Skip to main content

Advertisement

SpringerLink
Log in

Intensification of Hydrogen Production by a Co-culture of Syntrophomonas wolfei and Rhodopseudomonas palustris Employing High Concentrations of Butyrate as a Substrate

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The purpose of this study is to present an effective form of developing a sequential dark (DF) and photo (PF) fermentation using volatile fatty acids (VFAs) and nitrogen compounds as bonding components between both metabolic networks of microbial growing in each fermentation. A simultaneous (co-)culture of Syntrophomonas wolfei (with its ability to consume butyrate and produce acetate) and Rhodopseudomonas palustris (that can use the produced acetate as a carbon source) performed a syntrophic metabolism. The former bacteria consumed the acetate/butyrate mixture reducing the butyrate concentration below 2.0 g/L, permitting Rhodopseudomonas palustris to produce hydrogen. Considering that the inoculum composition (Syntrophomonas wolfei/Rhodopseudomonas palustris) and the nitrogen source (yeast extract) define the microbial biomass specific productivity and the butyrate consumption, a response surface methodology defined the best inoculum design and yeast extract (YE) yielding to the highest biomass concentration of 1.1 g/L after 380.00 h. A second culture process (without a nitrogen source) showed the biomass produced in the previous culture process yields to produce a total cumulated hydrogen concentration of 3.4 mmol. This value was not obtained previously with the pure strain Rhodopseudomonas palustris if the culture medium contained butyrate concentration above 2.0 g/L, representing a contribution to the sequential fermentation scheme based on DF and PF.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

Not applicable

Code Availability

Not applicable

References

  1. Afsar, N., Özgür, E., Gürgan, M., De Vrije, T., Yücel, M. U. S. T. A. F. A., Gündüz, U. F. U. K., & Eroglu, I. (2009). Hydrogen production by R. capsulatus on dark fermenter effluent of potato steam peel hydrolysate. Chem Eng Trans, 18, 385–90.

  2. Arhoun, B., Villen-Guzman, M., Gomez-Lahoz, C., Rodriguez-Maroto, J. M., Garcia-Herruzo, F., & Vereda-Alonso, C. (2019). Anaerobic co-digestion of mixed sewage sludge and fruits and vegetable wholesale market waste: Composition and seasonality effect. Journal of Water Process Engineering, 31, 100848.

  3. Barbosa, M. J., Rocha, J. M. S., Tramper, J., & Wijffels, R. H. (2001). Acetate as a carbon source for hydrogen production by photosynthetic bacteria. Journal of Biotechnology, 85(1), 25–33.

    Article  CAS  PubMed  Google Scholar 

  4. Beaty, P. S., & Mcinerney, M. J. (1990). Nutritional Features of Syntrophomonas-wolfei. Applied and Environmental Microbiology, 56(10), 3223–3224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Beaty, P. S., & McInerney, M. J. (1987). Growth of Syntrophomonas wolfei in pure culture on crotonate. Archives of Microbiology, 147(4), 389–393.

    Article  CAS  Google Scholar 

  6. Beaty, P. S., Wofford, N. Q., & McInerney, M. J. (1987). Separation of Syntrophomonas wolfei from Methanospirillum hungatii in syntrophic cocultures by using Percoll gradients. Applied and Environmental Microbiology, 53(5), 1183–1185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.

    Article  CAS  PubMed  Google Scholar 

  8. Cárdenas, D. P., Pulido, C., Aragón, Ó. L., & Aristizá, F. A. (2006). Evaluación de la producción de 1,3-propanodiol por cepas nativas de Clostridium sp mediante fermentación a partir de glicerol USP y glicerol industrial subproducto de la producción de biodiésel. Rev Col Cienc Quím Farm, 35(1), 120–137.

    Google Scholar 

  9. Chang, J. S., Show, P. L., Ling, T. C., Chen, C. Y., Ho, S. H., Tan, C. H., & Phong, W. N. (2017). Photobioreactors. In Current developments in biotechnology and bioengineering (pp. 313–352). Elsevier.

  10. Chaudhary, C., Saeedi, H., & Costello, M. J. (2017). Marine Species Richness Is Bimodal with Latitude: A Reply to Fernandez and Marques. Trends in Ecology and Evolution, 32(4), 234–237.

    Article  PubMed  Google Scholar 

  11. Chen, C. Y., Lee, C. M., & Chang, J. S. (2006). Feasibility study on bioreactor strategies for enhanced photohydrogen production from Rhodopseudomonas palustris WP3-5 using optical-fiber-assisted illumination systems. International Journal of Hydrogen Energy, 31(15), 2345–2355.

    Article  CAS  Google Scholar 

  12. Chen, C. Y., Lu, W., Bin, Liu, C. H., & Chang, J. S. (2008). Improved phototrophic H2production with Rhodopseudomonas palustris WP3-5 using acetate and butyrate as dual carbon substrates. Bioresource Technology, 99(9), 3609–3616.

    Article  CAS  PubMed  Google Scholar 

  13. Cortés, O., Guerra-Blanco, P., Chairez, I., Poznyak, T., & García-Peña, E. I. (2022). Polymers, the Light at the End of Dark Fermentation: Production of Poly (3-hydroxybutyrate-co-3-hydroxyvalerate) by a Photoheterotrophic Consortium. Journal of Polymers and the Environment, 30(6), 2392–2404.

    Article  Google Scholar 

  14. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., & Stackebrandt, E. (Eds.). (2006). The Prokaryotes. New York, NY: Springer US.

    Google Scholar 

  15. Elbeshbishy, E., Dhar, B. R., Nakhla, G., & Lee, H. S. (2017). A critical review on inhibition of dark biohydrogen fermentation. Renewable and Sustainable Energy Reviews, 79, 656–668.

  16. Eroglu, E., & Melis, A. (2011). Photobiological hydrogen production: Recent advances and state of the art. Bioresource Technology, 102(18), 8403–8413.

    Article  CAS  PubMed  Google Scholar 

  17. Esquivel-Elizondo, S., Chairez, I., Salgado, E., Aranda, J. S., Baquerizo, G., & Garcia-Peña, E. I. (2014). Controlled Continuous Bio-Hydrogen Production Using Different Biogas Release Strategies. Applied Biochemistry and Biotechnology, 173(7), 1737–1751.

    Article  CAS  PubMed  Google Scholar 

  18. Fernández Garrido, A. J. (2014). El proceso de Steam Reforming. Retrieved November 1, 2017, from http://www.ingenieriaquimica.net. Accessed  26 Mar 2020.

  19. Garcia-Peña, E. I., Niño-Navarro, C., Chairez, I., Torres-Bustillos, L., Ramírez-Muñoz, J., & Salgado-Manjarrez, E. (2018). Performance intensification of a stirred bioreactor for fermentative biohydrogen production. Preparative Biochemistry and Biotechnology, 48(1), 64–74.

    Article  PubMed  Google Scholar 

  20. Guerra-Blanco, P., Cortes, O., Poznyak, T., Chairez, I., & García-Peña, E. I. (2018). Polyhydroxyalkanoates (PHA) production by photoheterotrophic microbial consortia: effect of culture conditions over microbial population and biopolymer yield and composition. European Polymer Journal, 98, 94–104.

    Article  CAS  Google Scholar 

  21. Gonzalez-Garcia, R. A., Aispuro-Castro, R., Salgado-Manjarrez, E., Aranda-Barradas, J., & Garcia-Pena, E. I. (2017). Metabolic pathway and flux analysis of H2 production by an anaerobic mixed culture. International Journal of Hydrogen Energy, 42(7), 4069–4082.

    Article  CAS  Google Scholar 

  22. Gomez-Romero, J., Garcia-Peña, I., Ramirez-Muñoz, J., & Torres, L. G. (2014). Rheological characterization of a mixed fruit/vegetable puree feedstock for hydrogen production by dark fermentation. Advances in Chemical Engineering and Sciences, 4(January), 81–88.

    Article  Google Scholar 

  23. Gomez-Romero, J., Gonzalez-Garcia, A., Chairez, I., Torres, L., & García-Peña, E. I. (2014). Selective adaptation of an anaerobic microbial community: Biohydrogen production by co-digestion of cheese whey and vegetables fruit waste. International Journal of Hydrogen Energy, 39(24), 12541–12550.

    Article  CAS  Google Scholar 

  24. Gosse, J. L., Engel, B. J., Hui, J. C. H., Harwood, C. S., & Flickinger, M. C. (2010). Progress toward a biomimetic leaf: 4,000 h of hydrogen production by coating-stabilized nongrowing photosynthetic Rhodopseudomonas palustris. Biotechnology Progress, 26(4), 907–918.

    CAS  PubMed  Google Scholar 

  25. Hitit, Z. Y., Lazaro, C. Z., & Hallenbeck, P. C. (2017). Hydrogen production by co-cultures of Clostridium butyricum and Rhodospeudomonas palustris: Optimization of yield using response surface methodology. International Journal of Hydrogen Energy, 42(10), 6578–6589.

  26. Hitit, Z. Y., Lazaro, C., & Hallenbeck, P. C. (2017b). Increased hydrogen yield and COD removal from starch/glucose based medium by sequential dark and photo-fermentation using Clostridium butyricum and Rhodopseudomonas palustris. International Journal of Hydrogen Energy, 42(30), 18832–18843.

    Article  CAS  Google Scholar 

  27. Hwang, J. H., Kabra, A. N., Kim, J. R., & Jeon, B. H. (2014). Photoheterotrophic microalgal hydrogen production using acetate- and butyrate-rich wastewater effluent. Energy, 78, 887–894.

    Article  CAS  Google Scholar 

  28. Javed, M. A., Zafar, A. M., & Hassan, A. A. (2022). Regulate oxygen concentration using a co-culture of activated sludge bacteria and Chlorella vulgaris to maximize biophotolytic hydrogen production. Algal Research, 63, 102649.

    Article  Google Scholar 

  29. Kim, S., Agca, C., & Agca, Y. (2013). Effects of various physical stress factors on mitochondrial function and reactive oxygen species in rat spermatozoa. Reproduction Fertility and Development, 25(7), 1051–1064.

    Article  CAS  PubMed  Google Scholar 

  30. Lee, C. M., Chen, P. C., Wang, C. C., & Tung, Y. C. (2002). Photohydrogen production using purple nonsulfur bacteria with hydrogen fermentation reactor effluent. International Journal of Hydrogen Energy, 27(11–12), 1309–1313.

    Article  CAS  Google Scholar 

  31. Li, Z., Fang, A., Cui, H., Ding, J., Liu, B., Xie, G., … & Xing, D. (2021). Synthetic bacterial consortium enhances hydrogen production in microbial electrolysis cells and anaerobic fermentation. Chemical Engineering Journal, 417, 127986.

  32. Lo, Y. C., Chen, C. Y., Lee, C. M., & Chang, J. S. (2011). Photo fermentative hydrogen production using dominant components (acetate, lactate, and butyrate) in dark fermentation effluents. International Journal of Hydrogen Energy, 36(21), 14059–14068.

    Article  CAS  Google Scholar 

  33. Lu, C., Zhang, Z., Zhou, X., Hu, J., Ge, X., Xia, C., & Zhang, Q. (2018). Effect of substrate concentration on hydrogen production by photo-fermentation in the pilot-scale baffled bioreactor. Bioresource technology, 247, 1173–1176.

  34. Mabutyana, L., & Pott, R. W. (2021). Photo-fermentative hydrogen production by Rhodopseudomonas palustris CGA009 in the presence of inhibitory compounds. International Journal of Hydrogen Energy, 46(57), 29088–29099.

    Article  CAS  Google Scholar 

  35. McInerney, M. J., Bryant, M. P., Hespell, R. B., & Costerton, J. W. (1981a). Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid-oxidizing bacterium. Applied and Environmental Microbiology, 41(4), 1029–1039.

  36. Mckinlay, J. B., & Harwood, C. S. (2011). Calvin Cycle Flux, Pathway Constraints, and Substrate Oxidation State Bacteria. MBio, 2(7), 1–9.

  37. McKinlay, J. B., & Harwood, C. S. (2010). Photobiological production of hydrogen gas as a biofuel. Current Opinion in Biotechnology, 21(3), 244–251.

    Article  CAS  PubMed  Google Scholar 

  38. McKinlay, J. B., Oda, Y., Rühl, M., Posto, A. L., Sauer, U., & Harwood, C. S. (2014). Non-growing Rhodopseudomonas palustris Increases the Hydrogen Gas Yield from Acetate by Shifting from the Glyoxylate Shunt to the Tricarboxylic Acid Cycle. Journal of Biological Chemistry, 289(4), 1960–1970.

    Article  CAS  PubMed  Google Scholar 

  39. Melnicki, L., Bianchi, R., De Philippis, A., & Melis (2008). Hydrogen production during stationary phase in purple photosynthetic bacteria. International Journal of Hydrogen Energy, 33, 6525–6534.

    Article  CAS  Google Scholar 

  40. Nath, K., & Das, D. (2004). Improvement of fermentative hydrogen production: Various approaches. Applied Microbiology and Biotechnology, 65(5), 520–529.

    Article  CAS  PubMed  Google Scholar 

  41. Niño-Navarro, C., Chairez, I., Torres-Bustillos, L., Ramírez-Muñoz, J., Salgado-Manjarrez, E., & Garcia-Peña, E. I. (2016). Effects of fluid dynamics on enhanced biohydrogen production in a pilot stirred tank reactor: CFD simulation and experimental studies. International Journal of Hydrogen Energy, 41(33), 14630–14640.

    Article  Google Scholar 

  42. Ogata, T., & Yamanaka, K. (1982). Butyrate activation in Rhodopseudomonas palustris no. 82. Agricultural and Biological Chemistry, 46(10), 2593–2594.

    CAS  Google Scholar 

  43. Oh, Y. K., Seol, E. H., Kim, M. S., & Park, S. (2004). Photoproduction of hydrogen from acetate by a chemoheterotrophic bacterium Rhodopseudomonas palustris P4. International Journal of Hydrogen Energy, 29(11), 1115–1121.

    CAS  Google Scholar 

  44. Pandey, A., Sinha, P., & Pandey, A. (2021). Hydrogen production by sequential dark and photofermentation using wet biomass hydrolysate of Spirulina platensis: Response surface methodological approach. International Journal of Hydrogen Energy, 46(10), 7137–7146.

    Article  CAS  Google Scholar 

  45. Pans, M. A., Gayán, P., Luis, F., García-Labiano, F., Abad, A., & Adánez, J. (2015). Performance of a low-cost iron ore as an oxygen carrier for Chemical Looping Combustion of gaseous fuels. Chemical Engineering Research and Design, 93, 736–746.

  46. Pott, R. W., Howe, C. J., & Dennis, J. S. (2013). Photofermentation of crude glycerol from biodiesel using Rhodopseudomonas palustris: comparison with organic acids and the identification of inhibitory compounds. Bioresource technology, 130, 725–730.

    Article  CAS  PubMed  Google Scholar 

  47. Pott, R. W., Howe, C. J., & Dennis, J. S. (2014). The purification of crude glycerol derived from biodiesel manufacture and its use as a substrate by Rhodopseudomonas palustris to produce hydrogen. Bioresource technology, 152, 464–470.

    Article  CAS  PubMed  Google Scholar 

  48. Rai, P. K., & Singh, S. P. (2016). Integrated dark- and photo-fermentation: Recent advances and provisions for improvement. International Journal of Hydrogen Energy, 41(44), 19957–19971.

    Article  CAS  Google Scholar 

  49. Reykjavík. (2011). Hydrogen as Future Energy Carrier. Green Energy and Technology, 11, 33–70.

    Google Scholar 

  50. Rodionova, M. V., Poudyal, R. S., Tiwari, I., Voloshin, R. A., Zharmukhamedov, S. K., Nam, H. G., & Allakhverdiev, S. I. (2017). Biofuel production: Challenges and opportunities. International Journal of Hydrogen Energy, 42(12), 8450–8461.

    Article  CAS  Google Scholar 

  51. Sieber, J. R., Sims, D. R., Han, C., Kim, E., Lykidis, A., Lapidus, A. L., & McInerney, M. J. (2010). The genome of Syntrophomonas wolfei: New insights into syntrophic metabolism and biohydrogen production. Environmental Microbiology, 12(8), 2289–2301.

    CAS  PubMed  Google Scholar 

  52. Silva, G. F., Fereira, A. L., Cartaxo, S. J., & Fernandes, F. A. (2009). Simulation and optimization of H2 production by autothermal reforming of glycerol. In Computer aided chemical engineering, 27, 987–992. Elsevier.

  53. Tao, Y., Chen, Y., Wu, Y., He, Y., & Zhou, Z. (2007). High hydrogen yield from a two-step process of dark- and photo-fermentation of sucrose. International Journal of Hydrogen Energy, 32(2), 200–206.

    Article  CAS  Google Scholar 

  54. Skempton, A. W., & Chrimes, M. (Eds.). (2002). A Biographical Dictionary of Civil Engineers in Great Britain and Ireland: 1500–1830 (Vol. 1). Thomas Telford.

  55. Torres, M. J., González-Ballester, D., Gómez-Osuna, A., Galván, A., Fernández, E., & Dubini, A. (2022). Chlamydomonas-Methylobacterium oryzae cooperation leads to increased biomass, nitrogen removal and hydrogen production. Bioresource Technology, 352, 127088.

  56. Trchounian, K., & Trchounian, A. (2015). Hydrogen production from glycerol by Escherichia coli and other bacteria: An overview and perspectives. Applied Energy, 156, 174–184.

    Article  CAS  Google Scholar 

  57. Yu, Q., He, J., Zhao, Q., Wang, X., Zhi, Y., Li, X., & Ge, B. (2021). Regulation of nitrogen source for enhanced photobiological H2 production by co-culture of Chlamydomonas reinhardtii and Mesorhizobium sangaii. Algal Research, 58, 102422.

    Article  Google Scholar 

  58. Wang, J., & Yin, Y. (2021). Clostridium species for fermentative hydrogen production: An overview. International Journal of Hydrogen Energy, 46(70), 34599–34625.

    Article  CAS  Google Scholar 

  59. Zahedi, S., Sales, D., Romero, L. I., & Solera, R. (2013). Hydrogen production from the organic fraction of municipal solid waste in anaerobic thermophilic acidogenesis: Influence of organic loading rate and microbial content of the solid waste. Bioresource Technology, 129, 85–91.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The authors acknowledge the economical support given by the project titled “Estudio de los mecanismos que rigen cambios metabólicos de cultivos foto-heteretróficos debidos a bio-aumentación usando herramientas de biología de sistemas” with reference number 682137 that is funded by the Consejo Nacional de Ciencia y Tecnología (CONACyT) of the Mexican government. This work was also funded by IPN grant 20220846.

Author information

Authors and Affiliations

  1. Bioprocesses Department, UPIBI, Instituto Politécnico Nacional, Mexico City, Mexico

    D. A. Lozano, C. Niño-Navarro & I. Chairez

  2. Institute of Advanced Materials for Sustainable Manufacturing, Tecnologico de Monterrey, Monterrey, Mexico

    I. Chairez

  3. Bioengineering Department, UPIBI, Instituto Politécnico Nacional, Mexico City, Mexico

    E. Salgado-Manjarrez & E. I. García-Peña

Authors
  1. D. A. Lozano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Niño-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Chairez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Salgado-Manjarrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. I. García-Peña
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Daniel Lozano: conceptualization, literature search, data analysis, original draft

Cristina Niño Navarro: conceptualization, literature search, and data analysis

Isaac Chairez: conceptualization, critical revision of the work, and editing

Edgar Salgado Manjarrez: data analysis, critical revision of the work, and editing

Elvia Inés García Peña: conceptualization critical revision of the work and editing.

Corresponding author

Correspondence to I. Chairez.

Ethics declarations

Ethics Approval

Not applicable

Consent to Participate

Not applicable

Consent for Publication

Not applicable

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lozano, D.A., Niño-Navarro, C., Chairez, I. et al. Intensification of Hydrogen Production by a Co-culture of Syntrophomonas wolfei and Rhodopseudomonas palustris Employing High Concentrations of Butyrate as a Substrate. Appl Biochem Biotechnol 195, 1800–1822 (2023). https://doi.org/10.1007/s12010-022-04220-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04220-z

Keywords

Search

Navigation