Abstract
In order to colonize mammalian wounds, the anaerobic bacterium Clostridium tetani must presumably cope with temporary oxic conditions. Therefore, the recently decoded genome sequence was searched for genes which could confer oxygen tolerance. A few identified systems such as superoxide dismutases and peroxidases are probably responsible for this protection against toxic oxygen species. Another system was detected, a heme oxygenase which could have a role in establishing or maintaining an anoxic microenvironment in the process of wound colonization. The hemT gene encoding the heme oxygenase is expressed in C. tetani, as shown by reverse transcription–PCR. When overexpressed in Escherichia coli, the enzyme converts heme to biliverdin under strict oxic conditions.
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References
Arnon SS (1997) Human tetanus and human botulism. In: Rood JI, McClane BA, Songer JG, Titball RW (eds) The clostridia: molecular biology and pathogenesis. Academic, San Diego, pp 95–115
Bowler PG (2002) Wound pathophysiology, infection and therapeutic options. Ann Med 34:419–427
Briolat V, Reysset G (2002) Identification of the Clostridium perfringens genes involved in the adaptive response to oxidative stress. J Bacteriol 184:2333–2343
Brüggemann H, Gottschalk G (2004) Insights in metabolism and toxin production from the complete genome sequence of Clostridium tetani. Anaerobe 10:53–68
Brüggemann H, Bäumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, Herzberg C, Martinez-Arias R, Merkl R, Henne A, Gottschalk G (2003) The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc Natl Acad Sci USA 100:1316–1321
Gottschalk G, Andreesen JR, Hippe H (1981) The genus Clostridium. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer, Berlin Heidelberg New York, pp 1767–1803
Jean D, Briolat V, Reysset G (2004) Oxidative stress response in Clostridium perfringens. Microbiology 150:1649–1659
Lad L, Friedman J, Li H, Bhaskar B, De Montellano PRO, Poulos TL (2004) Crystal structure of human heme oxygenase-1 in a complex with biliverdin. Biochemistry 43:3793–3801
Lumppio HL, Shenvi NV, Summers AO, Voordouw G, Kurtz DM (2001) Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J Bacteriol 183:101–108
Migita CT, Zhang X, Yoshida T (2003) Expression and characterization of cyanobacterium heme oxygenase, a key enzyme in the phycobilin synthesis. Properties of the heme complex of recombinant active enzyme. Eur J Biochem 270:687–698
Nölling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, Gibson R, Lee HM, Dubois JA, Qiu D, Hitti J, GTC Sequencing Center Production, Finishing, and Bioinformatics Teams, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR (2001) Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183:4823–4838
O’Brien DK, Melville SB (2000) The anaerobic pathogen Clostridium perfringens can escape the phagosome of macrophages under aerobic conditions. Cell Microbiol 2:505–519
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
Schiavo G, Benfenati F, Poulain B, Rossetto O, Laureto PP de, DasGupta BR, Montecucco C (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832–835
Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H (2002) Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA 99:996–1001
Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043–1046
Wilks A (2002) Heme oxygenase: evolution, structure, and mechanism. Antioxid Redox Signal 4:603–6144
Wilks A, Schmitt MP (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J Biol Chem 273:837–841
Yamashita K, McDaid J, Ollinger R, Tsui TY, Berberat PO, Usheva A, Csizmadia E, Smith RN, Soares MP, Bach FH (2004) Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts. FASEB J 18:765–767
Zhu W, Wilks A, Stojiljkovic I (2000) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J Bacteriol 182:6783–6790
Acknowledgements
We thank M. Popoff (Institut Pasteur, Paris) for helpful discussions and the provision of C. tetani strain CN655 and thank O. Valerius (Departments of Molecular Microbiology and Genetics, University of Göttingen) for mass spectrometric analyses. The work was supported by a grant from the Niedersächsisches Ministerium für Wissenschaft und Kultur to the Göttingen Genomics Laboratory and by funds from the Competence Network Göttingen “Genome Research of Bacteria”, financed by the German Federal Ministry of Education and Research (BMBF).
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Dedicated to Prof. Dr. Hans-Günter Schlegel, the pioneer of microbiology in Göttingen and beyond, on the occasion of his 80th birthday.
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Brüggemann, H., Bauer, R., Raffestin, S. et al. Characterization of a heme oxygenase of Clostridium tetani and its possible role in oxygen tolerance. Arch Microbiol 182, 259–263 (2004). https://doi.org/10.1007/s00203-004-0721-1
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DOI: https://doi.org/10.1007/s00203-004-0721-1