Advances and Bottlenecks in Microbial Hydrogen Production Stephen, Alan J.; Archer, Sophie A.; Orozco, Rafael L.; Macaskie, Lynne E
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by University of Birmingham Research Portal University of Birmingham Advances and bottlenecks in microbial hydrogen production Stephen, Alan J.; Archer, Sophie A.; Orozco, Rafael L.; Macaskie, Lynne E. DOI: 10.1111/1751-7915.12790 License: Creative Commons: Attribution (CC BY) Document Version Publisher's PDF, also known as Version of record Citation for published version (Harvard): Stephen, AJ, Archer, SA, Orozco, RL & Macaskie, LE 2017, 'Advances and bottlenecks in microbial hydrogen production', Microbial Biotechnology, vol. 10, no. 5, pp. 1120-1127. https://doi.org/10.1111/1751-7915.12790 Link to publication on Research at Birmingham portal General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. 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Biohydrogen has been reviewed 2TT, UK. in comparison with other hydrogen production processes (Nikolaidis and Poullikkas, 2017). Biohydrogen embraces any H2 production involving bio- Summary logical material (Mohan and Pandey, 2013). The energy source can be solar or can come from conversion of fixed Biological production of hydrogen is poised to carbon substrates (or both, in various combinations). An become a significant player in the future energy mix. approach to CO -end of pipe treatment (e.g. from flue gas This review highlights recent advances and bottle- 2 from fossil fuel combustion or carbon-neutral fermentation necks in various approaches to biohydrogen pro- of biomass) is to grow algae on waste CO . Algal biohydro- cesses, often in concert with management of organic 2 gen production is well-described, but O from algal oxy- wastes or waste CO . Some key bottlenecks are 2 2 genic photosynthesis inhibits the hydrogenase that makes highlighted in terms of the overall energy balance of H .Akeystudy(Kubaset al., 2017) will open the way to the process and highlighting the need for economic 2 developing O -resistant hydrogenase. Emerging technol- and environmental life cycle analyses with regard 2 ogy uses cyanobacteria (blue-green algae) that make H also to socio-economic and geographical issues. 2 via hydrogenase and also nitrogenase; their O2-sensitivity is managed by temporal separation of photosynthetic O2 evolution and nitrogenase action, and by compartmenta- Introduction lization into microanaerobic heterocysts (Tiwari and Pan- Hydrogen provides a CO2-free sustainable alternative to dey, 2012). Despite a note that cyanobacterial fossil fuels. A pioneering global initiative, the ‘Hydrogen biohydrogen is probably uneconomic (Singh et al., 2016), Council’, comprising thirteen leading energy, transport an environmental life cycle analysis (LCA) has shown for and related industries, intends to increase investment in the first time that cyanobacterial bio-H2 has the potential to the hydrogen and fuel cell sectors (currently €1.4 be a competitor to desulfurized natural gas; the associated À Bn year 1) to stimulate hydrogen as a key part of the environmental impact of producing and extracting each future energy mix via new policies and schemes (Anon, gas, including use in a solid oxide fuel cell, was calculated 2017). and simulated respectively using the LCA software SIMAPRO Hydrogen is currently obtained mainly by steam (Archer et al., 2017). This research used published data reforming of hydrocarbons, releasing multiple green- from a raceway growth system (James et al., 2009). How- house gas emissions (DOE, 2013). Hence, new H2 pro- ever, at latitudes above ~40°N, the generally low incident duction methods are required such as biological solar energy makes stand-alone photobiological H2 sys- production (bio-H2; Dincer and Acar, 2015). H biotech- tems seasonal and uneconomic without some form of pro- nologies are maturing towards benchmarking against cess intensification. Boosting light delivery (e.g. LEDs, established clean energy from electrolysis of water, solar quantum dots) can be effective, but these may risk pho- photovoltaics and wind farms. Biohydrogen can be made topigment saturation and inhibition; this approach may be fermentatively from wastes, providing a simultaneous questionable economically and would be best addressed method of organic waste management (Chang et al., by a life cycle analysis. In sunny countries, light is plentiful, but in this case, ‘delivering cold’ is needed to extend crop Received 28 June, 2017; accepted 1 July, 2017. product and food life; cooling is energy-demanding and a *For correspondence. E-mail [email protected]; Tel. (44) global challenge (Strahan, 2017). 121 4145889; Fax (44) 121 4145925. Another challenge is organic materials from agri-food Microbial Biotechnology (2017) 10(5), 1120–1127 doi:10.1111/1751-7915.12790 and municipal wastes, which must be managed to avoid Funding Information landfilling which yields methane, a potent greenhouse Natural Environment Research Council (NE/L014076/1). gas. Current practices use anaerobic digestion (AD) with ª 2017 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology . This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Biohydrogen production 1121 biogas – methane used for power. We review some The mixed-acid fermentation, while irreversible, is À1 options for combining waste treatments with bio-H2 tech- thermodynamically limited to 2–4 mol H2 mol hexose nology as possibly the best approach to tackling effec- (Hallenbeck, 2012). The ‘NADH pathway’ of some tively these dual socio-economic problems; stand-alone microorganisms (Hallenbeck, 2012, 2017) can deliver a biohydrogen is possibly uneconomic, but this awaits a higher H yield, but is reversible under a positive H2 partial life cycle analysis, currently in progress. pressure, which is required for with a downstream H fuel cell. Thermophilic bacteria have advantages but require input of heat energy. Hence, the focus has been mainly on Biohydrogen production from waste: fermentation mesophilic bacteria (Balachandar et al., 2013). strategies for sustainable ‘waste to hydrogen Most mixed-acid fermentations follow a similar sche- energy’ matic: the cell forms reduced metabolic end-products: Fermentation is the disposal of excess metabolic reduc- organic acids (including toxic formate) and alcohol À1 tant (NADH) onto organic compounds in the absence of (Fig. 1A). Up to 2 mol H2 mol hexose (Hallenbeck and À alternative electron acceptors such as O2 and NO3 (Guo Ghosh, 2009) is produced via the activity of formate et al., 2010). The mixed-acid fermentation (‘dark fermen- hydrogen lyase (which splits formate to H2 + CO2), that tation’) pathway of the paradigm Escherichia coli (Fig. 1A) is < 20% of the theoretical maximum H2. Sustained bio- is simple, has high rates of H2 production but has limita- H2 production is limited by end-product (ethanol) toxicity tions (Saratale et al., 2013; Fig. 1A inset). Hexose sugars and acidification of the medium by accumulating organic À1 can stoichiometrically deliver 12 mol H2 mol hexose . acids (Redwood, 2007). Fig. 1. Mixed-acid fermentation (MAF) of E. coli (A) and use of purple non-sulfur bacteria (B) in photofermentation (PF) of organic acids (OAs) into H2. The organic acids are taken up by (e.g.) R. sphaeroides, and reducing power is generated as NADH (not shown). This reducing power can either be used for polyhydroxybutyrate synthesis or growth to maintain cellular redox or alternatively can be used for H2 production under light when growth is restricted by limitation of N or P source. Italicized bottlenecks are those overcome by use of the dual system (see text). ª 2017 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology, Microbial Biotechnology, 10, 1120–1127 1122 A. J. Stephen et al. The organic acids provide a means to overcome the Redwood (2007) calculated the break-even current thermodynamic limitation via their use in a coupled efficiency to quantify the role played by specific organic photofermentation reactor (Redwood et al., 2012a,b; Hal- acids (Table 1). Butyrate is the most attractive organic lenbeck, 2013, 2017) via electrodialysis (Fig 2). If acid for electrodialysis with the lowest break-even cur- organic acid mixtures are fed to purple non-sulfur bacte- rent efficiency at 13% (Table 1).