Skip to main content

Advertisement

Log in

Introducing capnophilic lactic fermentation in a combined dark-photo fermentation process: a route to unparalleled H2 yields

  • Bioenergy and biofuels
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Two-stage process based on photofermentation of dark fermentation effluents is widely recognized as the most effective method for biological production of hydrogen from organic substrates. Recently, it was described an alternative mechanism, named capnophilic lactic fermentation, for sugar fermentation by the hyperthermophilic bacterium Thermotoga neapolitana in CO2-rich atmosphere. Here, we report the first application of this novel process to two-stage biological production of hydrogen. The microbial system based on T. neapolitana DSM 4359T and Rhodopseudomonas palustris 42OL gave 9.4 mol of hydrogen per mole of glucose consumed during the anaerobic process, which is the best production yield so far reported for conventional two-stage batch cultivations. The improvement of hydrogen yield correlates with the increase in lactic production during capnophilic lactic fermentation and takes also advantage of the introduction of original conditions for culturing both microorganisms in minimal media based on diluted sea water. The use of CO2 during the first step of the combined process establishes a novel strategy for biohydrogen technology. Moreover, this study opens the way to cost reduction and use of salt-rich waste as feedstock.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abo-Hashesh M, Ghosh D, Tourigny A, Taous A, Hallenbeck PC (2011) Single stage photofermentative hydrogen production from glucose: an attractive alternative to two stage photofermentation or co-culture approaches. Int J Hydrog Energy 36:13889–13895. doi:10.1016/j.ijhydene.2011.02.122

    Article  CAS  Google Scholar 

  • Abo-Hashesh M, Desaunay N, Hallenbeck PC (2013) High yield single stage conversion of glucose to hydrogen by photofermentation with continuous cultures of Rhodobacter capsulatus JP91. Bioresour Technol 128:513–517. doi:10.1016/j.biortech.2012.10.091

  • Adessi A, De Philippis R (2014) Photobioreactor design and illumination systems for H2 production with anoxygenic photosynthetic bacteria: a review. Int J Hydrog Energy 39:3127–3141. doi:10.1016/j.ijhydene.2013.12.084

    Article  CAS  Google Scholar 

  • Adessi A, McKinlay JB, Harwood CS, De Philippis R (2012) A Rhodopseudomonas palustris nifA* mutant produces H2 from NH4 +-containing vegetable wastes. Int J Hydrog Energy 37:15893–15900. doi:10.1016/j.ijhydene.2012.08.009

    Article  CAS  Google Scholar 

  • APHA (1992) Standard methods for the examination of water and wastewater, 18th edn. APHA, AWWA and WEF, Washington DC

    Google Scholar 

  • Asada Y, Tokumoto M, Aihara Y, Oku M, Ishimi K, Wakayama T, Miyake J, Tomiyama M, Kohno H (2006) Hydrogen production by co-cultures of Lactobacillus and a photosynthetic bacterium, Rhodobacter sphaeroides RV. Int J Hydrog Energy 31:1509–1513. doi:10.1016/j.ijhydene.2006.06.017

    Article  CAS  Google Scholar 

  • Basile MA, Carfagna C, Cerruti P, Gomez d’Ayala G, Fontana A, Gambacorta A, Malinconico M, Dipasquale L (2012) Continuous hydrogen production by immobilized cultures of Thermotoga neapolitana on an acrylic hydrogel with pH-buffering properties. RSC Adv 2:3611–3614. doi:10.1039/C2RA01025A

    Article  CAS  Google Scholar 

  • Bianchi L, Mannelli F, Viti C, Adessi A, De Philippis R (2010) Hydrogen-producing purple non-sulfur bacteria isolated from the trophic lake Averno (Naples, Italy). Int J Hydrog Energy 35:12216–12223. doi:10.1016/j.ijhydene.2010.08.038

    Article  CAS  Google Scholar 

  • Burris RH (1991) Nitrogenases. J Biol Chem 266:9339–9342

    CAS  PubMed  Google Scholar 

  • Carlozzi P, Buccioni A, Minieri S, Pushparaj B, Piccardi R, Ena A, Pintucci C (2010) Production of bio-fuels (hydrogen and lipids) through a photofermentation process. Bioresour Technol 101:3115–3120. doi:10.1016/j.biortech.2009.12.049

    Article  CAS  PubMed  Google Scholar 

  • Chen CY, Yang MH, Yeh KL, Liu CH, Chang JS (2008) Biohydrogen production using sequential two stage dark and photo fermentation processes. Int J Hydrog Energy 33:4755–4762. doi:10.1016/j.ijhydene.2008.06.055

    Article  CAS  Google Scholar 

  • d’Ippolito G, Dipasquale L, Vella FM, Romano I, Gambacorta A, Cutignano A, Fontana A (2010) Hydrogen metabolism in the extreme thermophile Thermotoga neapolitana. Int J Hydrog Energy 35:2290–2295. doi:10.1016/j.ijhydene.2009.12.044

    Article  Google Scholar 

  • d’Ippolito G, Dipasquale L, Fontana A (2014) Recycling of carbon dioxide and acetate as lactic acid by the hydrogen-producing bacterium Thermotoga neapolitana. ChemSusChem 7:2678–2683. doi:10.1002/cssc.201402155

    Article  PubMed  Google Scholar 

  • Dipasquale L, d’Ippolito G, Gallo C, Vella FM, Gambacorta A, Picariello G, Fontana A (2012) Hydrogen production by the thermophilic eubacterium Thermotoga neapolitana from storage polysaccharides of the CO2-fixing diatom Thalassiosira weissflogii. Int J Hydrog Energy 37:12250–12257. doi:10.1016/j.ijhydene.2012.05.160

    Article  CAS  Google Scholar 

  • Dipasquale L, d’Ippolito G, Fontana A (2014) Capnophilic lactic fermentation and hydrogen synthesis by Thermotoga neapolitana: an unexpected deviation from the dark fermentation model. Int J Hydrog Energy 39:4857–4862. doi:10.1016/j.ijhydene.2013.12.183

    Article  CAS  Google Scholar 

  • Eriksen NT, Nielsen TM, Iversen N (2008) Hydrogen production in anaerobic and microaerobic Thermotoga neapolitana. Biotechnol Lett 30:103–109. doi:10.1007/s10529-007-9520-5

    Article  CAS  PubMed  Google Scholar 

  • Foglia D, Wukovits W, Friedl A, de Vrije T, Claassen PAM (2011) Fermentative hydrogen production: influence of application of mesophilic and thermophilic bacteria on mass and energy balances. Chem Eng Trans 25:815–820. doi:10.3303/CET1125136

    Google Scholar 

  • Ghosh D, Sobro IF, Hallenbeck PC (2012) Optimization of the hydrogen yield from single-stage photofermentation of glucose by Rhodobacter capsulatus JP91 using response surface methodology. Bioresour Technol 123:199–206. doi:10.1016/j.biortech.2012.07.061

    Article  CAS  PubMed  Google Scholar 

  • Guédon E, Martin-Verstraete I (2006) Cysteine metabolism and its regulation in bacteria. In: Wendisch VF (ed) Amino acid biosynthesis. Springer, Berlin, pp 196–218

    Google Scholar 

  • Hallenbeck PC (2014) Bioenergy from micro-organisms: an overview. In: Zannoni D, De Philippis R (eds) Microbial BioEnergy: hydrogen production. Springer, Dordrecht, pp 3–21

    Chapter  Google Scholar 

  • Hallenbeck PC, Abo-Hashesh M, Ghosh D (2012) Strategies for improving biological hydrogen production. Bioresour Technol 110:1–9. doi:10.1016/j.biortech.2012.01.103

    Article  CAS  PubMed  Google Scholar 

  • Igeño MI, González del Moral C, Castillo F, Caballero FJ (1995) Halotolerance of the phototrophic bacterium Rhodobacter capsulatus E1F1 is dependent on the nitrogen source. Appl Environ Microbiol 61:2970–2975

    PubMed  PubMed Central  Google Scholar 

  • Kars G, Gündüz U, Yücel M, Türker L, Eroğlu I (2006) Hydrogen production and transcriptional analysis of nifD, nifK and hupS genes in Rhodobacter sphaeroides O.U.001 grown in media with different concentrations of molybdenum and iron. Int J Hydrog Energy 31:1536–1544. doi:10.1016/j.ijhydene.2006.06.021

    Article  CAS  Google Scholar 

  • Kawaguchi H, Hashimoto K, Hirata K, Miyamoto K (2001) H2 production from algal biomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillus amylovorus. J Biosci Bioeng 91:277–282. doi:10.1016/S1389-1723(01)80134-1

    Article  CAS  PubMed  Google Scholar 

  • Keskin T, Abo-Hashesh M, Hallenbeck PC (2011) Photofermentative hydrogen production from wastes. Bioresour Technol 102:8557–8568. doi:10.1016/j.biortech.2011.04.004

    Article  CAS  PubMed  Google Scholar 

  • Kim MS, Baek JS, Yun YS, Sim SJ, Park S, Kim SC (2006) Hydrogen production from Chlamydomonas reinhardtii biomass using a two-step conversion process: anaerobic conversion and photosynthetic fermentation. Int J Hydrog Energy 31:812–816. doi:10.1016/j.ijhydene.2005.06.009

    Article  CAS  Google Scholar 

  • Kim MS, Kim DH, Cha J, Lee JK (2012) Effect of carbon and nitrogen sources on photo-fermentative H2 production associated with nitrogenase, uptake hydrogenase activity, and PHB accumulation in Rhodobacter sphaeroides KD131. Bioresour Technol 116:179–183. doi:10.1016/j.biortech.2012.04.0111

    Article  CAS  PubMed  Google Scholar 

  • Koku H, Eroğlu I, Gündüz U, Yücel M, Türker L (2003) Kinetics of biological hydrogen production by the photosynthetic bacterium Rhodobacter sphaeroides O.U. 001. Int J Hydrog Energy 28:381–388. doi:10.1016/S0360-3199(02)00080-0

    Article  CAS  Google Scholar 

  • Lee H-S, Vermaas WFJ, Rittmann BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28:262–271. doi:10.1016/j.tibtech.2010.01.007

    Article  CAS  PubMed  Google Scholar 

  • Lo YC, Chen SD, Chen CY, Huang TI, Lin CY, Chang JS (2008) Combining enzymatic hydrolysis and dark–photo fermentation processes for hydrogen production from starch feedstock: a feasibility study. Int J Hydrog Energy 33:5224–5233. doi:10.1016/j.ijhydene.2008.05.014

    Article  CAS  Google Scholar 

  • Miyake J, Kawamura S (1987) Efficiency of light energy conversion to hydrogen by the photosynthetic bacterium Rhodobacter sphaeroides. Int J Hydrog Energy 3:147–149. doi:10.1016/0360-3199(87)90146-7

    Article  Google Scholar 

  • Miyake J, Mao XY, Kawamura S (1984) Photoproduction of hydrogen from glucose by a co-culture of a photosynthetic bacteria and Clostridium butyricum. J Ferment Technol 62:531–535

    CAS  Google Scholar 

  • Munro SA, Zinder SH, Walker LP (2009) The fermentation stoichiometry of Thermotoga neapolitana and influence of temperature, oxygen, and pH on hydrogen production. Biotechnol Prog 25:1035–1042. doi:10.1002/btpr.201doi

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TAD, Han SJ, Kim JP, Kim MS, Sim SJ (2010) Hydrogen production of the hyperthermophilic eubacterium, Thermotoga neapolitana under N2 sparging condition. Bioresour Technol 101:S38–S41. doi:10.1016/j.biortech.2009.03.041

    Article  CAS  PubMed  Google Scholar 

  • Patel SKS, Kumar P, Kalia VC (2012) Enhancing biological hydrogen production through complementary microbial metabolisms. Int J Hydrog Energy 37:10590–10603. doi:10.1016/j.ijhydene.2012.04.045

    Article  CAS  Google Scholar 

  • Redwood MD, Paterson-Beedle M, Macaskie LE (2009) Integrating dark and light bio-hydrogen production strategies: towards the hydrogen economy. Rev Environ Sci Biotechnol 8:149–185. doi:10.1007/s11157-008-9144-9

    Article  CAS  Google Scholar 

  • Rittmann S, Herwig C (2012) A comprehensive and quantitative review of dark fermentative biohydrogen production. Microb Cell Fact 11:115. doi:10.1186/1475-2859-11-115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Show KY, Lee DJ, Tay JH, Lin CY, Chang JS (2012) Biohydrogen production: current perspectives and the way forward. Int J Hydrog Energy 37:15616–15631. doi:10.1016/j.ijhydene.2012.04.109

    Article  CAS  Google Scholar 

  • Vincenzini M, Marchini A, Ena A, De Philippis R (1997) H2 and poly-β-hydroxybutyrate, two alternative chemicals from purple non sulfur bacteria. Biotechnol Lett 19:759–762. doi:10.1023/A:1018336209252

    Article  CAS  Google Scholar 

  • Woodward J, Orr M, Cordray K, Greenbaum E (2000) Biotechnology: enzymatic production of biohydrogen. Nature 405:1014–1015. doi:10.1038/35016633

    Article  CAS  PubMed  Google Scholar 

  • Yokoi H, Maki R, Hirose J, Hayashi S (2002) Microbial production of hydrogen from starch-manufacturing wastes. Biomass Bioenerg 22:389–395. doi:10.1016/S0961-9534(02)00014-4

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the Italian Ministry of the Environment (MATTM; project PIRODE), MIUR (PON01_02740 “Sfruttamento Integrato di Biomasse Algali in Filiera Energetica di Qualità - SIBAFEQ”, Programma Operativo Nazionale - Ricerca e Competitività 2007–2013), and CNR (Italian National Research Centre) (EFOR project), Ente Cassa di Risparmio di Firenze (Project HYDROLAB2). RDP would also like to mention the contribution given to his activities by the participation in the IEA-HIA (International Energy Agency-Hydrogen Implementation Agreement), Annex 21 “Bioinspired and biological hydrogen”.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to A. Fontana or R. De Philippis.

Additional information

L. Dipasquale and A. Adessi equally contributed to this work as first authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dipasquale, L., Adessi, A., d’Ippolito, G. et al. Introducing capnophilic lactic fermentation in a combined dark-photo fermentation process: a route to unparalleled H2 yields. Appl Microbiol Biotechnol 99, 1001–1010 (2015). https://doi.org/10.1007/s00253-014-6231-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6231-4

Keywords

Navigation