Abstract
Thermococcus onnurineus NA1, an obligate anaerobic hyperthermophilic archaeon, showed variable oxygen (O2) sensitivity depending on the types of substrate employed as an energy source. Unexpectedly, the culture with yeast extract as a sole energy source showed enhanced growth by 2-fold in the presence of O2. Genome-wide transcriptome analysis revealed the upregulation of several antioxidant-related genes encoding thioredoxin peroxidase (TON_0862), rubrerythrin (TON_0864), rubrerythrin-related protein (TON_0873), NAD(P)H rubredoxin oxidoreductase (TON_0865), or thioredoxin reductase (TON_1603), which can couple the detoxification of reactive oxygen species with the regeneration of NAD(P)+ from NAD(P)H. We present a plausible mechanism by which O2 serves to maintain the intracellular redox balance. This study demonstrates an unusual strategy of an obligate anaerobe underlying O2-mediated growth enhancement despite not having heme-based or cytochrome-type proteins.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams, M.W.W. 1998. The biochemical diversity of life near and above 100°C in marine environments. J. Appl. Microbiol. 85, 108S–117S.
Andreasen, A.A. and Stier, T.J. 1954. Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J. Cell. Comp. Physiol. 43, 271–281.
Bae, S.S., Kim, Y.J., Yang, S.H., Lim, J.K., Jeon, J.H., Lee, H.S., Kang, S.G., Kim, S.J., and Lee, J.H. 2006. Thermococcus onnurineus sp. nov., a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area at the PACMANUS field. J. Microbiol. Biotechnol. 16, 1826–1831.
Baughn, A.D. and Malamy, M.H. 2004. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427, 441–444.
Cabiscol, E., Tamarit, J., and Ros, J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3, 3–8.
Cao, B., Nagarajan, K., and Loh, K.C. 2009. Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl. Microbiol. Biotechnol. 85, 207–228.
Case, C.L., Rodriguez, J.R., and Mukhopadhyay, B. 2009. Characterization of an NADH oxidase of the flavin-dependent disulfide reductase family from Methanocaldococcus jannaschii. Microbiology 155, 69–79.
Hogg, S. 2005. Essential microbiology. John Wiley and Sons Ltd, Chichester, West Sussex, UK.
Imlay, J.A. 2002. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv. Microb. Physiol. 46, 111–153.
Imlay, J.A. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77, 755–776.
Jenney, F.E., Verhagen, M.F., Cui, X., and Adams, M.W. 1999. Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306–309.
Kawasaki, S., Ishikura, J., Chiba, D., Nishino, T., and Niimura, Y. 2004. Purification and characterization of an H2O-forming NADH oxidase from Clostridium aminovalericum: existence of an oxygen-detoxifying enzyme in an obligate anaerobic bacteria. Arch. Microbiol. 181, 324–330.
Kim, M.S., Bae, S.S., Kim, Y.J., Kim, T.W., Lim, J.K., Lee, S.H., Choi, A.R., Jeon, J.H., Lee, J.H., Lee, H.S., et al. 2013. CO-dependent H2 production by genetically engineered Thermococcus onnurineus NA1. Appl. Environ. Microbiol. 79, 2048–2053.
Kim, Y.J., Lee, H.S., Kim, E.S., Bae, S.S., Lim, J.K., Matsumi, R., Lebedinsky, A.V., Sokolova, T.G., Kozhevnikova, D.A., Cha, S.S., et al. 2010. Formate-driven growth coupled with H2 production. Nature 467, 352–355.
Lee, H.S., Kang, S.G., Bae, S.S., Lim, J.K., Cho, Y., Kim, Y.J., Jeon, J.H., Cha, S.S., Kwon, K.K., Kim, H.T., et al. 2008. The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J. Bacteriol. 190, 7491–7499.
Lumppio, H.L., Shenvi, N.V., Summers, A.O., Voordouw, G., and Kurtz, D.M. 2001. Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J. Bacteriol. 183, 101–108.
Madigan, M., Martinko, J., Stahl, D., and Clark, D. 2010. Microbial Growth, pp. 117–149. In Cummings, B. (ed.), Brock biology of microorganisms, 13th ed. Person education, San Francisco, USA.
Moon, Y.J., Kwon, J., Yun, S.H., Lim, H., Kim, J., Kim, S., Kang, S., Lee, J.H., Kim, S., and Chung, Y.H. 2015. Proteomic insights into sulfur metabolism in the hydrogen-producing hyperthermophilic archaeon Thermococcus onnurineus NA1. Int. J. Mol. Sci. 16, 9167–9195.
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628.
Rojo, F. 2009. Degradation of alkanes by bacteria. Environ. Microbiol. 11, 2477–2490.
Staerck, C., Gastebois, A., Vandeputte, P., Calenda, A., Larcher, G., Gillmann, L., Papon, N., Bouchara, J.P., and Fleury, M.J.J. 2017. Microbial antioxidant defense enzymes. Microb. Pathog. 110, 56–65.
Storz, G. and Imlay, J.A. 1999. Oxidative stress. Curr. Opin. Microbiol. 2, 188–194.
Strand, K.R., Sun, C., Li, T., Jenney, F.E., Schut, G.J., and Adams, M.W.W. 2010. Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species. Arch. Microbiol. 192, 447–459.
Thorgersen, M.P., Stirrett, K., Scott, R.A., and Adams, M.W.W. 2012. Mechanism of oxygen detoxification by the surprisingly oxygen-tolerant hyperthermophilic archaeon, Pyrococcus furiosus. Proc. Natl. Acad. Sci. USA 109, 18547–18552.
Ward, D.E., Donnelly, C.J., Mullendore, M.E., van der Oost, J., de Vos, W.M., and Crane, E.J. 2001. The NADH oxidase from Pyrococcus furiosus. Implications for the protection of anaerobic hyperthermophiles against oxidative stress. Eur. J. Biochem. 268, 5816–5823.
Wolf, Y.I., Makarova, K.S., Yutin, N., and Koonin, E.V. 2012. Updated clusters of orthologous genes for archaea: a complex ancestor of the archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46.
Woods, D.R. and Jones, D.T. 1986. Physiological responses of Bacteroides and Clostridium strains to environmental stress factors. Adv. Microb. Physiol. 28, 1–64.
Yang, X. and Ma, K. 2005. Purification and characterization of an NADH oxidase from extremely thermophilic anaerobic bacterium Thermotoga hypogea. Arch. Microbiol. 183, 331–337.
Yang, X. and Ma, K. 2007. Characterization of an exceedingly active NADH oxidase from the anaerobic hyperthermophilicbacterium Thermotoga maritima. J. Bacteriol. 189, 3312–3317.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Supplemental material for this article may be found at http://www.springerlink.com/content/120956.
Rights and permissions
About this article
Cite this article
Lee, S.H., Youn, H., Kang, S.G. et al. Oxygen-mediated growth enhancement of an obligate anaerobic archaeon Thermococcus onnurineus NA1. J Microbiol. 57, 138–142 (2019). https://doi.org/10.1007/s12275-019-8592-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-019-8592-y