Conserved evolutionary units in the hemecopper oxidase superfamily revealed by novel homologous protein families

Protein Science

Volumn 23, Issue 9, 2014, Pages 1220-1234

  Pei, Jimin ^a   Li, Wenlin ^a,b   Kinch, Lisa N ^a   Grishin, Nick V ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Denitrification; Detoxification; Gene duplication; Gene fusion and fission; HCO homology proteins; Heme copper oxidase superfamily; MAPEG proteins

Indexed keywords

COPPER OXIDASE; HEME; NITRIC-OXIDE REDUCTASE; OXIDOREDUCTASE;

BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; SEQUENCE HOMOLOGY;

BIOCATALYSIS; EVOLUTION, MOLECULAR; HEME; MODELS, MOLECULAR; OXIDOREDUCTASES; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84906852609     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2503     Document Type: Article

References (73)

1. 2 is required by complex life on habitable planets and the concept of planetary "oxygenation time". Astrobiology 5:415-438.
2. Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M, Krause RA Jr, Lyons SK, McClain CR, McShea DW, Novack-Gottshall PM, Smith FA, Stempien JA, Wang SC (2009) Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc Natl Acad Sci USA 106:24-27.
3. Dahl TW, Hammarlund EU, Anbar AD, Bond DP, Gill BC, Gordon GW, Knoll AH, Nielsen AT, Schovsbo NH, Canfield DE (2010) Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proc Natl Acad Sci USA 107: 17911-17915.
4. Gribaldo S, Talla E, Brochier-Armanet C (2009) Evolution of the haem copper oxidases superfamily: A rooting tale. Trends Biochem Sci 34:375-381.
5. Pereira MM, Santana M, Teixeira M (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 1505:185-208.
6. van der Oost J, de Boer AP, de Gier JW, Zumft WG, Stouthamer AH, van Spanning RJ. The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol Lett 121:1-9.
7. Richter OM, Ludwig B (2003) Cytochrome c oxidase-structure, function, and physiology of a redox-driven molecular machine. Rev Physiol Biochem Pharmacol 147:47-74.
8. Ferguson-Miller S, Babcock GT (1996) Heme/copper terminal oxidases. Chem Rev 96:2889-2908.
9. Michel H, Behr J, Harrenga A, Kannt A (1998) Cytochrome c oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329-356.
10. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660-669.
11. Sousa FL, Alves RJ, Ribeiro MA, Pereira-Leal JB, Teixeira M, Pereira MM (2012) The superfamily of heme-copper oxygen reductases: Types and evolutionary considerations. Biochim Biophys Acta 1817:629-637.
12. Brochier-Armanet C, Talla E, Gribaldo S (2009) The multiple evolutionary histories of dioxygen reductases: Implications for the origin and evolution of aerobic respiration. Mol Biol Evol 26:285-297.
13. Gennis RB (1998) Multiple proton-conducting pathways in cytochrome oxidase and a proposed role for the activesite tyrosine. Biochim Biophys Acta 1365:241-248.
14. Rauhamaki V, Baumann M, Soliymani R, Puustinen A, Wikstrom M (2006) Identification of a histidinetyrosine cross-link in the active site of the cbb3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 103:16135-16140.
15. Hemp J, Christian C, Barquera B, Gennis RB, Martinez TJ (2005) Helix switching of a key active-site residue in the cytochrome cbb3 oxidases. Biochemistry 44:10766-10775.
16. 2O generation by bacterial nitric oxide reductase. Science 330:1666-1670.
17. 2O in the nitrogen cycle. Science 330:1632-1633.
18. Hendriks J, Gohlke U, Saraste M (1998) From NO to OO: nitric oxide and dioxygen in bacterial respiration. J Bioenerg Biomembr 30:15-24.
19. Stevanin TM, Laver JR, Poole RK, Moir JW, Read RC (2007) Metabolism of nitric oxide by Neisseriameningitidis modifies release of NO-regulated cytokines and chemokines by human macrophages. Microbes Infect 9:981-987.
20. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M (2000) Nitric oxide reductases in bacteria. Biochim Biophys Acta 1459:266-273.
21. Sousa FL, Alves RJ, Pereira-Leal JB, Teixeira M, Pereira MM (2011) A bioinformatics classifier and database for heme-copper oxygen reductases. PLoS One 6:e19117.
22. Castresana J, Lubben M, Saraste M, Higgins DG (1994) Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J 13:2516-2525.
23. de Vries S, Schroder I (2002) Comparison between the nitric oxide reductase family and its aerobic relatives, the cytochrome oxidases. Biochem Soc Trans 30:662- 667.
24. Ducluzeau AL, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34:9-15.
25. Castresana J, Saraste M (1995) Evolution of energetic metabolism: The respiration-early hypothesis. Trends Biochem Sci 20:443-448.
26. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
27. Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244-248.
28. Jakobsson PJ, Morgenstern R, Mancini J, Ford- Hutchinson A, Persson B (1999) Common structural features of MAPEG-a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci 8:689-692.
29. Holm PJ, Bhakat P, Jegerschold C, Gyobu N, Mitsuoka K, Fujiyoshi Y, Morgenstern R, Hebert H (2006) Structural basis for detoxification and oxidative stress protection in membranes. J Mol Biol 360:934-945.
30. Frickey T, Lupas A (2004) CLANS: A Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20:3702-3704.
31. Oliveira F, de Carvalho AM, de Oliveira CI (2013) Sand-fly saliva-man: The trigger trio. Frontiers Immunol 4:375.
32. Vannier-Santos MA, Martiny A, de Souza W (2002) Cell biology of Leishmania spp.: invading and evading. Curr Pharma Des 8:297-318.
33. Koreny L, Lukes J, Obornik M (2010) Evolution of the haem synthetic pathway in kinetoplastid flagellates: An essential pathway that is not essential after all? Intl J Parasitol 40:149-156.
34. Campos-Salinas J, Cabello-Donayre M, Garcia- Hernandez R, Perez-Victoria I, Castanys S, Gamarro F, Perez-Victoria JM (2011) A new ATP-binding cassette protein is involved in intracellular haem trafficking in Leishmania. Mol Microbiol 79:1430-1444.
35. Huynh C, Yuan X, Miguel DC, Renberg RL, Protchenko O, Philpott CC, Hamza I, Andrews NW (2012) Heme uptake by Leishmania amazonensis is mediated by the transmembrane protein LHR1. PLoS Pathog 8:e1002795.
36. Dutta S, Furuyama K, Sassa S, Chang KP (2008) Leishmania spp.: delta-aminolevulinate-inducible neogenesis of porphyria by genetic complementation of incomplete heme biosynthesis pathway. Exp Parasitol 118:629-636.
37. Chang CS, Chang KP (1985) Heme requirement and acquisition by extracellular and intracellular stages of Leishmania mexicana amazonensis. Mol Biochem Parasitol 16:267-276.
38. Anzaldi LL, Skaar EP (2010) Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect Immun 78:4977-4989.
39. Kwiatkowski AV, Laratta WP, Toffanin A, Shapleigh JP (1997) Analysis of the role of the nnrR gene product in the response of Rhodobacter sphaeroides 2.4.1 to exogenous nitric oxide. J Bacteriol 179:5618-5620.
40. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) STRING v9.1: proteinprotein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808-D815.
41. Bartnikas TB, Wang Y, Bobo T, Veselov A, Scholes CP, Shapleigh JP (2002) Characterization of a member of the NnrR regulon in Rhodobacter sphaeroides 2.4.3 encoding a haem-copper protein.Microbiology 148:825-833.
42. Stern AM, Hay AJ, Liu Z, Desland FA, Zhang J, Zhong Z, Zhu J (2012) The NorR regulon is critical for Vibrio cholerae resistance to nitric oxide and sustained colonization of the intestines. MBio 3:e00013-00012.
43. Stern AM, Liu B, Bakken LR, Shapleigh JP, Zhu J (2013) A novel protein protects bacterial irondependent metabolism from nitric oxide. J Bacteriol 195:4702-4708.
44. Jamet A, Euphrasie D, Martin P, Nassif X (2013) Identification of genes involved in Neisseria meningitidis colonization. Infect Immun 81:3375-3381.
45. Cozen AE, Weirauch MT, Pollard KS, Bernick DL, Stuart JM, Lowe TM (2009) Transcriptional map of respiratory versatility in the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. J Bacteriol 191: 782-794.
46. French CE, Bell JM, Ward FB (2008) Diversity and distribution of hemerythrin-like proteins in prokaryotes. FEMS Microbiol Lett 279:131-145.
47. Overton TW, Justino MC, Li Y, Baptista JM, Melo AM, Cole JA, Saraiva LM (2008) Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J Bacteriol 190:2004-2013.
48. Frey AD, Kallio PT (2005) Nitric oxide detoxification- A new era for bacterial globins in biotechnology? Trends Biotechnol 23:69-73.
49. Lo Conte L, Ailey B, Hubbard TJ, Brenner SE, Murzin AG, Chothia C (2000) SCOP: A structural classification of proteins database. Nucleic Acids Res 28:257-259.
50. Kim BH, Cheng H, Grishin NV (2009) HorA web server to infer homology between proteins using sequence and structural similarity. Nucleic Acids Res 37:W532-W538.
51. Cheng H, Kim BH, Grishin NV (2008) Discrimination between distant homologs and structural analogs: lessons from manually constructed, reliable data sets. J Mol Biol 377:1265-1278.
52. Martinez Molina D, Wetterholm A, Kohl A, McCarthy AA, Niegowski D, Ohlson E, Hammarberg T, Eshaghi S, Haeggstrom JZ, Nordlund P (2007) Structural basis for synthesis of inflammatory mediators by human leukotriene C4 synthase. Nature 448:613-616.
53. Martinez Molina D, Eshaghi S, Nordlund P (2008) Catalysis within the lipid bilayer-structure and mechanism of the MAPEG family of integral membrane proteins. Curr Opin Struct Biol 18:442-449.
54. Ohno S (1970) Evolution by Gene Duplication. Springer-Verlag, New York.
55. Kummerfeld SK, Teichmann SA (2005) Relative rates of gene fusion and fission in multi-domain proteins. Trends Genet 21:25-30.
56. Pasek S, Risler JL, Brezellec P (2006) Gene fusion/fission is a major contributor to evolution of multi-domain bacterial proteins. Bioinformatics 22:1418-1423.
57. Goodsell DS, Olson AJ (2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29: 105-153.
58. Levy ED, Boeri Erba E, Robinson CV, Teichmann SA (2008) Assembly reflects evolution of protein complexes. Nature 453:1262-1265.
59. Lynch M (2012) The evolution of multimeric protein assemblages. Mol Biol Evol 29:1353-1366.
60. Bouzat JL, McNeil LK, Robertson HM, Solter LF, Nixon JE, Beever JE, Gaskins HR, Olsen G, Subramaniam S, Sogin ML, Lewin HA (2000) Phylogenomic analysis of the alpha proteasome gene family from early-diverging eukaryotes. J Mol Evol 51:532-543.
61. Archibald JM, Logsdon JM Jr, Doolittle WF. Origin and evolution of eukaryotic chaperonins: phylogenetic evidence for ancient duplications in CCT genes (2000) Mol Biol Evol 17:1456-1466.
62. Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8:R51.
63. Choi S, Jeon J, Yang JS, Kim S (2008) Common occurrence of internal repeat symmetry in membrane proteins. Proteins 71:68-80.
64. Duran AM, Meiler J (2013) Inverted topologies in membrane proteins: A mini-review. Comput Struct Biotechnol J 8:e201308004.
65. Rose PW, Bi C, Bluhm WF, Christie CH, Dimitropoulos D, Dutta S, Green RK, Goodsell DS, Prlic A, Quesada M, Quinn GB, Ramos AG, Westbrook JD, Young J, Zardecki C, Berman HM, Bourne PE (2013) The RCSB Protein Data Bank: new resources for research and education. Nucleic Acids Res 41:D475-D482.
66. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: The protein families database. Nucleic Acids Res 42:D222-D230.
67. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH (2013) CDD: conserved domains and protein threedimensional structure. Nucleic Acids Res 41:D348- D352.
68. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195.
69. Pei J, Kim BH, Grishin NV (2008) PROMALS3D: A tool for multiple protein sequence and structure alignments. Nucleic Acids Res 36:2295-2300.
70. Holm L, Park J (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16:566-567.
71. Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM (2006) MUSTANG: A multiple structural alignment algorithm. Proteins 64:559-574.
72. Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res 35:W429-432.
73. Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Intl Conf Intellig Syst Mol Biol 6:175-182.