Discovery of a gene involved in a third bacterial protoporphyrinogen oxidase activity through comparative genomic analysis and functional complementation

Applied and Environmental Microbiology

Volumn 77, Issue 14, 2011, Pages 4795-4801

  Boynton, Tye O ^a   Gerdes, Svetlana ^b   Craven, Sarah H ^a   Neidle, Ellen L ^a   Phillips, John D ^c   Dailey, Harry A ^a,d  

^a UNIVERSITY OF GEORGIA   (United States)

^b Fellowship for Interpretation of Genomes   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d University of Georgia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACINETOBACTERS; AMINO ACID SEQUENCE; AUXOTROPHY; BIOSYNTHETIC GENE; BIOSYNTHETIC PATHWAY; CELL EXTRACTS; COMPARATIVE GENOMIC; COMPARATIVE GENOMICS; COMPLEMENTATION; EXPERIMENTAL VERIFICATION; GENOMIC ANALYSIS; HEME BIOSYNTHESIS; HUMAN GENES; LIVING ORGANISMS; MYXOCOCCUS XANTHUS; PROTEIN FAMILY; PROTOPORPHYRINOGEN OXIDASE; TETRAPYRROLES;

AEROBIC BACTERIA; AMINO ACIDS; BACTERIOLOGY; BIOCHEMISTRY; BIOSYNTHESIS; CATALYSTS; CELL CULTURE; ENZYMES; ESCHERICHIA COLI; PORPHYRINS;

GENE ENCODING;

BACTERIAL DNA; ESCHERICHIA COLI PROTEIN; HEME; HEMG PROTEIN, E COLI; PROTOPORPHYRINOGEN OXIDASE;

AMINO ACID; BACTERIUM; COMPARATIVE STUDY; ENZYME ACTIVITY; FACULTATIVE BEHAVIOR; GENETIC ANALYSIS; GENOMICS; IRON; OXIC CONDITIONS; PLASMID; PROTEIN;

ACINETOBACTER; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BIOSYNTHESIS; COMPARATIVE STUDY; ENZYMOLOGY; ESCHERICHIA COLI; GENE DELETION; GENE INACTIVATION; GENETICS; METABOLISM; MYXOCOCCUS XANTHUS; PHYLOGENY;

ACINETOBACTER; AMINO ACID SEQUENCE; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; GENOME, BACTERIAL; HEME; MYXOCOCCUS XANTHUS; PHYLOGENY; PROTOPORPHYRINOGEN OXIDASE; SEQUENCE DELETION;

ACINETOBACTER; ACINETOBACTER BAYLYI; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MYXOCOCCUS XANTHUS;

EID: 79961062855     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00171-11     Document Type: Article

References (51)

1. Bentley, S. D., et al. 2003. Sequencing and analysis of the genome of the Whipple's disease bacterium Tropheryma whipplei. Lancet 361:637-644.
2. Boynton, T. O., L. E. Daugherty, T. A. Dailey, and H. A. Dailey. 2009. Identification of Escherichia coli HemG as a novel, menadione-dependent flavodoxin with protoporphyrinogen oxidase activity. Biochemistry 48:6705-6711.
3. Breckau, D., E. Mahlitz, A. Sauerwald, G. Layer, and D. Jahn. 2003. Oxygendependent coproporphyrinogen III oxidase (HemF) from Escherichia coli is stimulated by manganese. J. Biol. Chem. 278:46625-46631.
4. Chance, B. 1972. The nature of electron transfer and energy coupling reactions. FEBS Lett. 23:3-20.
5. Collier, L. S., G. L. Gaines III, and E. L. Neidle. 1998. Regulation of benzoate degradation in Acinetobacter sp. strain ADP1 by BenM, a LysRtype transcriptional activator. J. Bacteriol. 180:2493-2501.
6. Corradi, H. R., et al. 2006. Crystal structure of protoporphyrinogen oxidase from Myxococcus xanthus and its complex with the inhibitor acifluorfen. J. Biol. Chem. 281:38625-38633.
7. Dailey, H. A., and T. A. Dailey. 1996. Protoporphyrinogen oxidase of Myxococcus xanthus. Expression, purification, and characterization of the cloned enzyme. J. Biol. Chem. 271:8714-8718.
8. Dailey, T. A., et al. 2010. Discovery and characterization of HemQ: an essential heme biosynthetic pathway component. J. Biol. Chem. 285:25978-25986.
9. Dailey, T. A., and H. A. Dailey. 1996. Human protoporphyrinogen oxidase: expression, purification, and characterization of the cloned enzyme. Protein Sci. 5:98-105.
10. Dailey, T. A., H. A. Dailey, P. Meissner, and A. R. Prasad. 1995. Cloning, sequence, and expression of mouse protoporphyrinogen oxidase. Arch. Biochem. Biophys. 324:379-384.
11. de Berardinis, V., et al. 2008. A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Mol. Syst. Biol. 4:174.
12. Foster, J., et al. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3:e121.
13. Franklin, M. R., J. D. Phillips, and J. P. Kushner. 1997. Cytochrome P450 induction, uroporphyrinogen decarboxylase depression, porphyrin accumulation and excretion, and gender influence in a 3-week rat model of porphyria cutanea tarda. Toxicol. Appl. Pharmacol. 147:289-299.
14. Galperin, M. Y., and E. V. Koonin. 2000. Who's your neighbor? New computational approaches for functional genomics. Nat. Biotechnol. 18:609-613.
15. Gilles-Gonzalez, M. A. 2001. Oxygen signal transduction. IUBMB Life 51: 165-173.
16. Hanson, A. D., A. Pribat, J. C. Waller, and V. de Crecy-Lagard. 2010. 'Unknown' proteins and 'orphan' enzymes: the missing half of the engineering parts list-and how to find it. Biochem. J. 425:1-11.
17. Harrington, E. D., et al. 2007. Quantitative assessment of protein function prediction from metagenomics shotgun sequences. Proc. Natl. Acad. Sci. U. S. A. 104:13913-13918.
18. Ioanoviciu, A., Y. T. Meharenna, T. L. Poulos, and P. R. Ortiz de Montellano. 2009. DevS oxy complex stability identifies this heme protein as a gas sensor in Mycobacterium tuberculosis dormancy. Biochemistry 48:5839-5848.
19. Ishida, T., et al. 1998. A primitive pathway of porphyrin biosynthesis and enzymology in Desulfovibrio vulgaris. Proc. Natl. Acad. Sci. U. S. A. 95:4853-4858.
20. Jacobs, N. J., and J. M. Jacobs. 1977. Evidence for involvement of the electron transport system at a late step of anaerobic microbial heme synthesis. Biochim. Biophys. Acta 459:141-144.
21. Jahn, D., and D. W. Heinz. 2009. Biosynthesis of 5-aminolevulinic acid, p. 29-42. In M. J. Warren and A. G. Smith (ed.), Tetrapyrroles: birth, life, and death. Landes Bioscience, Austin, TX.
22. Jordan, P. M. 1990. The biosynthesis of 5-aminolevulinic acid and its transformation in coproporphyrinogen in animals and bacteria, p. 55-121. In H. A. Dailey (ed.), Biosynthesis of heme and chlorophylls. McGraw-Hill, New York, NY.
23. Juni, E., and A. Janik. 1969. Transformation of Acinetobacter calco-aceticus (Bacterium anitratum). J. Bacteriol. 98:281-288.
24. Kato, K., R. Tanaka, S. Sano, A. Tanaka, and H. Hosaka. 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.
25. Korený, L., J. Lukes, and M. Obornik. 2010. Evolution of the haem synthetic pathway in kinetoplastid flagellates: an essential pathway that is not essential after all? Int. J. Parasitol. 40:149-156.
26. Kovach, M. E., R. W. Phillips, P. H. Elzer, R. M. Roop II, and K. M. Peterson. 1994. pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800-802.
27. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
28. La Scola, B., et al. 2001. Description of Tropheryma whipplei gen. nov., sp. nov., the Whipple's disease bacillus. Int. J. Syst. Evol. Microbiol. 51:1471-1479.
29. Layer, G., et al. 2006. The substrate radical of Escherichia coli oxygenindependent coproporphyrinogen III oxidase HemN. J. Biol. Chem. 281: 15727-15734.
30. Lermontova, I., E. Kruse, H. P. Mock, and B. Grimm. 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.
31. Lobo, S. A., A. Brindley, M. J. Warren, and L. M. Saraiva. 2009. Functional characterization of the early steps of tetrapyrrole biosynthesis and modification in Desulfovibrio vulgaris Hildenborough. Biochem. J. 420:317-325.
32. Matringe, M., J. M. Camadro, P. Labbe, and R. Scalla. 1989. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem. J. 260:231-235.
33. McNeil, L. K., et al. 2007. The National Microbial Pathogen Database Resource (NMPDR): a genomics platform based on subsystem annotation. Nucleic Acids Res. 35:D347-D353.
34. 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.
35. Narita, S., et al. 1996. Molecular cloning and characterization of a cDNA that encodes protoporphyrinogen oxidase of Arabidopsis thaliana. Gene 182: 169-175.
36. Osterman, A., and R. Overbeek. 2003. Missing genes in metabolic pathways: a comparative genomics approach. Curr. Opin. Chem. Biol. 7:238-251.
37. Osterman, A. L., and T. P. Begley. 2007. A subsystems-based approach to the identification of drug targets in bacterial pathogens. Prog. Drug Res. 64:131, 133-170.
38. Overbeek, R., et al. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702.
39. Overbeek, R., M. Fonstein, M. D'Souza, G. D. Pusch, and N. Maltsev. 1999. The use of gene clusters to infer functional coupling. Proc. Natl. Acad. Sci. U. S. A. 96:2896-2901.
40. Panek, H., and M. R. O'Brian. 2002. A whole genome view of prokaryotic haem biosynthesis. Microbiology 148:2273-2282.
41. Perutz, M. 1942. X-ray analysis of haemoglobin. Nature 149:491-494.
42. Raikhman, L. M., B. Annaev, O. N. Mamedniiazov, and E. G. Rozantsev. 1973. Molecular structure and mechanism of functioning of cytochrome P-450. Biofizika 18:228-234.
43. Rao, A. U., L. K. Carta, E. Lesuisse, and I. Hamza. 2005. Lack of heme synthesis in a free-living eukaryote. Proc. Natl. Acad. Sci. U. S. A. 102:4270-4275.
44. Sǎsǎrman, A., et al. 1979. Mapping of a new hem gene in Escherichia coli K12. J. Gen. Microbiol. 113:297-303.
45. Shepherd, M., and H. A. Dailey. 2005. A continuous fluorimetric assay for protoporphyrinogen oxidase by monitoring porphyrin accumulation. Anal. Biochem. 344:115-121.
46. Singleton, C., et al. 2010. Heme-responsive DNA binding by the global iron regulator Irr from Rhizobium leguminosarum. J. Biol. Chem. 285:16023-16031.
47. Storbeck, S., et al. 2010. A novel pathway for the biosynthesis of heme in Archaea: genome-based bioinformatic predictions and experimental evidence. Archaea 2010:175050.
48. Torres, V. J., et al. 2007. A Staphylococcus aureus regulatory system that responds to host heme and modulates virulence. Cell Host Microbe 1:109-119.
49. Wandersman, C., and P. Delepelaire. 2004. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58:611-647.
50. Wang, K. F., T. A. Dailey, and H. A. Dailey. 2001. Expression and characterization of the terminal heme synthetic enzymes from the hyperthermophile Aquifex aeolicus. FEMS Microbiol. Lett. 202:115-119.
51. Zámocký, M., P. G. Furtmuller, and C. Obinger. 2010. Evolution of structure and function of class I peroxidases. Arch. Biochem. Biophys. 500:45-57.