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Phylogenomic analysis of type 1 NADH:Quinone oxidoreductase

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Abstract

We performed phylogenomic analysis of the catalytic core of NADH:quinone oxidoreductases of type 1 (NDH-1). Analysis of phylogenetic trees, as constructed for the core subunits of NDH-1, revealed fundamental differences in their topologies. In the case of four putatively homologous ion-carrying membrane subunits, the trees for the NuoH and NuoN subunits contained separate archaeal clades, whereas subunits NuoL and NuoM were characterized by multiple archaeal clades spread among bacterial branches. Large, separate clades, which united sequences belonging to different archaeal subdomains, were also found for cytoplasmic subunits NuoD and NuoB, homologous to the large and small subunits of nickel-iron hydrogenases. A smaller such clade was also shown for subunit NuoC. Based on these data, we suggest that the ancestral NDH-1 complex could be present already at the stage of the Last Universal Cellular Ancestor (LUCA). Ancestral forms of membrane subunits NuoN and NuoH and cytoplasmic subunits NuoD, NuoB, and, perhaps NuoC, may have formed a membrane complex that operated as an ion-translocating membrane hydrogenase. After the complex attained the ability to reduce membrane quinones, gene duplications could yield the subunits NuoL and NuoM, which enabled translocation of additional ions.

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References

  1. Sazanov, L. A. (2015) A giant molecular proton pump: structure and mechanism of respiratory complex I, Nat. Rev. Mol. Cell Biol., 16, 375–388.

    Article  CAS  PubMed  Google Scholar 

  2. Brandt, U. (2006) Energy converting NADH:quinone oxidoreductase (complex I), Annu. Rev. Biochem., 75, 69–92.

    Article  CAS  PubMed  Google Scholar 

  3. Carroll, J., Fearnley, I. M., Skehel, J. M., Shannon, R. J., Hirst, J., and Walker, J. E. (2006) Bovine complex I is a complex of 45 different subunits, J. Biol. Chem., 281, 32724–32727.

    Article  CAS  PubMed  Google Scholar 

  4. Vinothkumar, K. R., Zhu, J., and Hirst, J. (2014) Architecture of mammalian respiratory complex I, Nature, 515, 80–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sazanov, L. A., and Hinchliffe, P. (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus, Science, 311, 1430–1436.

    Article  CAS  PubMed  Google Scholar 

  6. Sazanov, L. A. (2014) The mechanism of coupling between electron transfer and proton translocation in respiratory complex I, J. Bioenerg. Biomembr., 46, 247–253.

    Article  CAS  PubMed  Google Scholar 

  7. Moparthi, V. K., and Hägerhäll, C. (2011) The evolution of respiratory chain complex I from a smaller last common ancestor consisting of 11 protein subunits, J. Mol. Evol., 72, 484–497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Baumer, S., Ide, T., Jacobi, C., Johann, A., Gottschalk, G., and Deppenmeier, U. (2000) The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases, J. Biol. Chem., 275, 17968–17973.

    Article  CAS  PubMed  Google Scholar 

  9. Finel, M. (1998) Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem. Sci., 23, 412–413.

    Article  CAS  PubMed  Google Scholar 

  10. Weerakoon, D. R., and Olson, J. W. (2007) The Campylobacter jejuni NADH:ubiquinone oxidoreductase (complex I) utilizes flavodoxin rather than NADH, J. Bacteriol., 190, 915–925.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Efremov, R. G., Baradaran, R., and Sazanov, L. A. (2010) The architecture of respiratory complex I, Nature, 465, 441–445.

    Article  CAS  PubMed  Google Scholar 

  13. Sazanov, L. A., Baradaran, R., Efremov, R. G., Berrisford, J. M., and Minhas, G. (2013) A long road towards the structure of respiratory complex I, a giant molecular proton pump, Biochem. Soc. Trans., 41, 1265–1271.

    Article  CAS  PubMed  Google Scholar 

  14. Marreiros, B. C., Batista, A. P., Duarte, A. M., and Pereira, M. M. (2013) A missing link between complex I and group 4 membrane-bound [NiFe] hydrogenases, Biochim. Biophys. Acta, 1827, 198–209.

    Article  CAS  PubMed  Google Scholar 

  15. Swartz, T. H., Ikewada, S., Ishikawa, O., Ito, M., and Krulwich, T. A. (2005) The Mrp system: a giant among monovalent cation/proton antiporters? Extremophiles, 9, 345–354.

    Article  CAS  PubMed  Google Scholar 

  16. Putnoky, P., Kereszt, A., Nakamura, T., Endre, G., Grosskopf, E., Kiss, P., and Kondorosi, A. (1998) The pha gene cluster of Rhizobium meliloti involved in pH adaptation and symbiosis encodes a novel type of K+ efflux system, Mol. Microbiol., 28, 1091–1101.

    Article  CAS  PubMed  Google Scholar 

  17. Baradaran, R., Berrisford, J. M., Minhas, G. S., and Sazanov, L. A. (2013) Crystal structure of the entire respiratory complex I, Nature, 494, 443–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mathiesen, C., and 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  CAS  PubMed  Google Scholar 

  19. Friedrich, T., and 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  CAS  PubMed  Google Scholar 

  20. Albracht, S. P., Mariette, A., and De Jong, P. (1997) Bovine-heart NADH:ubiquinone oxidoreductase is a monomer with 8 Fe-S clusters and 2 FMN groups, Biochim. Biophys. Acta, 1318, 92–106.

    Article  CAS  PubMed  Google Scholar 

  21. Tersteegen, A., and Hedderich, R. (1999) Methanobacterium thermoautotrophicum encodes two multisubunit membranebound [NiFe] hydrogenases. Transcription of the operons and sequence analysis of the deduced proteins, Eur. J. Biochem., 264, 930–943.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Schut, G. J., Boyd, E. S., Peters, J. W., and Adams, M. W. (2013) The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications, FEMS Microbiol. Rev., 37, 182–203.

    Article  CAS  PubMed  Google Scholar 

  24. Schut, G. J., Zadvornyy, O., Wu, C. H., Peters, J. W., Boyd, E. S., and Adams, M. W. (2016) The role of geochemistry and energetics in the evolution of modern respiratory complexes from a proton-reducing ancestor, Biochim. Biophys. Acta, pii: S0005-2728.

    Google Scholar 

  25. Tatusov, R. L., Koonin, E. V., and Lipman, D. J. (1997) A genomic perspective on protein families, Science, 278, 631–637.

    Article  CAS  PubMed  Google Scholar 

  26. Galperin, M. Y., Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database, Nucleic Acids Res., 43 (Database issue), D261–269.

    Article  PubMed  Google Scholar 

  27. Kristensen, D. M., Kannan, L., Coleman, M. K., Wolf, Y. I., Sorokin, A., Koonin, E. V., and Mushegian, A. (2010) A low-polynomial algorithm for assembling clusters of orthologous groups from intergenomic symmetric best matches, Bioinformatics, 26, 1481–1487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Dibrova, D. V., Galperin, M. Y., and Mulkidjanian, A. Y. (2010) Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase, Bioinformatics, 26, 1473–1476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., and Koonin, E. V. (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases, Nat. Rev. Microbiol., 5, 892–899.

    Article  CAS  PubMed  Google Scholar 

  30. Mulkidjanian, A. Y., Galperin, M. Y., Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2008) Evolutionary primacy of sodium bioenergetics, Biol. Direct, 3, 13.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Dibrova, D. V., Cherepanov, D. A., Galperin, M. Y., Skulachev, V. P., and Mulkidjanian, A. Y. (2013) Evolution of cytochrome bc complexes: from membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates, Biochim. Biophys. Acta, 1827, 1407–1427.

    Article  CAS  PubMed  Google Scholar 

  32. Mulkidjanian, A. Y., Koonin, E. V., Makarova, K. S., Mekhedov, S. L., Sorokin, A., Wolf, Y. I., Dufresne, A., Partensky, F., Burd, H., Kaznadzey, D., Haselkorn, R., and Galperin, M. Y. (2006) The cyanobacterial genome core and the origin of photosynthesis, Proc. Natl. Acad. Sci. USA, 103, 13126–13131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Edgar, R. C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity, BMC Bioinformatics, 5, 113.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res., 32, 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2–a multiple sequence alignment editor and analysis workbench, Bioinformatics, 25, 1189–1191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sonnhammer, E. L., Eddy, S. R., and Durbin, R. (1997) Pfam: a comprehensive database of protein domain families based on seed alignments, Proteins, 28, 405–420.

    Article  CAS  PubMed  Google Scholar 

  37. Krogh, A., Larsson, B., Von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a Hidden Markov Model: application to complete genomes, J. Mol. Biol., 305, 567–580.

    Article  CAS  PubMed  Google Scholar 

  38. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0, Mol. Biol. Evol., 30, 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 4, 406–425.

    CAS  PubMed  Google Scholar 

  40. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992) The rapid generation of mutation data matrices from protein sequences, Comput. Appl. Biosci., 8, 275–282.

    CAS  PubMed  Google Scholar 

  41. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 39, 783–791.

    Article  Google Scholar 

  42. Philippe, H., and Forterre, P. (1999) The rooting of the universal tree of life is not reliable, J. Mol. Evol., 49, 509–523.

    Article  CAS  PubMed  Google Scholar 

  43. Nelson-Sathi, S., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J. O., Deppenmeier, U., and Martin, W. F. (2012) Acquisition of 1000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea, Proc. Natl. Acad. Sci. USA, 109, 20537–20542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Koonin, E. V. (2000) How many genes can make a cell: the minimal-gene-set concept, Annu. Rev. Genom. Hum. Genet., 1, 99–116.

    Article  CAS  Google Scholar 

  45. Koonin, E. V. (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor, Nat. Rev. Microbiol., 1, 127–136.

    Article  CAS  PubMed  Google Scholar 

  46. Biegel, E., and Muller, V. (2010) Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase, Proc. Natl. Acad. Sci. USA, 107, 18138–18142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Biegel, E., Schmidt, S., Gonzalez, J. M., and Muller, V. (2011) Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes, Cell. Mol. Life Sci., 68, 613–634.

    Article  CAS  PubMed  Google Scholar 

  48. Mulkidjanian, A. Y., Dibrov, P., and Galperin, M. Y. (2008) The past and present of the sodium energetics: may the sodiummotive force be with you, Biochim. Biophys. Acta, 1777, 985–992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Dibrova, D. V., Chudetsky, M. Y., Galperin, M. Y., Koonin, E. V., and Mulkidjanian, A. Y. (2012) The role of energy in the emergence of biology from chemistry, Orig. Life Evol. Biosph., 42, 459–468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mulkidjanian, A. Y., Galperin, M. Y., and Koonin, E. V. (2009) Co-evolution of primordial membranes and membrane proteins, Trends Biochem. Sci., 34, 206–215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dibrova, D. V., Galperin, M. Y., Koonin, E. V., and Mulkidjanian, A. Y. (2015) Ancient systems of sodium/ potassium homeostasis as predecessors of membrane bioenergetics, Biochemistry (Moscow), 80, 495–516.

    Article  CAS  Google Scholar 

  52. Klimchuk, O. I., Dibrova, D. V., and Mulkidjanian, A. Y. (2016) Phylogenomic analysis identifies a sodium-translocating decarboxylating oxidoreductase in Thermotogae, Biochemistry (Moscow), 81, 481–490.

    Article  CAS  Google Scholar 

  53. Skulachev, V. P. (1984) Sodium bioenergetics, Trends Biochem. Sci., 9, 483–485.

    Article  CAS  Google Scholar 

  54. Deamer, D. W. (1987) Proton permeation of lipid bilayers, J. Bioenerg. Biomembr., 19, 457–479.

    CAS  PubMed  Google Scholar 

  55. Mulkidjanian, A. Y., Bychkov, A. Y., Dibrova, D. V., Galperin, M. Y., and Koonin, E. V. (2012) Origin of first cells at terrestrial, anoxic geothermal fields, Proc. Natl. Acad. Sci. USA, 109, E821–830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Macallum, A. B. (1926) The paleochemistry of the body fluids and tissues, Physiol. Rev., 6, 316–357.

    Google Scholar 

  57. Mulkidjanian, A. Y., Bychkov, A. Y., Dibrova, D. V., Galperin, M. Y., and Koonin, E. V. (2012) Open questions on the origin of life at anoxic geothermal fields, Orig. Life Evol. Biosph., 42, 507–516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Galimov, E. M., Natochin, Y. V., Ryzhenko, B. N., and Cherkasova, E. V. (2012) Chemical composition of the primary aqueous phase of the Earth and origin of life, Geochem. Int., 50, 1048–1068.

    Article  CAS  Google Scholar 

  59. Maruyama, S., Ikoma, M., Genda, H., Hirose, K., Yokoyama, T., and Santosh, M. (2013) The naked planet Earth: most essential pre-requisite for the origin and evolution of life, Geosci. Frontiers, 4, 141–165.

    Article  CAS  Google Scholar 

  60. Deamer, D. W. (1997) The first living systems: a bioenergetic perspective, Microbiol. Mol. Biol. Rev., 61, 239–261.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Mulkidjanian, A. Y., and Galperin, M. Y. (2010) Evolutionary origins of membrane proteins, in Structural Bioinformatics of Membrane Proteins (Frishman, D., ed.) Springer, pp. 1–28.

    Google Scholar 

  62. Chen, I. A., and Szostak, J. W. (2004) Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles, Proc. Natl. Acad. Sci. USA, 101, 7965–7970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kotlyar, A. B., and Vinogradov, A. D. (1990) Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase, Biochim. Biophys. Acta, 1019, 151–158.

    Article  CAS  PubMed  Google Scholar 

  64. Roberts, P. G., and Hirst, J. (2012) The deactive form of respiratory complex I from mammalian mitochondria is a Na+/H+ antiporter, J. Biol. Chem., 287, 34743–34751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Wikström, M. (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone, FEBS Lett., 169, 300–304.

    Article  PubMed  Google Scholar 

  66. Galkin, A., Drose, S., and Brandt, U. (2006) The proton pumping stoichiometry of purified mitochondrial complex I reconstituted into proteoliposomes, Biochim. Biophys. Acta, 1757, 1575–1581.

    Article  CAS  PubMed  Google Scholar 

  67. Galkin, A. S., Grivennikova, V. G., and Vinogradov, A. D. (1999) H+/2e–stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles, FEBS Lett., 451, 157–161.

    Article  CAS  PubMed  Google Scholar 

  68. Bogachev, A. V., Murtazina, R. A., and Skulachev, V. P. (1996) H+/e–stoichiometry for NADH dehydrogenase I and dimethyl sulfoxide reductase in anaerobically grown Escherichia coli cells, J. Bacteriol., 178, 6233–6237.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Mayer, F., and Muller, V. (2014) Adaptations of anaerobic archaea to life under extreme energy limitation, FEMS Microbiol. Rev., 38, 449–472.

    Article  CAS  PubMed  Google Scholar 

  70. Castro, P. J., Silva, A. F., Marreiros, B. C., Batista, A. P., and Pereira, M. M. (2016) Respiratory complex I: a dual relation with H+ and Na+? Biochim. Biophys. Acta, 1857, 928–937.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119991, Moscow, Russia

    G. E. Novakovsky & A. Y. Mulkidjanian

  2. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    D. V. Dibrova & A. Y. Mulkidjanian

  3. Department of Physics, Osnabrueck University, 49069, Osnabrueck, Germany

    A. Y. Mulkidjanian

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  1. G. E. Novakovsky
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  2. D. V. Dibrova
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Original Russian Text © G. E. Novakovsky, D. V. Dibrova, A. Y. Mulkidjanian, 2016, published in Biokhimiya, 2016, Vol. 81, No. 6, pp. 813-829.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM15-403, June 28, 2016.

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Novakovsky, G.E., Dibrova, D.V. & Mulkidjanian, A.Y. Phylogenomic analysis of type 1 NADH:Quinone oxidoreductase. Biochemistry Moscow 81, 770–784 (2016). https://doi.org/10.1134/S0006297916070142

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