Skip to main content
SpringerLink
Log in

The Evolutionary Relationship Between Complex I and [NiFe]-Hydrogenase

  • Chapter
  • First Online:
A Structural Perspective on Respiratory Complex I

Abstract

Complex I (NADH:ubiquinone oxidoreductase), the first component of the respiratory chain in aerobic microorganisms and mitochondria, has been shown to be structurally related to [NiFe]-hydrogenases. A plausible theory postulates that the ancestor of complex I was formed by the association of a soluble hydrogenase with membrane-bound antiporters which had already acquired proton pumping capabilities. Contemporary examples of this type of hydrogenases are the energy-conserving enzymes found in several microorganisms. In this chapter we discuss this process and speculate on the origin of aerobic respiration and its relation to oxygen levels in the early atmosphere. We also compare the known crystal structures of the hydrophilic domain of complex I and [NiFe]-hydrogenase and postulate that a putative redox-induced rearrangement of a common long four-helical bundle between a kinked and a straight conformation may be involved in proton pumping.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albracht SPJ (1993) Intimate relationships of the large and the small subunits of all nickel hydrogenases with two nuclear-encoded subunits of mitochondrial NADH:ubiquinone oxidoreductase. Biochim Biophys Acta 1144:221–224

    Article  PubMed  CAS  Google Scholar 

  • Albracht SPJ (2010a) The reaction of NADPH with bovine mitochondrial NADH:ubiquinone oxidoreductase revisited. I. Proposed consequences for electron transfer in the enzyme. J Bioenerg Biomembr 42:261–278

    Article  PubMed  CAS  Google Scholar 

  • Albracht SPJ (2010b) The reaction of NADPH with bovine mitochondrial NADH:ubiquinone oxidoreductase revisited. II. Comparison of the proposed working hypothesis with literature data. J Bioenerg Biomembr 42:279–292

    Article  PubMed  CAS  Google Scholar 

  • Albracht SPJ, De Jong AMP (1997) Hypothesis: bovine-heart NADH:ubiquinone oxidoreductase is a monomer with 8 Fe-S clusters and 2 FMN groups. Biochim Biophys Acta 1318:92–106

    Article  PubMed  CAS  Google Scholar 

  • Albracht SP, Hedderich R (2000) Learning from hydrogenases: location of a proton pump and of a second FMN in bovine NAD-ubiquinone oxidoreductase (complex I). FEBS Lett 485:1–6

    Article  PubMed  CAS  Google Scholar 

  • Berrisford JM, Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. J Biol Chem 284:29773–29783

    Article  PubMed  CAS  Google Scholar 

  • Böhm R, Sauter M, Böck A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4:231–243

    Article  PubMed  Google Scholar 

  • Castresana J, Moreira D (1999) Respiratory chains in the last common ancestor of living organisms. J Mol Evol 49:453–460

    Article  PubMed  CAS  Google Scholar 

  • Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC6803 deficient in the type I NAPDH-dehydrogenase complex. J Bacteriol 186:1737–1746

    Article  PubMed  CAS  Google Scholar 

  • Deppenmeier U (2004) The membrane-bound electron transport system of Methanosarcina species. J Bioenerg Biomembr 36:55–64

    Article  PubMed  CAS  Google Scholar 

  • Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465:441–447

    Article  PubMed  CAS  Google Scholar 

  • Fearnley IM, Walker JE (1992) Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta 1140:105–134

    Article  PubMed  CAS  Google Scholar 

  • Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1–5

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T, Weiss H (1997) Modular evolution of the respiratory NADH: ubiquinone oxidoreductase and the origin of its modules. J Theor Biol 187:418–439

    Article  Google Scholar 

  • Garcin E, Vernede X, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC (1999) The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure 7:557–566

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R (2004) Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J Bioenerg Biomembr 36:65–75

    Article  PubMed  CAS  Google Scholar 

  • Hinchliffe P, Sazanov LA (2005) Organization of iron-sulfur clusters in respiratory complex I. Science 309:771–774

    Article  PubMed  CAS  Google Scholar 

  • Hosler JP, Ferguson-Miller S, Mills DA (2006) Energy transduction: proton transfer through the respiratory complexes. Annu Rev Biochem 75:165–187

    Article  PubMed  CAS  Google Scholar 

  • Kaesler B, Schönheit P (1989) The sodium cycle in methanogenesis. CO2 reduction to the formaldehyde level in methanogenic bacteria is driven by a primary electrochemical potential of Na+ generated by formaldehyde reduction to CH4. Eur J Biochem 186:309–316

    Article  PubMed  CAS  Google Scholar 

  • Kasting JF (1993) Earth’s early atmosphere. Science 259:920–926

    Article  PubMed  CAS  Google Scholar 

  • Konhauser KO, Pecoits E, Lalonde SV, Papineau D, Barley ME, Arndt NT, Zahnle K, Kamber BS (2009) Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458:750–751

    Article  PubMed  CAS  Google Scholar 

  • Kurland CG, Andersson SGE (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64(4):786–820

    Article  PubMed  CAS  Google Scholar 

  • Long M, Liu J, Chen Z, Bleijlevens B, Roseboom W, Albracht SP (2007) Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module. J Biol Inorg Chem 12:62–78

    Article  PubMed  CAS  Google Scholar 

  • Magalon A, Böck A (2000) Analysis of the HypC-HycE complex, a key intermediate in the assembly of the metal center of the Escherichia coli hydrogenase 3. J Biol Chem 275:21114–21120

    Article  PubMed  CAS  Google Scholar 

  • Malki S, Saimmaime I, De Luca G, Rousset M, Dermoun Z, Belaich J-P (1995) Characterization of an operon encoding an NADP-reducing hydrogenase in Desulfovibrio fructosovorans. J Bacteriol 177:2628–2636

    PubMed  CAS  Google Scholar 

  • Martin W, Mueller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41

    Article  PubMed  CAS  Google Scholar 

  • Mathiesen C, Hägerhäll C (2003) The ‘antiporter module’ of respiratory chain complex I includes the MrpC/NuoK subunit – a revision of the modular evolution scheme. FEBS Lett 549:7–13

    Article  PubMed  CAS  Google Scholar 

  • Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 Å and modelling studies of its interaction with the tetrahaem cytochrome c3. J Biol Inorg Chem 6:63–81

    Article  PubMed  CAS  Google Scholar 

  • Meuer J, Kuettner HC, Zhang JK, Hedderich R, Metcalf WW (2002) Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci USA 99:5632–5637

    Article  PubMed  CAS  Google Scholar 

  • Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23

    Article  PubMed  CAS  Google Scholar 

  • Nicolet Y, Lemon BJ, Fontecilla-Camps JC, Peters JW (2000) A novel FeS cluster in Fe-only hydrogenases. Trends Biochem Sci 25:138–143

    Article  PubMed  CAS  Google Scholar 

  • Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum. Science 282:1853–1858

    Article  PubMed  CAS  Google Scholar 

  • Pilkington SJ, Skehel JM, Gennis RB, Walker JE (1991) Relationship between mitochondrial NADH-ubiquinone reductase and a bacterial NAD-reducing hydrogenase. Biochemistry 30:2166–2175

    Article  PubMed  CAS  Google Scholar 

  • Samuilov VD (2005) Energy problems in life evolution. Biochemistry (Moscow) 70:246–250

    Article  CAS  Google Scholar 

  • Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430–1436

    Article  PubMed  CAS  Google Scholar 

  • Tian F, Too OB, Pavlov AA, De Sterck H (2005) A hydrogen-rich early earth atmosphere. Science 308:1014–1017

    Article  PubMed  CAS  Google Scholar 

  • Van der Linden E, Burgdorf T, de Lacey AL, Buhrke T, Scholte M, Fernandez VM, Friedrich B, Albracht SPJ (2006) An improved purification procedure for the soluble [NiFe]-hydrogenase of Ralstonia eutropha: new insights into its (in) stability and spectroscopic properties. J Biol Inorg Chem 11:247–260

    Article  PubMed  Google Scholar 

  • Verhagen MF, O’Rourke T, Adams MW (1999) The hyperthermophilic bacterium, Thermotoga maritima, contains an unusually complex iron-hydrogenase: amino acid sequence analyses versus biochemical characterization. Biochim Biophys Acta 1412:212–229

    Article  PubMed  CAS  Google Scholar 

  • Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587

    Article  PubMed  CAS  Google Scholar 

  • Winner C, Gottschalk G (1989) Η2 and CO2 production from methanol or formaldehyde by the methanogenic bacterium strain Gö1 treated with 2-bromoethanesulfonic acid. FEMS Microbiol Lett 65:259–264

    CAS  Google Scholar 

  • Yagi T, Matsuno-Yagin A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 47:2266–2274

    Article  Google Scholar 

  • Zwicker K, Galkin A, Dröse S, Grgic L, Kerscher S, Brandt U (2006) The redox-Bohr group associated with iron-sulfur cluster N2 of complex I. J Biol Chem 281:23013–23017

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Cristallographie et de Cristallogenèse des Protéines, CEA, CNRS, Université Joseph Fourier, 41, rue Jules Horowitz, 38027, Grenoble Cedex 1, France

    Anne Volbeda & Juan C. Fontecilla-Camps

Authors
  1. Anne Volbeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan C. Fontecilla-Camps
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan C. Fontecilla-Camps .

Editor information

Editors and Affiliations

  1. , Mitochondrial Biology Unit, Medical Research Council, Hills road, Cambridge, CB2 0XY, Cambridgeshire, United Kingdom

    Leonid Sazanov

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Volbeda, A., Fontecilla-Camps, J.C. (2012). The Evolutionary Relationship Between Complex I and [NiFe]-Hydrogenase. In: Sazanov, L. (eds) A Structural Perspective on Respiratory Complex I. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4138-6_6

Download citation

Publish with us

Policies and ethics

Search

Navigation