; a partial Kreb's cycle; a reduced respiratory chain; and a laterally acquired rhodoquinone (RQ) biosynthesis enzyme. The latter observation suggests that RQ is an electron carrier of a fumarate reductase-type complex II in this MRO. Conclusions The unique functional profile of this MRO underscores the tremendous plasticity of mitochondrial function within eukaryotes and showcases the role of LGT in forging metabolic mosaics of ancestral and newly acquired organellar pathways.

AB - Background Many microbial eukaryotes have evolved anaerobic alternatives to mitochondria known as mitochondrion-related organelles (MROs). Yet, only a few of these have been experimentally investigated. Here we report an RNA-seq-based reconstruction of the MRO proteome of Pygsuia biforma, an anaerobic representative of an unexplored deep-branching eukaryotic lineage. Results Pygsuia's MRO has a completely novel suite of functions, defying existing "function-based" organelle classifications. Most notable is the replacement of the mitochondrial iron-sulfur cluster machinery by an archaeal sulfur mobilization (SUF) system acquired via lateral gene transfer (LGT). Using immunolocalization in Pygsuia and heterologous expression in yeast, we show that the SUF system does indeed localize to the MRO. The Pygsuia MRO also possesses a unique assemblage of features, including: cardiolipin, phosphonolipid, amino acid, and fatty acid metabolism; a partial Kreb's cycle; a reduced respiratory chain; and a laterally acquired rhodoquinone (RQ) biosynthesis enzyme. The latter observation suggests that RQ is an electron carrier of a fumarate reductase-type complex II in this MRO. Conclusions The unique functional profile of this MRO underscores the tremendous plasticity of mitochondrial function within eukaryotes and showcases the role of LGT in forging metabolic mosaics of ancestral and newly acquired organellar pathways.

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A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia

Abstract

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