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Diversity of the Heme–Copper Superfamily in Archaea: Insights from Genomics and Structural Modeling

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Bioenergetics

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 45))

Abstract

Recent advances in DNA sequencing technologies have provided unprecedented access into the diversity of the microbial world. Herein we use the comparative genomic analysis of microbial genomes and environmental metagenomes coupled with structural modelling to explore the diversity of aerobic respiration in Archaea. We focus on the heme–copper oxidoreductase superfamily which is responsible for catalyzing the terminal reaction in aerobic respiration—the reduction of molecular oxygen to water. Sequence analyses demonstrate that there are at least eight heme–copper oxygen reductase families: A-, B-, C-, D-, E-, F-, G-, and H-families. Interestingly, five of these oxygen reductase families (D-, E-, F-, G-, and H-families) are currently found exclusively in Archaea. We review the structural properties of all eight families focusing on the members found within Archaea. Structural modelling coupled with sequence analysis suggests that many of the oxygen reductases identified from thermophilic Archaea have modified proton channel properties compared to the currently studied mesophilic bacterial oxygen reductases. These structural differences may be due to adaptation to the specific environments in which these enzymes function. We conclude with a brief analysis of the phylogenetic distribution and evolution of Archaeal heme–copper oxygen reductases.

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References

  • Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakkonen L, Puustinen A, Iwata S, Wikström M (2000) The Structure of the Heme–Copper Oxidase from Escherichia coli and its Binding Site for Ubiquinone. Nat Struct Biol 7(10):910–917

    Article  PubMed  CAS  Google Scholar 

  • Bathe S, Norris PR (2007) Ferrous iron- and sulfur-induced genes in Sulfolobus metallicus. Appl Environ Microbiol 73(8):2491–2497

    Article  PubMed  CAS  Google Scholar 

  • Bertini I, Cavallaro G, Rosato A (2007) Evolution of mitochondrial-type cytochrome c domains and of the protein machinery for their assembly. J Inorg Biochem 101(11–12):1798–1811

    Article  PubMed  CAS  Google Scholar 

  • Blomberg LM, Blomberg MR, Siegbahn PE (2006) Reduction of nitric oxide in bacterial nitric oxide reductase-a theoretical model study. Biochim Biophys Acta 1757(4):240–252

    Article  PubMed  CAS  Google Scholar 

  • Cavicchioli R (2006) Cold-adapted archaea. Nat Rev Microbiol 4(5):331–343

    Article  PubMed  CAS  Google Scholar 

  • Cho CM, Yan T, Liu X, Wu L, Zhou J, Stein LY (2006) Transcriptome of a Nitrosomonas europaea mutant with a disrupted nitrite reductase gene (nirK). Appl Environ Microbiol 72(6):4450–4454

    Article  PubMed  CAS  Google Scholar 

  • Collman JP, Yan YL, Lei J, Dinolfo PH (2006) Active-site models of bacterial nitric oxide reductase featuring tris-histidyl and glutamic acid mimics: influence of a carboxylate ligand on Fe(B) binding and the heme Fe/Fe(B) redox potential. Inorg Chem 45(19):7581–7583

    Article  PubMed  CAS  Google Scholar 

  • Cramm R, Siddiqui RA, Friedrich B (1997) Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol 179(21):6769–6777

    PubMed  CAS  Google Scholar 

  • DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50(4):470–478

    Article  PubMed  CAS  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara T, Fukumori Y, Yamanaka T (1989) Purification and properties of Halobacterium halobium cytochrome aa3 which lacks CuA and CuB. J Biochem (Tokyo) 105(2):287–922

    CAS  Google Scholar 

  • Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB (1994) The Superfamily of Heme–Copper Respiratory Oxidases. J Bacteriol 176(18):5587–5600

    PubMed  CAS  Google Scholar 

  • Girsch P, de Vries S (1997) Purification and initial kinetic and spectroscopic characterization of NO reductase from Paracoccus denitrificans. Biochim Biophys Acta 1318(1–2):202–216

    PubMed  CAS  Google Scholar 

  • Giuffre A, Stubaueer G, Sarti P, Brunori M, Zumft WG, Buse G, Soulimane T (1999) The Heme–copper Oxidases of Thermus thermophilus Catalyze the Reduction of Nitric Oxide: Evolutionary Implications. PNAS 96:14718–14723

    Article  PubMed  CAS  Google Scholar 

  • Gomes CM, Backgren C, Teixeira M, Puustinen A, Verkhovskaya ML, Wikstrom M, Verkhovsky MI (2001) Heme–copper oxidases with modified D- and K-pathways are yet efficient proton pumps. FEBS Lett 497(2–3):159–164

    Article  PubMed  CAS  Google Scholar 

  • Han D, Namslauer A, Pawate A, Morgan JE, Nagy S, Vakkasoglu AS, Brzezinski P, Gennis RB (2006) Replacing Asn207 by aspartate at the neck of the D channel in the aa3-type cytochrome c oxidase from Rhodobacter sphaeroides results in decoupling the proton pump. Biochemistry 45(47):14064–14074

    Article  PubMed  CAS  Google Scholar 

  • Hemp J (2007) The Heme–Copper Oxidoreductase Superfamily: Genomics and Structural Analyses. PhD Thesis, University of Illinois at Urbana-Champaign

    Google Scholar 

  • Hemp J, Han H, Roh JH, Kaplan S, Martinez TJ, Gennis RB (2007) Comparative genomics and site-directed mutagenesis support the existence of only one input channel for protons in the C-family (cbb3 oxidases) heme–copper oxygen reductases. Biochemistry 46(35):9963–9972

    Article  PubMed  CAS  Google Scholar 

  • Hemp J, Robinson DE, Ganesan KB, Martinez TJ, Kelleher NL, Gennis RB (2006) Evolutionary Migration of a Post-Translationally Modified Active-Site Residue in the Proton-Pumping Heme–Copper Oxygen Reductases. Biochemistry 45(51):15405–15410

    Article  PubMed  CAS  Google Scholar 

  • Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M (2000) Nitric oxide reductases in bacteria. Biochim Biophys Acta 1459(2–3):266–273

    PubMed  CAS  Google Scholar 

  • Hendriks J, Warne A, Gohlke U, Haltia T, Ludovici C, Lubben M, Saraste M (1998) The active site of the bacterial nitric oxide reductase is a dinuclear iron center. Biochemistry 37(38):13102–13109

    Article  PubMed  CAS  Google Scholar 

  • Hosler JP, Ferguson-Miller S, Calhoun MW, Thomas JW, Hill J, Lemieux L, Ma J, Georgiou C, Fetter J, Shapleigh J, Tecklenburg MMJ, Babcock GT, Gennis RB (1993) Insight into the Active-Site Structure and Function of Cytochrome Oxidase by Analysis of Site-Directed Mutants of Bacterial Cytochrome aa 3 and Cytochrome bo. J Bioenerg Biomembr 25(2):121–136

    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 

  • Ingledew WJ (2004) Fe(II) Oxidation by Thiobacillus ferrooxidans: The Role of the Cytochrome c Oxidase in Energy Coupling. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Ishikawa R, Ishido Y, Tachikawa A, Kawasaki H, Matsuzawa H, Wakagi T (2002) Aeropyrum pernix K1, a strictly aerobic and hyperthermophilic archaeon, has two terminal oxidases, cytochrome ba3 and cytochrome aa3. Arch Microbiol 179(1):42–49

    Article  PubMed  CAS  Google Scholar 

  • Kappler U, Sly LI, McEwan AG (2005) Respiratory gene clusters of Metallosphaera sedula – differential expression and transcriptional organization. Microbiology 151(Pt 1):35–43

    Article  PubMed  CAS  Google Scholar 

  • Komorowski L, Verheyen W, Schafer G (2002) The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases. Biol Chem 383(11):1791–1799

    Article  PubMed  CAS  Google Scholar 

  • Konstantinov AA, Siletsky S, Mitchell D, Kaulen A, Gennis RB (1997) The Roles of the Two Proton Input Channels in Cytochrome c Oxidase from Rhodobacter sphaeroides Probed by the Effects of Site-Directed Mutations on Time-Resolved Electrogenic Intraprotein Proton Transfer. Proc Natl Acad Sci USA 94:9085–9090

    Article  PubMed  CAS  Google Scholar 

  • Lübben M, Kolmerer B, Saraste M (1992) An Archaebacterial Terminal Oxidase Combines Core Structures of Two Mitochondrial Respiratory Complexes. EMBO J 11(3):805–812

    PubMed  Google Scholar 

  • Lübben M, Morand K (1994) Novel Prenylated Hemes as Cofactors of Cyhtochrome Oxidases. J Biol Chem 269(34):21473–21479

    PubMed  Google Scholar 

  • Madigan MT, Martinko JM (2006) Brock Biology of Microorganisms. Pearson/Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Mattar S, Engelhard M (1997) Cytochrome ba3 from Natronobacterium pharaonis—an archaeal four-subunit cytochrome-c-type oxidase. Eur J Biochem 250(2):332–341

    Article  PubMed  CAS  Google Scholar 

  • Michel H, Behr J, Harrenga A, Kannt A (1998) Cytochrome c oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329–356

    Article  PubMed  CAS  Google Scholar 

  • Muller FH, Bandeiras TM, Urich T, Teixeira M, Gomes CM, Kletzin A (2004) Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase. Mol Microbiol 53(4):1147–1160

    Article  PubMed  CAS  Google Scholar 

  • Nunoura T, Sako Y, Wakagi T, Uchida A (2003) Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense. Microbiology 149(Pt 3):673–688

    Article  PubMed  CAS  Google Scholar 

  • Nunoura T, Sako Y, Wakagi T, Uchida A (2005) Cytochrome aa3 in facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense. Can J Microbiol 51(8):621–627

    Article  PubMed  CAS  Google Scholar 

  • Ostermeier C, Harrenga A, Ermler U, Michel H (1997) Structure at 2.7 Å Resolution of the Paracoccus denitrificans Two-Subunit Cytochrome c Oxidase Complexed with an Antibody Fv Fragment. Proc Natl Acad Sci USA 94:10547–10553

    Article  PubMed  CAS  Google Scholar 

  • Pereira MM, Santana M, Teixeira M (2001) A Novel Scenario for the Evoluation of Haem-copper Oxygen Reductases. Biochim Biophys Acta 1505:185–208

    Article  PubMed  CAS  Google Scholar 

  • Philippot L (2005) Denitrification in pathogenic bacteria: for better or worst? Trends Microbiol 13(5):191–192

    Article  PubMed  CAS  Google Scholar 

  • Poole RK, Cook GM (2000) Redundancy of Aerobic Respiratory Chains in Bacteria? Routes, Reasons and Regulation. Adv Microb Physiol 43:165–224

    Article  PubMed  CAS  Google Scholar 

  • Purschke WG, Schmidt CL, Petersen A, Schäfer G (1997) The Terminal Quinol Oxidase of the Hyperthermophilic Archaeon Acidianus ambivalens Exhibits a Novel Subunit Structure and Gene Organization. J Bacteriol 179(4):1344–1353

    PubMed  CAS  Google Scholar 

  • Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394

    Article  PubMed  CAS  Google Scholar 

  • Rauhamaki V, Baumann M, Soliymani R, Puustinen A, Wikstrom M (2006) Identification of a histidine-tyrosine cross-link in the active site of the cbb3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 103(44):16135–16140

    Article  PubMed  CAS  Google Scholar 

  • Reimann J, Flock U, Lepp H, Honigmann A, Adelroth P (2007) A pathway for protons in nitric oxide reductase from Paracoccus denitrificans. Biochim Biophys Acta 1767(5):362–373

    Article  PubMed  CAS  Google Scholar 

  • Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: genomic analysis of microbial communities. Annu Rev Genet 38:525–552

    Article  PubMed  CAS  Google Scholar 

  • Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MS, Op den Camp HJ, Derksen JW, Pina-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443(7107):93–96

    Article  PubMed  CAS  Google Scholar 

  • Robertson CE, Harris JK, Spear JR, Pace NR (2005) Phylogenetic diversity and ecology of environmental Archaea. Curr Opin Microbiol 8(6):638–642

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Schäfer G (2004) Respiratory Chains in Archaea: From Minimal Systems to Supercomplexes. In: Zannoni D (ed) Advances in Photosynthesis and Respiration, vol 16. Respiration in Archaea and Bacteria: Diversity of Prokaryotic Respiratory Systems. Springer, Berlin Heidelberg New York, pp 1–33

    Google Scholar 

  • Schäfer G, Engelhard M, Müller V (1999) Bioenergetics of the Archaea. Microbiol Mol Biol Rev 63(3):570–620

    PubMed  Google Scholar 

  • Sharma V, Puustinen A, Wikstrom M, Laakkonen L (2006) Sequence analysis of the cbb3 oxidases and an atomic model for the Rhodobacter sphaeroides enzyme. Biochemistry 45(18):5754–5765

    Article  PubMed  CAS  Google Scholar 

  • Sievert SM, Scott KM, Klotz MG, Chain PSG, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J (2007) The genome of epsilon-proteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol (in press)

    Google Scholar 

  • Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, Than ME (2000) Structure and Mechanism of the Aberrant ba 3-cytochrome c Oxidase from Thermus thermophilus. EMBO J 19(8):1766–1776

    Article  PubMed  CAS  Google Scholar 

  • Soulimane T, Than ME, Dewor M, Huber R, Buse G (2000) Primary structure of a novel subunit in ba3-cytochrome oxidase from Thermus thermophilus. Protein Sci 9(11):2068–2073

    Article  PubMed  CAS  Google Scholar 

  • Stein LY, Arp DJ, Berube PM, Chain PSG, Hauser L, Jetten MSM, Klotz MG, Larimer FW, Norton JM, Op den Camp HJM, Shin M, Wei X (2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ Microbiol 9(12):2993–3007

    Article  PubMed  CAS  Google Scholar 

  • Suharti, Strampraad MJ, Schroder I, de Vries S (2001) A novel copper A containing menaquinol NO reductase from Bacillus azotoformans. Biochemistry 40(8):2632–2639

    Article  PubMed  CAS  Google Scholar 

  • Svensson-Ek M, Abramson J, Larsson G, Tornroth S, Brzezinski P, Iwata S (2002) The X-ray Crystal Structures of Wild-type and EQ (I-286) Mutant Cytochrome c Oxidases from Rhodobacter sphaeroides. J Mol Biol 321:329–339

    Article  PubMed  CAS  Google Scholar 

  • Tanaka M, Ogawa N, Ihara K, Sugiyama Y, Mukohata Y (2002) Cytochrome aa(3) in Haloferax volcanii. J Bacteriol 184(3):840–845

    Article  PubMed  CAS  Google Scholar 

  • Thorndycroft FH, Butland G, Richardson DJ, Watmough NJ (2007) A new assay for nitric oxide reductase reveals two conserved glutamate residues form the entrance to a proton-conducting channel in the bacterial enzyme. Biochem J 401(1):111–119

    Article  PubMed  CAS  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428(6978):37–43

    Article  PubMed  CAS  Google Scholar 

  • Victor BL, Baptista AM, Soares CM (2004) Theoretical identification of proton channels in the quinol oxidase aa3 from Acidianus ambivalens. Biophys J 87(6):4316–4325

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74(11):5088–5090

    Article  PubMed  CAS  Google Scholar 

  • Wraight CA (2006) Chance and design-proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta 1757(8):886–912

    Article  PubMed  CAS  Google Scholar 

  • Yarzabal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 150(Pt 7):2113–2123

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa S, Shinzawa-Itoh K, Tsukihara T (2000) X-ray Structure and the Reaction Mechanism of Bovine Heart Cytochrome c Oxidase. J Inorg Biochem 82:1–7

    Article  PubMed  CAS  Google Scholar 

  • Zumft WG (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme–copper oxidase type. J Inorg Biochem 99(1):194–215

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Robert B. Gennis .

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Günter Schäfer Harvey S. Penefsky

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Hemp, J., Gennis, R.B. (2008). Diversity of the Heme–Copper Superfamily in Archaea: Insights from Genomics and Structural Modeling. In: Schäfer, G., Penefsky, H.S. (eds) Bioenergetics. Results and Problems in Cell Differentiation, vol 45. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2007_046

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