The molecular evolution of catalatic hydroperoxidases: Evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota

Molecular Biology and Evolution

Volumn 20, Issue 7, 2003, Pages 1098-1112

  Klotz, Martin G ^b   Loewen, Peter C ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b NONE

Author keywords

Catalase; Catalase peroxidase; Lateral gene transfer; Nonheme catalase

Indexed keywords

CATALASE; CATALATIC HYDROPEROXIDASE; ENZYME; PEROXIDASE; UNCLASSIFIED DRUG;

ALGA; AMINO ACID SEQUENCE; ARTICLE; BACTERIUM; ENZYME ACTIVITY; EUKARYOTE EVOLUTION; EVIDENCE BASED MEDICINE; FUNGUS; GENETIC CODE; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT; PROKARYOTE; UNINDEXED SEQUENCE;

ALGAE; BACTERIA; CATALASE; CATALYSIS; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; FUNGI; GENE TRANSFER, HORIZONTAL; GENOME; HEME; PHYLOGENY; PLANTS; PROTEINS;

ALGAE; BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI; PROKARYOTA; PROTISTA;

EID: 0038613121     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg129     Document Type: Article

References (80)

1. Allgood, G. S., and J. J. Perry. 1986. Characterization of a manganese-containing catalase from the obligate thermophile Thermophilum album. J. Bacteriol. 168:563-567.
2. Almarsson, O., A. Sinha, E. Gopinath, and T. C. Bruice. 1993. Mechanism of one-electron oxidation of NAD(P)H and function of NADPH bound to catalase. J. Am. Chem. Soc. 115:7093-7102.
3. Ames, B. N. 1995. Understanding the causes of aging and cancer. Microbiologia 11:305-308.
4. Amo, T., H. Atomi, and T. Imanaka. 2002. Unique presence of a manganese catalase in a hyperthermophilic Archaeon, Pyrobaculum calidifontis VA1. J. Bacteriol. 184:3305-3312.
5. Andersson, J. O., and A. J. Roger. 2002. Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions, and Prokaryote-to-Eukaryote lateral gene transfers. Eukaryotic Cell 1:304-310.
6. Bansal, A. K., and T. E. Meyer. 2002. Evolutionary analysis by whole-genome comparisons. J. Bacteriol. 184:2260-2272.
7. Carpena, X., M. Soriano, M. G. Klotz, L. Donald, I. Fita, and P. C. Loewen. 2002. Structure of the clade I catalase, CatF of Pseudomonas syringae, at 1.8 Å resolution. Proteins 50:423-436.
8. Cavalier-Smith, T. 2002a. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol. 52:7-76.
9. -. 2002b. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
10. Deppenmeier, U., A. Johann, T. Hartsch et al. (22 co-authors). 2002. The genome of Methanosarcina mazei: Evidence for lateral gene transfer between Bacteria and Archaea. J. Mol. Microbiol. Biotechnol. 4:453-461.
11. Doolittle, W. F. 1999. Phylogenetic classification and the universal tree. Science 284:2124-2129.
12. Embley, T. M., and W. Martin. 1998. A hydrogen-producing mitochondrion. Nature 392:37-41.
13. Epstein, P. N., P. A. Overbeek, and A. N. Means. 1989. Calmodulin-induced early-onset diabetes in transgenic mice. Cell 58:1067-1073.
14. Faguy, D. M., and W. F. Doolittle. 2000. Horizontal transfer of catalase-peroxidase genes between Archaea and pathgogenic bacteria. Trends Genet. 16:196-197.
15. Felsenstein, J. 1994. PHYLIP (phylogeny inference package). Version 3.5. User manual. Washington University, St. Louis, Mo.
16. Frugoli, J. A., M. A. McPeek, T. L. Thomas, and C. R. McClung. 1998. Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics 149:355-365.
17. Frugoli, J. A., H. H. Zhong, M. L. Nuccio, P. McCourt, M. A. McPeek, T. L. Thomas, and C. R. McClung. 1996. Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 112:327-336.
18. Gogarten, J. P., W. F. Doolittle, and J. G. Lawrence. 2002. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19:2226-2238.
19. Guan, L., and J. G. Scandalios. 1996. Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. J. Mol. Evol. 42:570-579.
20. Gupta, R. S. 1998. Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62:1435-1491.
21. Hartman, H., and A. Fedorov. 2002. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl. Acad. Sci. USA 99:1420-1425.
22. Hayman, G. T., and P. L. Bolen. 1993. Movement of shuttle plasmids from Escherichia coli into yeasts other than Saccharomyces cerevisiae using trans-kingdom conjugation. Plasmid 30:251-257.
23. Henkle-Dührsen, K., V. H. O. Eckelt, G. Wildenburg, M. Blaxter, and R. D. Walter. 1998. Gene structure, activity and localization of a catalase from intracellular bacteria in Onchocerca volvulus. Mol. Biochem. Parasitol. 96:69-81.
24. Henze, K., and W. Martin. 2001. How do mitochondrial genes get into the nucleus? Trends Genet. 17.
25. 2. Biochem. J. 354:107-114.
26. Hillar, A., P. Nicholls, J. L. Switala, and P. C. Loewen. 1994. NADPH binding and control of catalase compound II formation: comparison of bovine, yeast and Escherichia coli enzymes. Biochem. J. 300:531-539.
27. Hiner, A. N. P., J. Hernandez-Ruiz, G. A. Williams, M. B. Arnao, F. Garcia-Canovas, and M. Acosta. 2001. Catalase-like oxygen production by horseradish peroxidase must predominantly be an enzyme-catalyzed reaction. Arch. Biochem. Biophys. 392:295-302.
28. Imlay, J. A., S. M. Chin, and S. Linn. 1988. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240:640-642.
29. Ishikawa, T., Y. Ohta, T. Takeda, S. Shigeoka, and M. Nishikimi. 1998. Increased cellular resistance to oxidative stress by expression of cyanobacterium catalase-peroxidase in animal cells. FEBS Lett. 426:221-224.
30. Jespersen, H. M., V. H. Kjaersgård, L. Østergaard, and K. G. Welinder. 1997. From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem. J. 326:305-310.
31. Johnson, C. H., M. G. Klotz, J. L. York, V. Kruft, and J. E. McEwen. 2002. Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148:1129-1142.
32. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
33. Jones, P., and I. Wilson. 1978. Catalases and iron complexes with catalase-like properties, Vol. 7. Marcel Dekker, New York.
34. Kang, Y. J., Y. Chen, and P. N. Epstein. 1996. Suppression of doxorubicin cardiotoxicity by overexpression of catalase in the heart of transgenic mice. J. Biol Chem. 271:12610-12616.
35. Kawasaki, L., and J. Aguirre. 2001. Multiple catalase genes are differentially regulated in Aspergillus nidulans. J. Bacteriol. 183:1434-1440.
36. Kawasaki, L., D. Wysong, R. Diamond, and J. Aguirre. 1997. Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J. Bacteriol. 179:3284-3292.
37. Kim, J. A., Z. Sha, and J. E. Mayfield. 2000. Regulation of Brucella abortus catalase. Infect. Immun. 68:3861-3866.
38. Kirkman, H. N., and G. F. Gaetani. 1984. Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH. Proc. Natl. Acad. Sci. USA 81:4343-4347.
39. Klotz, M., G. Klassen, and P. Loewen. 1997. Phylogenetic relationships among prokaryotic and eukaryotic catalases. Mol. Biol. Evol. 14:951-958.
40. Kono, Y., and I. Fridovich. 1983. Isolation and characterization of the pseudocatalase of Lactobacillus plantarum: a new manganese containing enzyme. J. Biol. Chem. 258:6015-6019.
41. Lawrence, J. G., R. W. Hendrix, and S. Casjens. 2001. Where are the pseudogenes in bacterial genomes? Trends Microbiol. 9:535-540.
42. Loew, O. 1900. Physiological studies of Connecticut leaf tobacco. U.S. Dept of Agri Repts. 65:5-57.
43. Loewen, P. C. 1997. Bacterial catalases. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Loewen, P. C., M. G. Klotz, and D. J. Hassett. 2000. Catalase an "old" enzyme that continues to surprise us. ASM News 66:76-82.
45. Ma, J. F., U. A. Ochsner, M. G. Klotz, V. K. Nanayakkara, M. L. Howell, Z. Johnson, J. E. Posey, M. L. Vasil, J. J. Monaco, and D. J. Hassett. 1999. Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa. J. Bacteriol. 181:3730-3742.
46. Makarova, K. S., L. Aravind, Y. I. Wolf, R. L. Tatusov, K. W. Minton, E. V. Koonin, and M. J. Daly. 2001. Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev. 65:44-79.
47. Martin, W., and M. Müller. 1998. The hydrogen hypothesis for the first Eukaryote. Nature 392:37-41.
48. Mayfield, J. E., and M. R. Duvall. 1996. Anomalous phylogenies based on bacterial catalase gene sequences. J. Mol. Evol. 42:469-471.
49. Mayr, E. 1998. Two empires or three? Proc. Natl. Acad. Sci. USA 95:9720-9723.
50. McCord, J. M., J. Keele, B. B., and I. Fridovich. 1971. An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc. Natl. Acad. Sci. USA 68:1024-1027.
51. Müller, M., and W. Martin. 1999. The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes. Bioessays 21:377-381.
52. Nesbø, C. L., S. L'Haridon, K. O. Stetter, and W. F. Doolittle. 2001. Phylogenetic analysis of two "archaeal" genes in Thermotoga maritima reveal multiple transfers berween Archaea and bacteria. Mol. Biol. Evol. 18:362-375.
53. Nicholls, P., I. Fita, and P. C. Loewen. 2001. Enzymology and structure of catalases. Adv. Inorg. Chem. 51:51-106.
54. Nixon, J. E. J., A. Wang, J. Field, H. G. Morrison, A. G. McArthur, M. L. Sogin, B. J. Loftus, and J. Samuelson. 2002. Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic Prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryotic Cell 1:181-190.
55. Ochman, H., J. G. Lawrence, and A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299-304.
56. Olsen, G. J., C. R. Woese, and R. Overbeek. 1994. The winds of (evolutionary) change: breathing new life into microbiology. J. Bacteriol. 177:1-6.
57. Richter, H. E., and P. C. Loewen. 1982. Rapid inactivation of bacteriophage T7 by ascorbic acid is repairable. Biochim. Biophys. Acta 697:25-30.
58. Rotte, C., K. Henze, M. Müller, and W. Martin. 2000. Origins of hydrogenosomes and mitochondria. Curr. Opin. Microbiol. 3:481-486.
59. Scandalios, J. G., L. Guan, and A. N. Polidoros. 1997. Catalase in plants: gene structure, properties, regulation, and expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. Schubert, J., and J. W. Wilmer. 1991. Does hydrogen peroxide exist "free' in biological systems? Free Radic. Biol. Med. 11:545-555.
61. Seaver, L. C., and J. A. Imlay. 2001a. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-7181.
62. -. 2001b. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183:7182-7189.
63. Sprague, J., G.F. 1991. Genetic exchange between kingdoms. Curr. Opin. Genet. Dev. 1:530-533.
64. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
65. Sumner, J. B., and A. L. Dounce. 1937. Crystalline catalase. J. Biol. Chem. 121:417-424.
66. Sun, W., T. A. Kadima, M. A. Pickard, and H. B. Dunford. 1994. Catalase activity of chloroperoxidase and its interaction with peroxidase activity. Biochem. Cell. Biol. 72:321-331.
67. Sutherland, M. W. 1991. The generation of oxygen radicals during host plant responses to infection. Mol. Physiol. Plant Pathol. 39:79-93.
68. Switala, J., J. O. O'Neil, and P. C. Loewen. 1999. Catalase HPII from Escherichia coli exhibits enhanced resistance to denaturation. Biochemistry 38:3895-901.
69. Swofford, D. L. 1999. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0.b8. Sinauer Associates, Sunderland, Mass.
70. Thomas, J. A., D. R. Morris, and L. P. Hager. 1970. Chloroperoxidase. VII. Classical peroxidatic, catalatic and halogenating forms of the enzyme. J. Biol. Chem. 245:3129-3134.
71. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
72. Waldo, G. S., R. M. Fronko, and J. E. Penner-Hahn. 1991. Inactivation and reactivation of manganese catalase: oxidation-state assignments using X-ray absorption spectroscopy. Biochemistry 30:10486-10490.
73. Welinder, K. G. 1991. Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily. Biochim. Biophys. Acta 1080:215-220.
74. -. 1992. Superfamily of plant, fungal and bacterial peroxidases. Curr. Opin. Struct. Biol. 2:388-393.
75. White, O., J. A. Eisen, J. F. Heidelberg et al. (33 co-authors). 1999. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571-1577.
76. Whittaker, M. M., V. V. Barynin, S. V. Antonyuk, and J. W. Whittaker. 1999. The oxidized (3,3) state of manganese catalase: comparison of enzymes from Thermus thermophilus and Lactobacillus pantarum. Biochemistry 38:9126-9136.
77. Woese, C. R. 1987. Bacterial evolution. Microbiol. Rev. 51:221-271.
78. Wolf, Y. I., I. B. Rogozin, N. V. Grishin, and E. V. Koonin. 2002. Genome trees and the tree of life. Trends Genet. 18:472-478.
79. Zamocky, M., and F. Koller. 1999. Understanding the structure and function of catalases: clues from molecular evolution and in vitro mutagenesis. Prog. Biophys. Mol. Biol. 72:19-66.
80. Zamocky, M., G. Regelsberger, C. Jakopitsch, and C. Obinger. 2001. The molecular peculiarities of catalase-peroxidases. FEBS Lett. 492:177-182.