Long-term Operation of Continuous Culture of the Hyperthermophilic archaeon, Thermococcus onnurineus for Carbon Monoxide-dependent Hydrogen Production

Abstract

In this study, we performed a kinetic analysis of CO-dependent H2 production by metabolically engineered Thermococcus onnurineus NA1, MC01 in terms of the cell activity as well as mass transfer rate. We conducted continuous cultures with varying dilution rate, CO flow rate, or agitation speed. Despite oscillations in cell density, the cultures reached steady states at all operating conditions. As the dilution rate increased from 0.1 to 0.3 h−1, specific activity of H2 production (SAHP) and volumetric cell production rate were linearly increased. Also, the SAHP remained almost constant at the fixed dilution rate of 0.3 h−1 even though the CO transfer rate was changed by adjusting the CO flow rate or the agitation speed. This relationship could be expressed as a typical Luedeking-Piret model, implying that high cell density culture with a sufficient growth rate is essential to obtain higher H2 productivity. On the other hand, more elevated CO transfer at the same dilution rate improved H2 production rate (HPR) by the increase of the cell density, not in the rise of SAHP. Through the continuous culture, 108 mmol/g-cell/h and 121 mmol/L/h of SAHP and HPR, respectively, could be achieved at a dilution rate of 0.3 h−1 with CO supply rate of 0.07 vvm and agitation speed of 700 rpm. Considering high H2 production activity and long-term stability of the strain over 1,000 h, MC01 is confirmed to have an outstanding potential for CO-dependent H2 production.

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References

  1. 1.

    Hay, I. X. W., T. Y. Wu, Y. C. Juan, and Y. Md. Jahim (2013) Biohydrogen production through photo fermentation or dark fermentation using waste as a substrate: Overview, economics, and future prospects of hydrogen usage. Biofuel. Bioprod. Biorefin. 7: 334–352.

    CAS  Article  Google Scholar 

  2. 2.

    Rittmann, S. K. M. R., H. S. Lee, I K. Lim, T. W. Kim, I. H. Lee, and S. G. Kang (2014) One-carbon substrate-based biohydrogen production: Microbes, mechanism, and productivity. Biotechnol. Adv. 33: 165–177.

    Article  Google Scholar 

  3. 3.

    Nguyen, T. A. D., J. P. Kim, M. S. Kim, Y. K. Oh, and S. J. Sim (2008) Optimization of hydrogen production by hyperthermophilic eubacteria, Thermotoga maritima and Thermotoga neapolitana in batch fermentation. Int. J. Hydrogen Energy. 33: 1483–1488.

    CAS  Article  Google Scholar 

  4. 4.

    Show, K. Y., D. J. Lee, J. H. Tay, C. Y. Lin, and J. S. Chang (2012) Biohydrogen production: Current perspectives and the way forward. Int. J. Hydrogen Energy. 37: 15615–15631.

    Article  Google Scholar 

  5. 5.

    Oh, Y. K., Y. J. Kim, J. Y. Park, T. H. Lee, M. S. Kim, and S. Park (2005) Biohydrogen production from carbon monoxide and water by Rhodopseudomonas palustris P4. Biotechnol. Bioprocess Eng 10: 270–274.

    CAS  Article  Google Scholar 

  6. 6.

    Oelegeschläger, E. and M. Rother (2008) Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea. Arch. Microbiol. 190: 257–269.

    Article  Google Scholar 

  7. 7.

    Henstra, A. M., J. Sipma, A. Rinzema, and A. J. M. Stams (2007) Microbiology of synthesis gas fermentation for biofuel production. Curr Opin. Biotechnol. 18: 200–206.

    CAS  Article  Google Scholar 

  8. 8.

    Köpke, M., C. Held, S. Hujer, H. Liesegang, A. Wiezer, A. Wolllierr, A. Ehrenreich, W. Liebl, G. Gottschalk, and P. Dürre (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc. Natl. Acad. Sci. USA. 107: 13087–13092.

    Article  Google Scholar 

  9. 9.

    Kim, M. S., S. S. Bae, Y. J. Kim, T. W. Kim, J. K. Lim, S. H. Lee, A. R. Choi, J. H. Jeon, J. H. Lee, H. S. Lee, and S. G. Kang (2013) CO-dependent H2 production by genetically engineered Thermococcus onnurineus NA1. Appl. Environ. Microbiol. 79: 2048–2053.

    CAS  Article  Google Scholar 

  10. 10.

    Im, H. S., C. Kim, Y. E. Song, J. Baek, C. H. Im, and J. R. Kim (2019) Isolation of novel CO converting microorganism using zero valent iron for a bioelectrochemical system (BES). Biotechnol. Bioprocess Eng. 24: 232–239.

    CAS  Article  Google Scholar 

  11. 11.

    Uffen, R. L. (1976) Anaerobic growth of a Rhodopseudomonas species in the dark with carbon monoxide as sole carbon and energy substrate. Proc. Natl. Acad. Sci. USA. 73: 3298–3302.

    CAS  Article  Google Scholar 

  12. 12.

    Jung, G. Y., J. R. Kim, J. Y. Park, and S. Park (2002) Hydrogen production by a new chemoheterotrophic bacterium Citrobacter sp. Y19. Int. J. Hydrogen Energy. 27: 601–610.

    CAS  Article  Google Scholar 

  13. 13.

    Sokolova, T. G., C. Jeanthon, N. A. Kostrikina, N. A. Chernyh, A. V. Lebedinsky, E. Stackebrandt, and E. A. Bonch-Osmolovskaya (2004) The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles. 8: 317–323.

    CAS  Article  Google Scholar 

  14. 14.

    Lee, H. S., S. G. Kang, S. S. Bae, J. K. Lim, Y. Cho, Y. J. Kim, J. H. Jeon, S. S. Cha, K. K. Kwon, H. T. Kim, C. J. Park, H. W. Lee, S. I. Kim, J. Chun, R. R. Colwell, S. J. Kim, and J. H. Lee (2008) The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J. Bacteriol. 190: 7491–7499.

    CAS  Article  Google Scholar 

  15. 15.

    Köpke, M., C. Mihalcea, J. C. Bromley, and S. D. Simpson (2011) Fermentative production of ethanol from carbon monoxide. Curr. Opin. Biotechnol. 22: 320–325.

    Article  Google Scholar 

  16. 16.

    Holden, J. E., K. Takai, M. Summit, S. Bolton, J. Zyskowski, and J. A. Baross (2001) Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol. Ecol. 36: 51–60.

    CAS  Article  Google Scholar 

  17. 17.

    Balch, W. E. and R. S. Wolfe (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl. Environ. Microbiol. 32: 781–791.

    CAS  Article  Google Scholar 

  18. 18.

    Ku Ismail, K. S., G. Najafpour, H. Younesi, A. R. Mohamed, and A. H. Kamaruddin (2008) Biological hydrogen production from CO: Bioreactor performance. Biochem. Eng. J. 39: 468–477.

    Article  Google Scholar 

  19. 19.

    Garcia-Ochoa, F. and E. Gomez (2009) Bioreactor scale-up and oxygen transfer rate in microbial processes: An overview. Biotechnol. Adv. 27: 153–176.

    CAS  Article  Google Scholar 

  20. 20.

    Bae, S. S., T W. Kim, H. S. Lee, K. K. Kwon, Y. J. Kim, M. S. Kim, J. H. Lee, and S. G. Kang (2012) H2 production from CO, formate or starch using the hyperthermophilic archaeon, Thermococcus onnurineus.Biotechnol. Lett. 34: 75–79.

    CAS  Article  Google Scholar 

  21. 21.

    Xiu, Z. L., A. P. Zeng, and W. D. Deckwer (1998) Multiplicity and stability analysis of microorganisms in continuous culture: Effects of metabolic overflow and growth inhibition. Biotechnol. Bioeng 57: 251–261.

    CAS  Article  Google Scholar 

  22. 22.

    Kim, M. S., H. N. Fitriana, T. W. Kim, S. G. Kang, S. G. Jeon, S. H. Chung, G. W. Park, and J. G. Na (2017) Enhancement of the hydrogen productivity in microbial water gas shift reaction by Thermococcus onnurineus NA1 using a pressurized bioreactor. Int. J. Hydrogen Energy. 42: 27593–27599.

    CAS  Article  Google Scholar 

  23. 23.

    Li, X., K. Scott, W. J. Kelly, and Z. Huang (2018) Development of a computational fluid dynamics model for scaling-up Ambr bioreactors. Biotechnol. Bioprocess Eng. 23: 710–725.

    CAS  Article  Google Scholar 

  24. 24.

    Younesi, H., G. Najafpour, K. S. Ku Ismail, A. R. Mohamed, and A. H. Kamaruddin (2008) Biohydrogen production in a continuous stirred tank bioreactor from synthesis gas by anaerobic photosynthetic bacterium: Rhodopirillum rubrum.Bioresour Technol. 99: 2612–2619.

    CAS  Article  Google Scholar 

  25. 25.

    Klasson, K. T., A. Gupta, E. C. Clausen, and J. L. Gaddy (1993) Evaluation of mass-transfer and kinetic parameters for Rhodospirillum rubrum in a continuous stirred tank reactor. Appl. Biochem. Biotechnol. 39: 549–557.

    Article  Google Scholar 

  26. 26.

    Zhao, Y., R. Cimpoia, Z. Liu, and S. R. Guiot (2011) Kinetics of CO conversion into H2 by Carboxydothermus hydrogenoformans.Appl. Microbiol. Biotechnol. 91: 1677–1684.

    CAS  Article  Google Scholar 

  27. 27.

    Haddad, M., R. Cimpoia, and S. R. Guiot (2014) Performance of Carboxydothermus hydrogenoformans in a gas-lift reactor for syngas upgrading into hydrogen. Int. J. Hydrogen Energy. 39: 2543–2548.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grant from the KIOST in house program (PE99722), the Sogang University Research Grant of 2017 (201710069.01), Chonnam National University (Grant number: 2019-0206), and the C1 Gas Refinery Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2015M3D3A1A01064884).

The authors declare no conflict of interest.

Neither ethical approval nor informed consent was required for this study.

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Correspondence to Jeong-Geol Na or Sung Gyun Kang.

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Kim, T.W., Bae, S.S., Lee, S. et al. Long-term Operation of Continuous Culture of the Hyperthermophilic archaeon, Thermococcus onnurineus for Carbon Monoxide-dependent Hydrogen Production. Biotechnol Bioproc E 25, 485–492 (2020). https://doi.org/10.1007/s12257-020-0005-x

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Keywords

  • carbon monoxide
  • biohydrogen production
  • continuous culture
  • hyperthermophilic archaeon
  • Thermococcus onnurineus