Clostridium bifermentansc as an Aero-Tolerant Exponent of Strictly Anaerobe Genera


Strictly anaerobic bacteria in the evolutionary way formed some mechanisms of oxygen tolerance. These changes enable strictly anaerobic bacteria existing in natural environment in which avoiding oxygen is not possible. Clostridium bifermentans is described as a strictly anaerobe species; however, in the literature, there is some information about its oxygen tolerance. Thus, in this work, the level of C. bifermentans aero-tolerance, its mechanisms, and the ability to metabolite production in presence of oxygen in cultivation medium were investigated. It was found out that C. bifermentans is able to survive in the presence of oxygen. Moreover, they are able to utilize oxygen and product metabolites when the level of oxygen is below 10%. In bacteria cells superoxide dismutase was detected.

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Leja, K. , Myszka, K. , Olkowicz, M. , Juzwa, W. and Czaczyk, K. (2014) Clostridium bifermentansc as an Aero-Tolerant Exponent of Strictly Anaerobe Genera. Advances in Microbiology, 4, 216-224. doi: 10.4236/aim.2014.44028.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Brioukhanov, A.L. and Netrusov, A.I. (2007) Aerotolerance of Strictly Anaerobic Microorganisms and Factors of Defense against Oxidative Stress: A Review. Applied Biochemistry and Microbiology, 43, 637-654.
[2] Hewitt, J. and Morris, J.G. (1975) Superoxide Dismutase in Some Obligately Anaerobic Bacteria. FEBS Letters, 50, 315-318.
[3] Brioukhanov, A.L., Thauer, R.K. and Netrusov, A.I. (2002) Catalase and Superoxide Dismutase in the Cells of Strictly Anaerobic Microorganisms. Journal of Medical Microbiology, 71, 330-335.
[4] Karnholz, A., Kusel, K., Gossner, A., Schramm, A. and Drake, H.L. (2002) Tolerance and Metabolic Response of Acetogenic Bacteria toward Oxygen (O2). Applied and Environmental Microbiology, 2, 1005-1009.
[5] Rocha, E.R., Selby, T., Coleman, J.P. and Smith, C.J. (1995) Oxidative Stress Response in an Anaerobe, Bacteroides fragilis: A Role for Catalase in Protection against Hydrogen Peroxide. Journal of Bacteriology, 178, 6895-6903.
[6] Cypionka, H. (2000) Oxygen Respiration by Desulfovibrio species. Annual Review of Microbiology, 54, 827-848.
[7] Hillmann, F., Riebe, O., Fischer, R.J., Mot, A., Caranto, J.D., Kurtz, D.M. and Bahl, H. (2009) Reductive Dioxygen Scavenging by Flavo-Diiron Proteins of Clostridium Acetobutylicum. FEBS Letters, 583, 241-245.
[8] Jedrzejczak-Krzepkowska, M. and Bielecki, S. (2011) Bifidobacteria and Fructane Stimulating Their Growth. Postepy Biochemii, 57, 1-9 (in Polish).
[9] Lombard, M., Fontecave, M., Touati, D. and Nivière, V. (2002) Reaction of the Desulfoferrodoxin from Desulfoarculus baarsii with Superoxide Anion Evidence for a Superoxide Reductase Activity. Journal of Biological Chemistry, 275, 115-121.
[10] Rolfe, R.D., Hentges, D.J., Campbell, B.J. and Barrett, J.T. (1978) Factors Related to the Oxygen Tolerance of Anaerobic Bacteria. Applied and Environmental Microbiology, 36, 306-313.
[11] Kawasaki, S., Watamura, Y., Ono, M., Watanabe, T., Takeda, K. and Niimura, Y. (2005) Adaptive Responses to Oxygen Stress in Obligatory Anaerobes Clostridium acetobutylicum and Clostridium aminovalericum. Applied and Environmental Microbiology, 71, 8442-8450.
[12] Morris, J.G. (1976) Oxygen and the Obligatory Anaerobe. Journal of Applied Bacteriology, 40, 229-244.
[13] Nakayama, K. (1990) The Superoxide Dismutase-Encoding Gene of the Obligately Anaerobic Bacterium Bacteroides gingivalis. Gene, 96, 149-150.
[14] Meile, L., Fischer, K. and Leisinger, T. (2005) Characterization of the Superoxide Dismutase Gene and Its Upstream Region from Methanobacterium thermoautotrophicum Marburg. FEMS Microbioogyl Letters, 128, 247-253.
[15] Takao, M., Oikawa, A. and Yasui, A. (1990) Characterization of a Superoxide Dismutase Gene from the Archaebacterium Methanobacterium thermoautotrophicum. Archivum of Biochemistry and Biophysis, 283, 210-216.
[16] Shenvi, N.V. and Kurtz, D.M. (1977) Desulfovibrio vulgaris Superoxide Dismutase (sod) Gene. Complete eds, EMBL/GenBank Direct Submission. Accession number AF034841,
[17] Geissmann, T.A., Teuber, M. and Meile, L. (1999) Transcriptional Analysis of the Rubrerythrin and Superoxide Dismutase Genes of Clostridium perfringens. Journal of Bacteriology, 181, 7136-7139.
[18] Archer, R.H. Maddox, I.S. and Chong, R. (1982) Transformation of Cholic Acid by Clostridium bifermentans. Journal of Applied Microbiology, 52, 49-56.
[19] Chamkha, M., Patel, B.K.C., Garcia, J.L. and Labata, M. (2001) Isolation of Clostridium bifermentans from Oil Mill Wastewaters Converting Cinnamic Acid to 3-Phenylpropionic Acid and Emendation of the Species. Anaerobe, 7, 189-197.
[20] Verhulst, A., Semjen, G., Meerts, U., Janssen, G., Parmentier, G., Asselberghs, S. and van Hespen, H. (1985) Biohydrogenation of Linoleic Acid by Clostridium sporogenes, Clostridium bifermentans, Clostridium sordellii and Bacteroides sp. FEMS Microbiology Letters, 31, 255-259.
[21] Zhang, S., Kim, T.H., Lee, Y. and Hwang, S.J. (2012) Effects of VFAs Concentration on Bio-Hydrogen Production with Clostridium bifermentans 3AT-ma. Energy Procedia, 14, 518-523.
[22] Admassu, W., Sethuraman, A.V., Crawford, R. and Korus, R.A. (1998) Growth Kinetics of Clostridium bifermentans and Its Ability to Degrade TNT Using an Inexpensive Alternative Medium. Bioremediation Journal, 2, 17-28.
[23] Gibbs, P.A. (1964) Factors Affecting the Germination of Spores of Clostridium bifermentans. Microbiology, 37, 41-48.
[24] Kawasaki, S., Tomoyuki, N., Yoshitaka, N., Yoshimi, B., Tai, U., Kazuo, K., Michio, K. and Youichi, N. (1998) Effect of Oxygen on the Growth of Clostridium butyricum (Type Species of the Genus Clostridium), and the Distribution of Enzymes for Oxygen and for Active Oxygen Species in Clostridia. Journal of Fermentation and Bioengineering, 86, 368-372.
[25] Myszka, K., Leja, K., Olejnik-Schmidt, A.K. and Czaczyk, K. (2012) Isolation Process of Industrially Useful Clostridium bifermentans from Natural Samples. Journal of Bioscience and Bioengineering, 113, 631-633.
[26] Kaeberlein, T., Lewis, K. and Epstein, S.S. (2002) Isolating “Uncultivable” Microorganisms in Pure Culture in a Simulated Natural Environment. Science, 296, 1127-1129.
[27] Nicol, R.W., Marchand, K. and Lubitz, W.D. (2012) Bioconversion by Crude Glycerol by Fungi. Applied Microbiology and Biotechnology, 93, 1865-1875.
[28] Cremonesi, P., Vanoni, L., Silvetti, T., Morandi, S. and Brasca, M. (2012) Identification of Clostridium beijerinckii, C butyricum, C sporogenes, C tyrobutyricum Isolated from Silage, Raw Milk and Hard Cheese by a Multiplex PCR Assay. Journal of Dairy Research, 79, 318-323.
[29] Meier, T.R., Myers, D.D., Ko, E.K.A., Holden, M. and Claire, H.F. (2007) Gangrenous Clostridium perfringens Infection and Subsequent Wound Management in a Rhesus Macaque (Macaca mulatta). Journal of the American Association for Laboratory Animal Science, 46, 68-73.
[30] Beckers, L., Hiligsmann, S., Lambert, S.D., Heinrichs, B. and Thonart, P. (2013) Improving Effect of Metal and Oxide Nanoparticles Encapsulated in Porous Silica on Fermentative Biohydrogen Production by Clostridium butyricum. Bioresource Technology, 133, 109-117.
[31] Buckel, W. (2005) Special Clostridial Enzymes and Fermentation Pathways. In: Buckel, W., Ed., Handbook on Clostridia, CRC Press LLC, Boca Raton, 81-83.
[32] Yang, X., Tu, M., Xie, R., Adhikari, S. and Tong, Z. (2013) A Comparison of Three pH Control Methods for Revealing Effects of Undissociated Butyric Acid on Specific Butanol Production Rate in Batch Fermentation of Clostridium acetobutylicum. AMB Express, 3, 3-6.
[33] Collas, F., Kuit, W., Clément, B., Marchal, R., López-Contreras, A.M. and Monot, F. (2012) Simultaneous Production of Isopropanol, Butanol, Ethanol and 2,3-Butanediol by Clostridium acetobutylicum ATCC 824 Engineered Strains. AMB Express, 2, 45-47.
[34] Wilkens, E., Ringel, A.K., Hortig, D., Willke, T. and Vorlop, K.D. (2012) High-Level Production of 1,3-Propanediol from Crude Glycerol by Clostridium butyricum AKR102a. Applied Microbiology and Biotechnology, 93, 1057-1063.
[35] Huyen, N.T.T., Yen, D.T., Yen, N.T., Nga, V.T. and Hien, L.T. (2012) Using of Response Surface Methodology for Optimization of Biohydrogen Production by Clostridium spp. Isolated in Vietnam. Journal of Biology, 43, 1-12.
[36] Kubiak, P., Leja, K., Myszka, K., Celińska, E., Spychala, M., Powa4月me 754 755这两篇到时候doi分开owska-Szymanowska, D., Czaczyk, K. and Grajek, W. (2012) Physiological Predisposition of Various Clostridium Species to Synthetize 1,3-Propanediol from Glycerol. Process Biochemistry, 47, 1308-1319.
[37] Leja, K., Myszka, K., Kubiak, P., Wojciechowska, J., Olejnik-Schmidt, A.K., Czaczyk, K. and Grajek, W. (2011) Isolation and Identification of Clostridium spp from Natural Samples that Performs Effective Conversion of Glycerol to 1,3-Propanediol. Acta Scientarum Polonorum-Biotechnologia, 10, 25-34.
[38] Braeckman, B.P., Houthoofd, K., Vreese, A.D. and Vanfleteren, J.R. (2002) Assaying Metabolic Activity in Ageing Caenorhabditis elegans. Mechanisms of Ageing and Development, Genetic Effects on Aging III, 123, 105-119.
[39] Springer, J.E., Azbill, R.D. and Carlson, S.L. (1998) A Rapid and Sensitive Assay for Measuring Mitochondrial Metabolic Activity in Isolated Neural Tissue. Brain Research Protocols, 2, 259-263.
[40] Pflügl, S., Marx, H., Mattanovich, D. and Sauer, M. (2012) 1,3-Propanediol Production from Glycerol with Lactobacillus diolivorans. Bioresource Technology, 119, 133-140.
[41] Marçal1, D., Rêgo, A.T., Carrondo, M.A. and Enguita, F.J. (2008) 1,3-Propanediol Dehydrogenase from Klebsiella pneumoniae: Decameric Quaternary Structure and Possible Subunit Cooperativity. Journal of Bacteriology, 191, 1143-1151.
[42] Setlow, P. and Waites, W.M. (1976) Identification of Several Unique, Low-Molecular-Weight Basic Proteins in Dormant Spores of Clostridium bifermentans and Their Degradation during Spore Germination. Journal of Bacteriology, 127, 1015-1017.

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