Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems?

James W.A. Allen, Andrew P. Jackson, Daniel J. Rigden, Antony C. Willis, Stuart J. Ferguson, Michael L. Ginger

Research output: Contribution to journalReview article

53 Citations (Scopus)

Abstract

Mitochondrial cytochromes c and c1 are present in all eukaryotes that use oxygen as the terminal electron acceptor in the respiratory chain. Maturation of c-type cytochromes requires covalent attachment of the heme cofactor to the protein, and there are at least five distinct biogenesis systems that catalyze this post-translational modification in different organisms and organelles. In this study, we use biochemical data, comparative genomic and structural bioinformatics investigations to provide a holistic view of mitochondrial c-type cytochrome biogenesis and its evolution. There are three pathways for mitochondrial c-type cytochrome maturation, only one of which is present in prokaryotes. We analyze the evolutionary distribution of these biogenesis systems, which include the Ccm system (System I) and the enzyme heme lyase (System III). We conclude that heme lyase evolved once and, in many lineages, replaced the multicomponent Ccm system (present in the proto-mitochondrial endosymbiont), probably as a consequence of lateral gene transfer. We find no evidence of a System III precursor in prokaryotes, and argue that System III is incompatible with multi-heme cytochromes common to bacteria, but absent from eukaryotes. The evolution of the eukaryotic-specific protein heme lyase is strikingly unusual, given that this protein provides a function (thioether bond formation) that is also ubiquitous in prokaryotes. The absence of any known c-type cytochrome biogenesis system from the sequenced genomes of various trypanosome species indicates the presence of a third distinct mitochondrial pathway. Interestingly, this system attaches heme to mitochondrial cytochromes c that contain only one cysteine residue, rather than the usual two, within the heme-binding motif. The isolation of single-cysteine-containing mitochondrial cytochromes c from free-living kinetoplastids, Euglena and the marine flagellate Diplonema papillatum suggests that this unique form of heme attachment is restricted to, but conserved throughout, the protist phylum Euglenozoa.

LanguageEnglish
Pages2385-2402
Number of pages18
JournalFEBS Journal
Volume275
Issue number10
DOIs
Publication statusPublished - 1 Apr 2008
Externally publishedYes

Fingerprint

Cytochrome c Group
Heme
Lyases
Cytochromes c
Eukaryota
Euglenozoa
Cysteine
Euglena
Cytochromes c1
Meiotic Prophase I
Gene transfer
Horizontal Gene Transfer
Proteins
Trypanosomiasis
Sulfides
Cytochromes
Post Translational Protein Processing
Bioinformatics
Electron Transport
Computational Biology

Cite this

Allen, James W.A. ; Jackson, Andrew P. ; Rigden, Daniel J. ; Willis, Antony C. ; Ferguson, Stuart J. ; Ginger, Michael L. / Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems?. In: FEBS Journal. 2008 ; Vol. 275, No. 10. pp. 2385-2402.
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abstract = "Mitochondrial cytochromes c and c1 are present in all eukaryotes that use oxygen as the terminal electron acceptor in the respiratory chain. Maturation of c-type cytochromes requires covalent attachment of the heme cofactor to the protein, and there are at least five distinct biogenesis systems that catalyze this post-translational modification in different organisms and organelles. In this study, we use biochemical data, comparative genomic and structural bioinformatics investigations to provide a holistic view of mitochondrial c-type cytochrome biogenesis and its evolution. There are three pathways for mitochondrial c-type cytochrome maturation, only one of which is present in prokaryotes. We analyze the evolutionary distribution of these biogenesis systems, which include the Ccm system (System I) and the enzyme heme lyase (System III). We conclude that heme lyase evolved once and, in many lineages, replaced the multicomponent Ccm system (present in the proto-mitochondrial endosymbiont), probably as a consequence of lateral gene transfer. We find no evidence of a System III precursor in prokaryotes, and argue that System III is incompatible with multi-heme cytochromes common to bacteria, but absent from eukaryotes. The evolution of the eukaryotic-specific protein heme lyase is strikingly unusual, given that this protein provides a function (thioether bond formation) that is also ubiquitous in prokaryotes. The absence of any known c-type cytochrome biogenesis system from the sequenced genomes of various trypanosome species indicates the presence of a third distinct mitochondrial pathway. Interestingly, this system attaches heme to mitochondrial cytochromes c that contain only one cysteine residue, rather than the usual two, within the heme-binding motif. The isolation of single-cysteine-containing mitochondrial cytochromes c from free-living kinetoplastids, Euglena and the marine flagellate Diplonema papillatum suggests that this unique form of heme attachment is restricted to, but conserved throughout, the protist phylum Euglenozoa.",
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Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems? / Allen, James W.A.; Jackson, Andrew P.; Rigden, Daniel J.; Willis, Antony C.; Ferguson, Stuart J.; Ginger, Michael L.

In: FEBS Journal, Vol. 275, No. 10, 01.04.2008, p. 2385-2402.

Research output: Contribution to journalReview article

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T1 - Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems?

AU - Allen, James W.A.

AU - Jackson, Andrew P.

AU - Rigden, Daniel J.

AU - Willis, Antony C.

AU - Ferguson, Stuart J.

AU - Ginger, Michael L.

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AB - Mitochondrial cytochromes c and c1 are present in all eukaryotes that use oxygen as the terminal electron acceptor in the respiratory chain. Maturation of c-type cytochromes requires covalent attachment of the heme cofactor to the protein, and there are at least five distinct biogenesis systems that catalyze this post-translational modification in different organisms and organelles. In this study, we use biochemical data, comparative genomic and structural bioinformatics investigations to provide a holistic view of mitochondrial c-type cytochrome biogenesis and its evolution. There are three pathways for mitochondrial c-type cytochrome maturation, only one of which is present in prokaryotes. We analyze the evolutionary distribution of these biogenesis systems, which include the Ccm system (System I) and the enzyme heme lyase (System III). We conclude that heme lyase evolved once and, in many lineages, replaced the multicomponent Ccm system (present in the proto-mitochondrial endosymbiont), probably as a consequence of lateral gene transfer. We find no evidence of a System III precursor in prokaryotes, and argue that System III is incompatible with multi-heme cytochromes common to bacteria, but absent from eukaryotes. The evolution of the eukaryotic-specific protein heme lyase is strikingly unusual, given that this protein provides a function (thioether bond formation) that is also ubiquitous in prokaryotes. The absence of any known c-type cytochrome biogenesis system from the sequenced genomes of various trypanosome species indicates the presence of a third distinct mitochondrial pathway. Interestingly, this system attaches heme to mitochondrial cytochromes c that contain only one cysteine residue, rather than the usual two, within the heme-binding motif. The isolation of single-cysteine-containing mitochondrial cytochromes c from free-living kinetoplastids, Euglena and the marine flagellate Diplonema papillatum suggests that this unique form of heme attachment is restricted to, but conserved throughout, the protist phylum Euglenozoa.

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KW - Cytochrome c

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KW - Evolution

KW - Heme lyase

KW - Lateral gene transfer

KW - Mitochondria

KW - Post-translational modification

KW - Trypanosoma

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EP - 2402

JO - FEBS Journal

T2 - FEBS Journal

JF - FEBS Journal

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