Anaerobic microbes: Oxygen detoxification without superoxide dismutase

Science

Volumn 286, Issue 5438, 1999, Pages 306-309

  Jenney Jr , Francis E ^a   Verhagen, Marc F J M ^a   Cui, Xiaoyuan ^a,b   Adams, Michael W W ^a  

^a University of Georgia ^*  (United States)

^b NATIONAL STARCH AND CHEMICAL COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDOREDUCTASE; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RUBREDOXIN; SUPEROXIDE DISMUTASE;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL METABOLISM; CATALYSIS; ENZYME ASSAY; NONHUMAN; OXYGEN TOXICITY; PRIORITY JOURNAL; PYROCOCCUS FURIOSUS; REACTION ANALYSIS;

ACETYLATION; AMINO ACID SEQUENCE; ANAEROBIOSIS; BACTERIA, ANAEROBIC; CATALYSIS; CYTOCHROME C GROUP; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; NADP; OXIDATION-REDUCTION; OXIDOREDUCTASES; PYROCOCCUS; RUBREDOXINS; SUPEROXIDE DISMUTASE; SUPEROXIDES; TEMPERATURE; WATER;

BACTERIA (MICROORGANISMS); PYROCOCCUS FURIOSUS;

EID: 0345109287     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.286.5438.306     Document Type: Article

References (71)

1. J. S. Valentine et al., Curr. Opin. Chem. Biol. 2, 253 (1998).
2. D. T. Sawyer and J. S. Valentine, Acc. Chem. Res. 14, 393 (1981).
3. C. Beauchamp and I. Fridovich, J. Biol. Chem. 245, 4641 (1970); I. Fridovich, J. Exp. Biol. 201, 1203 (1998).
4. C. Beauchamp and I. Fridovich, J. Biol. Chem. 245, 4641 (1970); I. Fridovich, J. Exp. Biol. 201, 1203 (1998).
5. J. M. McCord and I. Fridovich, J. Biol. Chem. 244, 6049 (1969); B. L. Stoddard, P. L. Howell, D. Ringe, G. A. Petsko, Biochemistry 29, 8885 (1990); M. L. Ludwig, A. L. Metzger, K. A. Pattridge, W. C. Stallings, J. Mol. Biol. 219, 335 (1991); J. A. Tainer, E. D. Getzoff, J. S. Richardson, D. C. Richardson, Nature 306, 284 (1983); S. B. Choudhury et al., Biochemistry 38, 3744 (1999).
6. J. M. McCord and I. Fridovich, J. Biol. Chem. 244, 6049 (1969); B. L. Stoddard, P. L. Howell, D. Ringe, G. A. Petsko, Biochemistry 29, 8885 (1990); M. L. Ludwig, A. L. Metzger, K. A. Pattridge, W. C. Stallings, J. Mol. Biol. 219, 335 (1991); J. A. Tainer, E. D. Getzoff, J. S. Richardson, D. C. Richardson, Nature 306, 284 (1983); S. B. Choudhury et al., Biochemistry 38, 3744 (1999).
7. J. M. McCord and I. Fridovich, J. Biol. Chem. 244, 6049 (1969); B. L. Stoddard, P. L. Howell, D. Ringe, G. A. Petsko, Biochemistry 29, 8885 (1990); M. L. Ludwig, A. L. Metzger, K. A. Pattridge, W. C. Stallings, J. Mol. Biol. 219, 335 (1991); J. A. Tainer, E. D. Getzoff, J. S. Richardson, D. C. Richardson, Nature 306, 284 (1983); S. B. Choudhury et al., Biochemistry 38, 3744 (1999).
8. J. M. McCord and I. Fridovich, J. Biol. Chem. 244, 6049 (1969); B. L. Stoddard, P. L. Howell, D. Ringe, G. A. Petsko, Biochemistry 29, 8885 (1990); M. L. Ludwig, A. L. Metzger, K. A. Pattridge, W. C. Stallings, J. Mol. Biol. 219, 335 (1991); J. A. Tainer, E. D. Getzoff, J. S. Richardson, D. C. Richardson, Nature 306, 284 (1983); S. B. Choudhury et al., Biochemistry 38, 3744 (1999).
9. J. M. McCord and I. Fridovich, J. Biol. Chem. 244, 6049 (1969); B. L. Stoddard, P. L. Howell, D. Ringe, G. A. Petsko, Biochemistry 29, 8885 (1990); M. L. Ludwig, A. L. Metzger, K. A. Pattridge, W. C. Stallings, J. Mol. Biol. 219, 335 (1991); J. A. Tainer, E. D. Getzoff, J. S. Richardson, D. C. Richardson, Nature 306, 284 (1983); S. B. Choudhury et al., Biochemistry 38, 3744 (1999).
10. B. Chance, H. Seis, A. Boveris, Physiol. Rev. 59, 527 (1979).
11. P. R. Ortiz de Montellano, Annu. Rev. Pharmacol. Toxicol. 32, 89 (1992).
12. A. M. Roberton and R. S. Wolfe, J. Bacteriol. 102, 43 (1970).
13. H. Cypionka, F. Widdel, N. Pfennig, FEMS Microbiol. Ecol. 31, 39 (1985).
14. M. S. Johnson, I. B. Zhulin, M.-E. R. Gapuzan, B. L. Taylor, J. Bacteriol. 179, 5598 (1997).
15. E. W. J. van Niel and J. C. Gottschal, Appl. Environ. Microbiol. 64, 1034 (1998).
16. K.-N. Lai and E. M. Gregory, GenBank direct submission, accession number M96560 (1992); E. R. Rocha, T. Selby, J. P. Coleman, C. J. Smith, J. Bacteriol. 178, 6895 (1996); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034841 (1997); M. Kitamura, S. Kojima, H. Akjtsu, I. Kumagai, T. Nakaya, GenBank direct submission, accession number AB020341 (1998); K. Nakayama, J. Bacteriol. 176, 1939 (1994).
17. K.-N. Lai and E. M. Gregory, GenBank direct submission, accession number M96560 (1992); E. R. Rocha, T. Selby, J. P. Coleman, C. J. Smith, J. Bacteriol. 178, 6895 (1996); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034841 (1997); M. Kitamura, S. Kojima, H. Akjtsu, I. Kumagai, T. Nakaya, GenBank direct submission, accession number AB020341 (1998); K. Nakayama, J. Bacteriol. 176, 1939 (1994).
18. K.-N. Lai and E. M. Gregory, GenBank direct submission, accession number M96560 (1992); E. R. Rocha, T. Selby, J. P. Coleman, C. J. Smith, J. Bacteriol. 178, 6895 (1996); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034841 (1997); M. Kitamura, S. Kojima, H. Akjtsu, I. Kumagai, T. Nakaya, GenBank direct submission, accession number AB020341 (1998); K. Nakayama, J. Bacteriol. 176, 1939 (1994).
19. K.-N. Lai and E. M. Gregory, GenBank direct submission, accession number M96560 (1992); E. R. Rocha, T. Selby, J. P. Coleman, C. J. Smith, J. Bacteriol. 178, 6895 (1996); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034841 (1997); M. Kitamura, S. Kojima, H. Akjtsu, I. Kumagai, T. Nakaya, GenBank direct submission, accession number AB020341 (1998); K. Nakayama, J. Bacteriol. 176, 1939 (1994).
20. K.-N. Lai and E. M. Gregory, GenBank direct submission, accession number M96560 (1992); E. R. Rocha, T. Selby, J. P. Coleman, C. J. Smith, J. Bacteriol. 178, 6895 (1996); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034841 (1997); M. Kitamura, S. Kojima, H. Akjtsu, I. Kumagai, T. Nakaya, GenBank direct submission, accession number AB020341 (1998); K. Nakayama, J. Bacteriol. 176, 1939 (1994).
21. C. J. Bult et al., Science 273, 1058 (1996).
22. H. P. Klenk et al., Nature 390, 364 (1997).
23. Y. Kawarabayasi et al., DNA Res. 5, 55 (1998).
24. D. Prieur et al., Genoscope (available at www. genoscope.cns.fr/) (1999).
25. K. E. Nelson et al., Nature 399, 323 (1999).
26. Preliminary sequence data were obtained from The Genome Therapeutics Corporation Web site at www. genomecorp.com. Sequencing of Clostridium acetobutylicum was accomplished with support from the U.S. Department of Energy.
27. The standard SOD assay involves steady-state generation of superoxide by means of bovine xanthine oxidase plus xanthine modified from the following: L. Flohé, R. Becker, R. Brigelius, E. Lengfelder, F. Ötting, in CRC Handbook of Free Radicals and Antioxidants in Biomedicine, J. Miguel, Ed. (CRC Press, Boca Raton, FL, 1988), vol. 3, p. 287. Reaction conditions were 50 mM potassium phosphate (pH 7.8), 0.2 mM xanthine, and 20 μM horse heart cytochrome c at 25°C. Superoxide directly reduces cytochrome c as measured by the increase in absorption (at 550 nm) due to the reduced cytochrome. SOD (bovine, Sigma) inhibits superoxide-dependent reduction of cytochrome c; one unit of activity is the amount of protein necessary to inhibit the rate by 50%.
28. G. Fiala and K. O. Stetter, Arch. Microbiol. 145, 56 (1986).
29. F. E. Jenney Jr. and M. W. W. Adams, in preparation. The Genbank accession number for SOR from P. furiosus is AF156097. Iron concentration was determined with a Thermo Jarrell-Ash 965 inductively coupled argon plasma spectrometer (ICAP) at the Chemical Analysis Laboratory of the University of Georgia.
30. P. R. Blake et al., Biochemistry 30, 10885 (1991).
31. A. V. Coelho et al., J. Biol. Inorg. Chem. 2, 680 (1997).
32. L. Chen et al., Eur. J. Biochem. 226, 613 (1994); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034965 (1997).
33. L. Chen et al., Eur. J. Biochem. 226, 613 (1994); N. V. Shenvi and D. M. Kurtz Jr., GenBank direct submission, accession number AF034965 (1997).
34. G. Silva et al., Eur. J. Biochem. 259, 235 (1999); C. V. Romão et al., ibid. 261, 438 (1999).
35. G. Silva et al., Eur. J. Biochem. 259, 235 (1999); C. V. Romão et al., ibid. 261, 438 (1999).
36. Inhibition of pyrogallol auto-oxidation, epinephrine auto-oxidation, and nitroblue tetrazolium reduction were measured as described in the following references, respectively: S. L. Marklund, in CRC Handbook of Methods for Oxygen Radical Research, R. A. Greenwald, Ed (CRC Press, Boca Raton, FL, 1985), p. 243;
37. D. G. Searcy, J. P. Whitehead, M. J. Maroney, Arch. Biochem. Biophys. 318, 251 (1995);
38. C. Beauchamp and I. Fridovich, Anal. Biochem. 44, 276 (1971).
39. A. Azzi, C. Montecucco, C. Richter, Biochem. Biophys. Res. Comm. 65, 597 (1975).
40. C. M. Fraser et al., Science 281, 375 (1998).
41. The only exception is the methanogen Methanobacterium thermoautotrophicum, but it possesses a desulfoferrodoxin homolog (as well as a classical SOD gene) [D. R. Smith et al., J. Bacteriol. 179, 7135 (1997 )]. Anaerobic eukaryotes also appear to have mechanisms to detoxify oxygen in the absence of detectable SOD and catalase [F. D. Marvin-Sikkema, T. M. Pedro Gomes, J.-P. Grivet, J. C. Gottschal, R. A. Prins, Arch. Microbiol. 160, 388 (1993)].
42. The only exception is the methanogen Methanobacterium thermoautotrophicum, but it possesses a desulfoferrodoxin homolog (as well as a classical SOD gene) [D. R. Smith et al., J. Bacteriol. 179, 7135 (1997 )]. Anaerobic eukaryotes also appear to have mechanisms to detoxify oxygen in the absence of detectable SOD and catalase [F. D. Marvin-Sikkema, T. M. Pedro Gomes, J.-P. Grivet, J. C. Gottschal, R. A. Prins, Arch. Microbiol. 160, 388 (1993)].
43. An amino acid sequence alignment of the nine available SORs is available as supplementary material at www.sciencemag.org/feature/data/1042812.shl.
44. T. Kaneko et al., DNA Res. 3, 109 (1996).
45. F. R. Blattner et al., Science 277, 1453 (1997).
46. S. I. Liochev and I. Fridovich, J. Biol. Chem. 272, 25573 (1997); M. J. Pianzzola, M. Soubes, D. Touati, J. Bacteriol. 178, 6736 (1996).
47. S. I. Liochev and I. Fridovich, J. Biol. Chem. 272, 25573 (1997); M. J. Pianzzola, M. Soubes, D. Touati, J. Bacteriol. 178, 6736 (1996).
48. G. R. Moore and G. W. Pettigrew, Cytochromes c: evolutionary, Structural and Physicochemical Aspects (Springer-Verlag, Berlin, 1990), p. 328.
49. R. Bau et al., J. Bioinorg. Chem. 3, 484 (1998).
50. M. W. W. Adams, Adv. Inorg. Chem. 38, 341 (1992).
51. L. Chen et al., FEBS Lett. 216, 443 (1993).
52. K. Ma and M. W. W. Adams, J. Bacteriol., 181, 5530 (1999).
53. Catalase activity was assayed as in H. Aebi, Methods Enzymol. 105, 121 (1984).
54. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
55. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
56. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
57. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
58. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
59. The anaerobe genomes (12-16, 27, 28) contain several genes whose products could be involved in peroxide detoxification. All have open reading frames (ORFs) that are highly similar to mammalian 1-cys peroxiredoxin {the P. furiosus ORF [R. Weiss et al., available at http:// combdna.umbi.umd.edu/bags.html (1999)] has 32% identity with the gene in Mus musculus [T. H. Lee et al., GenBank direct submission, accession number AAD03716 (1998); S. W. Kang, I. C. Baines, S. G. Rhee, J. Biol. Chem. 273, 6303 (1998)]}. Many also contain genes encoding one or more putative NAD(P)H-dependent peroxidases. Pyrococcus furiosus contains an ORF that is 48% similar to NADH peroxidase from a mesophilic facultative aerobe [R. P. Ross and A. Claiborne, J. Mol. Biol. 277, 658 (1992); T. C. Mallett and A. Claiborne, Biochemistry 37, 8790 (1998); T. Stehle, S. A. Ahmed, A. Claiborne, G. E. Schulz, J. Mol. Biol. 221, 1325 (1991)].
60. L. B. Poole and H. R. Ellis, Biochemistry 35, 56 (1996); L. A. Tartaglia, G. Storz, M. H. Brodsky, A. Lai, B. N. Arnes, J. Biol. Chem. 265, 10535 (1990).
61. L. B. Poole and H. R. Ellis, Biochemistry 35, 56 (1996); L. A. Tartaglia, G. Storz, M. H. Brodsky, A. Lai, B. N. Arnes, J. Biol. Chem. 265, 10535 (1990).
62. D. M. Kurtz Jr., J. Biol. Inorg. Chem. 2, 159 (1997).
63. Y. Lehmann, L. Meile, M. Teuber, J. Bacteriol. 178, 7152 (1996); F. Bonomi, D. M. Kurtz Jr., X. Cui, J. Biol. Inorg. Chem. 1, 67 (1996); P. S. Alban, D. L. Popham, K. E. Rippere, N. R. Krieg, J. Appl. Mircobiol. 85, 875 (1998).
64. Y. Lehmann, L. Meile, M. Teuber, J. Bacteriol. 178, 7152 (1996); F. Bonomi, D. M. Kurtz Jr., X. Cui, J. Biol. Inorg. Chem. 1, 67 (1996); P. S. Alban, D. L. Popham, K. E. Rippere, N. R. Krieg, J. Appl. Mircobiol. 85, 875 (1998).
65. Y. Lehmann, L. Meile, M. Teuber, J. Bacteriol. 178, 7152 (1996); F. Bonomi, D. M. Kurtz Jr., X. Cui, J. Biol. Inorg. Chem. 1, 67 (1996); P. S. Alban, D. L. Popham, K. E. Rippere, N. R. Krieg, J. Appl. Mircobiol. 85, 875 (1998).
66. M. W. W. Adams and A. Kletzin, Adv. Prot. Chem. 48, 101 (1996).
67. Y. Fouquet et al., Econ. Geol. 88, 2018 (1993); M. K. Tivey, in Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions, S. E. Humphris, R. A. Zierenberg, L. S. Mullineaux, R. E. Thomson, Eds. (American Geophysical Union, Washington, DC, 1995), pp. 158-177.
68. Y. Fouquet et al., Econ. Geol. 88, 2018 (1993); M. K. Tivey, in Seafloor Hydrothermal Systems: Physical, Chemical, Biological, and Geological Interactions, S. E. Humphris, R. A. Zierenberg, L. S. Mullineaux, R. E. Thomson, Eds. (American Geophysical Union, Washington, DC, 1995), pp. 158-177.
69. R. Huber, P. Stoffers, J. L. Cheminee, H. H. Richnow, K. O. Stetter, Nature 345, 179 (1990); M. Summit and J. A. Baross, Deep-Sea Res. Part II 45, 2751 (1998).
70. R. Huber, P. Stoffers, J. L. Cheminee, H. H. Richnow, K. O. Stetter, Nature 345, 179 (1990); M. Summit and J. A. Baross, Deep-Sea Res. Part II 45, 2751 (1998).
71. Supported by grants from the American Cancer Society (PF-4254), the Oliver S. and Jennie R. Donaldson Charitable Trust, the Department of Energy (FG05-95ER20175), and NSF (MCB 9809060).