Molecular phylogeny and intricate evolutionary history of the three isofunctional enzymes involved in the oxidation of protoporphyrinogen IX

Genome Biology and Evolution

Volumn 6, Issue 8, 2014, Pages 2141-2155

  Kobayashi, Koichi ^a   Masuda, Tatsuru ^a   Tajima, Naoyuki ^a   Wada, Hajime ^a,b   Sato, Naoki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Heme; HemG; HemJ; HemY; Protoporphyrin IX; Tetrapyrrole

Indexed keywords

HEME; ISOENZYME; PROTOPORPHYRIN; PROTOPORPHYRINOGEN; PROTOPORPHYRINOGEN OXIDASE; TETRAPYRROLE DERIVATIVE;

ANIMAL; BACTERIUM; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PHYLOGENY; PLANT;

ANIMALS; BACTERIA; BIOSYNTHETIC PATHWAYS; HEME; ISOENZYMES; MODELS, MOLECULAR; OXIDATION-REDUCTION; PHYLOGENY; PLANTS; PROTOPORPHYRINOGEN OXIDASE; PROTOPORPHYRINS; TETRAPYRROLES;

EID: 84923177266     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu170     Document Type: Article

References (59)

1. Abicht HK, Martinez J, Layer G, Jahn D, Solioz M. 2012. Lactococcus lactis HemW (HemN) is a haem-binding protein with a putative role in haem trafficking. Biochem J. 442:335–343.
2. Adachi J, Hasegawa M. 1996. MOLPHY Version 2.3: programs for molecular phylogenetics based on maximum likelihood. Computer Science Monographs. Vol. 28. Tokyo (Japan): Institute of Statistical Mathematics. p. 1–150.
3. Boynton TO, et al. 2011. Discovery of a gene involved in a third bacterial protoporphyrinogen oxidase activity through comparative genomic analysis and functional complementation. Appl Environ Microbiol. 77:4795–4801.
4. Boynton TO, Daugherty LE, Dailey TA, Dailey HA. 2009. Identification of Escherichia coli HemG as a novel, menadione-dependent flavodoxin with protoporphyrinogen oxidase activity. Biochemistry 48: 6705–6711.
5. Camadro JM, Labbe P. 1996. Cloning and characterization of the yeast HEM14 gene coding for protoporphyrinogen oxidase, the molecular target of diphenyl ether-type herbicides. J Biol Chem. 271: 9120–9128.
6. Cavallaro G, Decaria L, Rosato A. 2008. Genome-based analysis of heme biosynthesis and uptake in prokaryotic systems. J Proteome Res. 7: 4946–4954.
7. Corradi HR, et al. 2006. Crystal structure of protoporphyrinogen oxidase from Myxococcus xanthus and its complex with the inhibitor acifluorfen. J Biol Chem. 281:38625–38633.
8. Corrigall AV, et al. 1998. Purification of and kinetic studies on a cloned protoporphyrinogen oxidase from the aerobic bacterium Bacillus subtilis. Arch Biochem Biophys. 358:251–256.
9. Dailey TA, Dailey HA. 1998. Identification of an FAD superfamily containing protoporphyrinogen oxidases, monoamine oxidases, and phytoene desaturase. Expression and characterization of phytoene desaturase of Myxococcus xanthus. J Biol Chem. 273:13658–13662.
10. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797.
11. Ferreiras GC, Andrew TL, Karr SW, Daileyg HA. 1988. Organization of the terminal two enzymes of the heme biosynthetic pathway. Orientation of protoporphyrinogen oxidase and evidence for a membrane complex. J Biol Chem. 263:3835–3839.
12. Galperin MY, Walker DR, Koonin EV. 1998. Analogous enzymes: independent inventions in enzyme evolution. Genome Res. 8:779–790.
13. Hansson M, Hederstedt L. 1992. Cloning and characterization of the Bacillus subtilis hemEHY gene cluster, which encodes protoheme IX biosynthetic enzymes. J Bacteriol. 174:8081–8093.
14. Hao G-F, et al. 2013. Computational and experimental insights into the mechanism of substrate recognition and feedback inhibition of protoporphyrinogen oxidase. PLoS One 8:e69198.
15. Heinemann IU, et al. 2007. Functional definition of the tobacco protoporphyrinogen IX oxidase substrate-binding site. Biochem J. 402: 575–580.
16. Heinemann IU, Jahn M, Jahn D. 2008. The biochemistry of heme biosynthesis. Arch Biochem Biophys. 474:238–251.
17. Jacobs JM, Jacobs NJ. 1993. Porphyrin accumulation and export by isolated barley (Hordeum vulgare) plastids (effect of diphenyl ether herbicides). Plant Physiol. 101:1181–1187.
18. Jobb G, von Haeseler A, Strimmer K. 2004. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 4:18.
19. Kato K, Tanaka R, Sano S, Tanaka A, Hosaka H. 2010. Identification of a gene essential for protoporphyrinogen IX oxidase activity in the cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci U S A. 107:16649–16654.
20. Koch M, et al. 2004. Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J. 23: 1720–1728.
21. Kraulis PJ. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr. 24: 946–950.
22. Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286–2288.
23. Lee HJ, Duke MV, Duke SO. 1993. Cellular localization of protoporphyrinogen-oxidizing activities of etiolated barley (Hordeum vulgare L.) leaves (relationship to mechanism of action of protoporphyrinogen oxidase-inhibiting herbicides). Plant Physiol. 102:881–889.
24. Lermontova I, Grimm B. 2006. Reduced activity of plastid protoporphyrinogen oxidase causes attenuated photodynamic damage during high-light compared to low-light exposure. Plant J. 48:499–510.
25. Lermontova I, Kruse E, Mock HP, Grimm B. 1997. Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci U S A. 94: 8895–8900.
26. Masoumi A, et al. 2008. Complex formation between protoporphyrinogen IX oxidase and ferrochelatase during haem biosynthesis in Thermosynechococcus elongatus. Microbiology 154:3707–3714.
27. Matringe M, Camadro J, Labbet P, Scalla R. 1989. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem J. 260:231–235.
28. Meissner PN, et al. 1996. A R59W mutation in human protoporphyrinogen oxidase results in decreased enzyme activity and is prevalent in South Africans with variegate porphyria. Nat Genet. 13:95–97.
29. Möbius K, et al. 2010. Heme biosynthesis is coupled to electron transport chains for energy generation. Proc Natl Acad Sci U S A. 107: 10436–10441.
30. Molina A, et al. 1999. Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J. 17:667–678.
31. Nagaraj VA, Arumugam R, Prasad D, Rangarajan PN, Padmanaban G. 2010. Protoporphyrinogen IX oxidase from Plasmodium falciparum is anaerobic and is localized to the mitochondrion. Mol Biochem Parasitol. 174:44–52.
32. Nowack ECM, Melkonian M, Glöckner G. 2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol. 18:410–418.
33. Oborník M, Green BR. 2005. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol. 22:2343–2353.
34. Omelchenko MV, Galperin MY, Wolf YI, Koonin EV. 2010. Non-homologous isofunctional enzymes: a systematic analysis of alternative solutions in enzyme evolution. Biol Direct. 5:31.
35. Panek H, Brian MRO. 2002. A whole genome view of prokaryotic haem biosynthesis. Microbiology 148:2273–2282.
36. Perrière G, Gouy M. 1996. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369.
37. Qin X, et al. 2010. Structural insight into unique properties of protoporphyrinogen oxidase from Bacillus subtilis. J Struct Biol. 170: 76–82.
38. Qin X, et al. 2011. Structural insight into human variegate porphyria disease. FASEB J. 25:653–664.
39. Rao AU, Carta LK, Lesuisse E, Hamza I. 2005. Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci U S A. 102:4270–4275.
40. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574.
41. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 234:779–815.
42. Sasaki NV, Sato N. 2010. Elucidating genome structure evolution by analysis of isoapostatic gene clusters using statistics of variance of gene distances. Genome Biol Evol. 2:1–12.
43. Sasarman A, et al. 1993. Nucleotide sequence of the hemG gene involved in the protoporphyrinogen oxidase activity of Escherichia coli K12. Can J Microbiol. 39:1155–1161.
44. Sato N. 2000. SISEQ: manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16:180–181.
45. Sato N. 2002. Comparative analysis of the genomes of Cyanobacteria and plants. Genome Inform. 13:173–182.
46. Sato N. 2009. Gclust: trans-kingdom classification of proteins using automatic individual threshold setting. Bioinformatics 25:599–605.
47. Sato N, Ishikawa M, Fujiwara M, Sonoike K. 2005. Mass identification of chloroplast proteins of endosymbiont origin by phylogenetic profiling based on organism-optimized homologous protein groups. Genome Inform. 16:56–68.
48. Shih PM, et al. 2013. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci U S A. 110:1053–1058.
49. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247.
50. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690.
51. Storbeck S, et al. 2010. A novel pathway for the biosynthesis of heme in Archaea: genome-based bioinformatic predictions and experimental evidence. Archaea 2010: Article ID 175050.
52. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596–1599.
53. Tanaka R, Kobayashi K, Masuda T. 2011. Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0145.
54. Tang K-H, et al. 2011. Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 12:334.
55. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680.
56. Warnich L. 1996. Identification of three mutations and associated haplotypes in the protoporphyrinogen oxidase gene in South African families with variegate porphyria. Hum Mol Genet. 5: 981–984.
57. Watanabe N, et al. 2001. Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem. 276:20474–20481.
58. Witkowski DA, Halling BP. 1989. Inhibition of plant protoporphyrinogen oxidase by the herbicide acifluorfen-methyl. Plant Physiol. 90: 1239–1242.
59. Xu K, Delling J, Elliott T. 1992. The genes required for heme synthesis in Salmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J Bacteriol. 174:3953–3963.