The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin

Brigitte Boxma, Guenola Ricard, Angela H A M van Hoek, Edouard Severing, Seung-Yeo Moon-van der Staay, Georg W M van der Staay, Theo A van Alen, Rob M de Graaf, Geert Cremers, Michiel Kwantes, Neil R McEwan, C Jamie Newbold, Jean-Pierre Jouany, Tadeusz Michalowski, Peter Pristas, Martijn A Huynen, Johannes H P Hackstein

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

BACKGROUND: The hydrogenosomes of the anaerobic ciliate Nyctotherus ovalis show how mitochondria can evolve into hydrogenosomes because they possess a mitochondrial genome and parts of an electron-transport chain on the one hand, and a hydrogenase on the other hand. The hydrogenase permits direct reoxidation of NADH because it consists of a [FeFe] hydrogenase module that is fused to two modules, which are homologous to the 24 kDa and the 51 kDa subunits of a mitochondrial complex I.

RESULTS: The [FeFe] hydrogenase belongs to a clade of hydrogenases that are different from well-known eukaryotic hydrogenases. The 24 kDa and the 51 kDa modules are most closely related to homologous modules that function in bacterial [NiFe] hydrogenases. Paralogous, mitochondrial 24 kDa and 51 kDa modules function in the mitochondrial complex I in N. ovalis. The different hydrogenase modules have been fused to form a polyprotein that is targeted into the hydrogenosome.

CONCLUSION: The hydrogenase and their associated modules have most likely been acquired by independent lateral gene transfer from different sources. This scenario for a concerted lateral gene transfer is in agreement with the evolution of the hydrogenosome from a genuine ciliate mitochondrion by evolutionary tinkering.

Original languageEnglish
Pages (from-to)230
JournalBMC Evolutionary Biology
Volume7
DOIs
Publication statusPrint publication - 16 Nov 2007
Externally publishedYes

Fingerprint

Nyctotherus
NADH dehydrogenase (ubiquinone)
gene transfer
mitochondrion
ciliate
Ciliophora
mitochondria
electron transport chain
genome
electron
horizontal gene transfer

Keywords

  • Animals
  • Chimera/genetics
  • Ciliophora/enzymology
  • Electron Transport Complex I/genetics
  • Evolution, Molecular
  • Gene Transfer, Horizontal
  • Genome, Mitochondrial
  • Genome, Protozoan
  • Hydrogenase/genetics
  • Iron-Sulfur Proteins/genetics
  • Phylogeny
  • Sequence Alignment
  • Sequence Homology, Amino Acid

Cite this

Boxma, B., Ricard, G., van Hoek, A. H. A. M., Severing, E., Moon-van der Staay, S-Y., van der Staay, G. W. M., ... Hackstein, J. H. P. (2007). The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. BMC Evolutionary Biology, 7, 230. https://doi.org/10.1186/1471-2148-7-230
Boxma, Brigitte ; Ricard, Guenola ; van Hoek, Angela H A M ; Severing, Edouard ; Moon-van der Staay, Seung-Yeo ; van der Staay, Georg W M ; van Alen, Theo A ; de Graaf, Rob M ; Cremers, Geert ; Kwantes, Michiel ; McEwan, Neil R ; Newbold, C Jamie ; Jouany, Jean-Pierre ; Michalowski, Tadeusz ; Pristas, Peter ; Huynen, Martijn A ; Hackstein, Johannes H P. / The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. In: BMC Evolutionary Biology. 2007 ; Vol. 7. pp. 230.
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abstract = "BACKGROUND: The hydrogenosomes of the anaerobic ciliate Nyctotherus ovalis show how mitochondria can evolve into hydrogenosomes because they possess a mitochondrial genome and parts of an electron-transport chain on the one hand, and a hydrogenase on the other hand. The hydrogenase permits direct reoxidation of NADH because it consists of a [FeFe] hydrogenase module that is fused to two modules, which are homologous to the 24 kDa and the 51 kDa subunits of a mitochondrial complex I.RESULTS: The [FeFe] hydrogenase belongs to a clade of hydrogenases that are different from well-known eukaryotic hydrogenases. The 24 kDa and the 51 kDa modules are most closely related to homologous modules that function in bacterial [NiFe] hydrogenases. Paralogous, mitochondrial 24 kDa and 51 kDa modules function in the mitochondrial complex I in N. ovalis. The different hydrogenase modules have been fused to form a polyprotein that is targeted into the hydrogenosome.CONCLUSION: The hydrogenase and their associated modules have most likely been acquired by independent lateral gene transfer from different sources. This scenario for a concerted lateral gene transfer is in agreement with the evolution of the hydrogenosome from a genuine ciliate mitochondrion by evolutionary tinkering.",
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Boxma, B, Ricard, G, van Hoek, AHAM, Severing, E, Moon-van der Staay, S-Y, van der Staay, GWM, van Alen, TA, de Graaf, RM, Cremers, G, Kwantes, M, McEwan, NR, Newbold, CJ, Jouany, J-P, Michalowski, T, Pristas, P, Huynen, MA & Hackstein, JHP 2007, 'The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin', BMC Evolutionary Biology, vol. 7, pp. 230. https://doi.org/10.1186/1471-2148-7-230

The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. / Boxma, Brigitte; Ricard, Guenola; van Hoek, Angela H A M; Severing, Edouard; Moon-van der Staay, Seung-Yeo; van der Staay, Georg W M; van Alen, Theo A; de Graaf, Rob M; Cremers, Geert; Kwantes, Michiel; McEwan, Neil R; Newbold, C Jamie; Jouany, Jean-Pierre; Michalowski, Tadeusz; Pristas, Peter; Huynen, Martijn A; Hackstein, Johannes H P.

In: BMC Evolutionary Biology, Vol. 7, 16.11.2007, p. 230.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin

AU - Boxma, Brigitte

AU - Ricard, Guenola

AU - van Hoek, Angela H A M

AU - Severing, Edouard

AU - Moon-van der Staay, Seung-Yeo

AU - van der Staay, Georg W M

AU - van Alen, Theo A

AU - de Graaf, Rob M

AU - Cremers, Geert

AU - Kwantes, Michiel

AU - McEwan, Neil R

AU - Newbold, C Jamie

AU - Jouany, Jean-Pierre

AU - Michalowski, Tadeusz

AU - Pristas, Peter

AU - Huynen, Martijn A

AU - Hackstein, Johannes H P

PY - 2007/11/16

Y1 - 2007/11/16

N2 - BACKGROUND: The hydrogenosomes of the anaerobic ciliate Nyctotherus ovalis show how mitochondria can evolve into hydrogenosomes because they possess a mitochondrial genome and parts of an electron-transport chain on the one hand, and a hydrogenase on the other hand. The hydrogenase permits direct reoxidation of NADH because it consists of a [FeFe] hydrogenase module that is fused to two modules, which are homologous to the 24 kDa and the 51 kDa subunits of a mitochondrial complex I.RESULTS: The [FeFe] hydrogenase belongs to a clade of hydrogenases that are different from well-known eukaryotic hydrogenases. The 24 kDa and the 51 kDa modules are most closely related to homologous modules that function in bacterial [NiFe] hydrogenases. Paralogous, mitochondrial 24 kDa and 51 kDa modules function in the mitochondrial complex I in N. ovalis. The different hydrogenase modules have been fused to form a polyprotein that is targeted into the hydrogenosome.CONCLUSION: The hydrogenase and their associated modules have most likely been acquired by independent lateral gene transfer from different sources. This scenario for a concerted lateral gene transfer is in agreement with the evolution of the hydrogenosome from a genuine ciliate mitochondrion by evolutionary tinkering.

AB - BACKGROUND: The hydrogenosomes of the anaerobic ciliate Nyctotherus ovalis show how mitochondria can evolve into hydrogenosomes because they possess a mitochondrial genome and parts of an electron-transport chain on the one hand, and a hydrogenase on the other hand. The hydrogenase permits direct reoxidation of NADH because it consists of a [FeFe] hydrogenase module that is fused to two modules, which are homologous to the 24 kDa and the 51 kDa subunits of a mitochondrial complex I.RESULTS: The [FeFe] hydrogenase belongs to a clade of hydrogenases that are different from well-known eukaryotic hydrogenases. The 24 kDa and the 51 kDa modules are most closely related to homologous modules that function in bacterial [NiFe] hydrogenases. Paralogous, mitochondrial 24 kDa and 51 kDa modules function in the mitochondrial complex I in N. ovalis. The different hydrogenase modules have been fused to form a polyprotein that is targeted into the hydrogenosome.CONCLUSION: The hydrogenase and their associated modules have most likely been acquired by independent lateral gene transfer from different sources. This scenario for a concerted lateral gene transfer is in agreement with the evolution of the hydrogenosome from a genuine ciliate mitochondrion by evolutionary tinkering.

KW - Animals

KW - Chimera/genetics

KW - Ciliophora/enzymology

KW - Electron Transport Complex I/genetics

KW - Evolution, Molecular

KW - Gene Transfer, Horizontal

KW - Genome, Mitochondrial

KW - Genome, Protozoan

KW - Hydrogenase/genetics

KW - Iron-Sulfur Proteins/genetics

KW - Phylogeny

KW - Sequence Alignment

KW - Sequence Homology, Amino Acid

U2 - 10.1186/1471-2148-7-230

DO - 10.1186/1471-2148-7-230

M3 - Article

C2 - 18021395

VL - 7

SP - 230

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

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Boxma B, Ricard G, van Hoek AHAM, Severing E, Moon-van der Staay S-Y, van der Staay GWM et al. The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. BMC Evolutionary Biology. 2007 Nov 16;7:230. https://doi.org/10.1186/1471-2148-7-230