Advertisement

Biological hydrogen production: molecular and electrolytic perspectives

  • Ganesh Mahidhara
  • Hannah Burrow
  • Ch. Sasikala
  • Ch. V. RamanaEmail author
Review
  • 75 Downloads

Abstract

Exploration of renewable energy sources is an imperative task in order to replace fossil fuels and to diminish atmospheric pollution. Hydrogen is considered one of the most promising fuels for the future and implores further investigation to find eco-friendly ways toward viable production. Expansive processes like electrolysis and fossil fuels are currently being used to produce hydrogen. Biological hydrogen production (BHP) displays recyclable and economical traits, and is thus imperative for hydrogen economy. Three basic modes of BHP were investigated, including bio photolysis, photo fermentation and dark fermentation. Photosynthetic microorganisms could readily serve as powerhouses to successively produce this type of energy. Cyanobacteria, blue green algae (bio photolysis) and some purple non-sulfur bacteria (Photo fermentation) utilize solar energy and produce hydrogen during their metabolic processes. Ionic species, including hydrogen (H+) and electrons (e) are combined into hydrogen gas (H2), with the use of special enzymes called hydrogenases in the case of bio photolysis, and nitrogenases catalyze the formation of hydrogen in the case of photo fermentation. Nevertheless, oxygen sensitivity of these enzymes is a drawback for bio photolysis and photo fermentation, whereas, the amount of hydrogen per unit substrate produced appears insufficient for dark fermentation. This review focuses on innovative advances in the bioprocess research, genetic engineering and bioprocess technologies such as microbial fuel cell technology, in developing bio hydrogen production.

Keywords

Photo fermentation Bio photolysis Dark fermentation Microbial electrolytic cells 

Notes

Acknowledgements

This work is financially supported by the council of scientific and industrial research, New Delhi under CSIR RA Postdoctoral Fellowship Scheme.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdalla AM, Hossain S, Nisfindy OB, Azad AT, Dawood M, Azad AK (2018) Hydrogen production, storage, transportation and key challenges with applications: a review. Energy Convers Manag 165:602–627.  https://doi.org/10.1016/j.enconman.2018.03.088 CrossRefGoogle Scholar
  2. Adessi A, Concato M, Sanchini A, Rossi F, De Philippis R (2016) Hydrogen production under salt stress conditions by a freshwater Rhodopseudomonas palustris strain. Appl Microbiol Biotechnol 100:2917–2926.  https://doi.org/10.1007/s00253-016-7291-4 CrossRefPubMedGoogle Scholar
  3. Anjana K, Kaushik A (2014) Enhanced hydrogen production by immobilized cyanobacterium Lyngbya perelegans under varying anaerobic conditions. Biomass Bioenergy 63:54–57.  https://doi.org/10.1016/j.biombioe.2014.01.019 CrossRefGoogle Scholar
  4. Archana A, Sasikala C, Ramana CV (2003) Augmentation of H2 photoproduction in Rhodopseudomonas palustris by N-heterocyclic aromatic compounds. Biotechnol Lett 25:79–82.  https://doi.org/10.1023/A:1021717424268 CrossRefPubMedGoogle Scholar
  5. Baykara SZ (2018) Hydrogen: a brief overview on its sources, production and environmental impact. Int J Hydrog Energy 43:10605–10614.  https://doi.org/10.1016/j.ijhydene.2018.02.022 CrossRefGoogle Scholar
  6. Bičáková O, Straka P (2012) Production of hydrogen from renewable resources and its effectiveness. Int J Hydrogen Energy 37:11563–11578.  https://doi.org/10.1016/j.ijhydene.2012.05.047 CrossRefGoogle Scholar
  7. Call D, Logan BE (2008) Hydrogen production in a single chamber microbial electrolysis cell lacking a membrane. Environ Sci Technol 42:3401–3406CrossRefGoogle Scholar
  8. Chen C-Y, Yang M-H, Yeh K-L, Liu C-H, Chang J-S (2008) Biohydrogen production using sequential two-stage dark and photo fermentation processes. International J Hydrogen Energy 33:4755–4762.  https://doi.org/10.1016/j.ijhydene.2008.06.055 CrossRefGoogle Scholar
  9. Cheng S, Logan BE (2007) Sustainable and efficient biohydrogen production via electrohydrogenesis. Proc Natl Acad Sci 104:18871–18873.  https://doi.org/10.1073/pnas.0706379104 CrossRefPubMedGoogle Scholar
  10. Delucchi MA, Yang C, Burke AF, Ogden JM, Kurani K, Kessler J, Sperling D (2014) An assessment of electric vehicles: technology, infrastructure requirements, greenhouse-gas emissions, petroleum use, material use, lifetime cost, consumer acceptance and policy initiatives. Philos Trans Ser A 372:20120325.  https://doi.org/10.1098/rsta.2012.0325 CrossRefGoogle Scholar
  11. Ebrahimzadeh AA, Khazaee I, Fasihfar A (2018) Numerical investigation of dimensions and arrangement of obstacle on the performance of PEM fuel cell. Heliyon 4:e00974–e00974.  https://doi.org/10.1016/j.heliyon.2018.e00974 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ge B, He J, Zhang Q, Wei Y, Xi L, Khan NU, Huang F (2019) Evaluation of various sulfides for enhanced photobiological H2 production by a dual-species co-culture system of Chlamydomonas reinhardtii and Thiomonas intermedia. Process Biochem 82:110–116.  https://doi.org/10.1016/j.procbio.2019.03.028 CrossRefGoogle Scholar
  13. Godaux D, Bailleul B, Berne N, Cardol P (2015) Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-Like1-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol 168:648–658.  https://doi.org/10.1104/pp.15.00105 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hallenbeck PC, Abo-Hashesh M, Ghosh D (2012) Strategies for improving biological hydrogen production. Bioresour Technol 110:1–9.  https://doi.org/10.1016/j.biortech.2012.01.103 CrossRefPubMedGoogle Scholar
  15. Hassan AHS, Mietzel T, Brunstermann R, Schmuck S, Schoth J, Küppers M, Widmann R (2018) Fermentative hydrogen production from low-value substrates. World J Microbiol Biotechnol 34:176.  https://doi.org/10.1007/s11274-018-2558-9 CrossRefPubMedGoogle Scholar
  16. Head IM, Gray ND (2016) Microbial Biotechnology 2020; microbiology of fossil fuel resources. Microbial Biotechnol 9:626–634.  https://doi.org/10.1111/1751-7915.12396 CrossRefGoogle Scholar
  17. Hitit ZY, Zampol Lazaro C, Hallenbeck PC (2017) Increased hydrogen yield and COD removal from starch/glucose based medium by sequential dark and photo-fermentation using Clostridium butyricum and Rhodopseudomonas palustris. Int J Hydrogen Energy 42:18832–18843.  https://doi.org/10.1016/j.ijhydene.2017.05.161 CrossRefGoogle Scholar
  18. Kaushik A, Anjana K (2011) Biohydrogen production by Lyngbya perelegans: influence of physico-chemical environment. Biomass Bioenergy 35:1041–1045.  https://doi.org/10.1016/j.biombioe.2010.11.024 CrossRefGoogle Scholar
  19. Keskin T, Abo-Hashesh M, Hallenbeck PC (2011) Photofermentative hydrogen production from wastes. Bioresour Technol 102:8557–8568.  https://doi.org/10.1016/j.biortech.2011.04.004 CrossRefPubMedGoogle Scholar
  20. Kim YM, Cho HS, Jung GY, Park JM (2011) Engineering the pentose phosphate pathway to improve hydrogen yield in recombinant Escherichia coli. 108:2941–2946.  https://doi.org/10.1002/bit.23259 CrossRefPubMedGoogle Scholar
  21. Kim Y, Logan BE (2011) Hydrogen production from inexhaustible supplies of fresh and salt water using microbial reverse-electrodialysis electrolysis cells. Proc Natl Acad Sci 108:16176–16181.  https://doi.org/10.1073/pnas.1106335108 CrossRefPubMedGoogle Scholar
  22. Kosourov S, Jokel M, Aro E-M, Allahverdiyeva Y (2018) A new approach for sustained and efficient H2 photoproduction by Chlamydomonas reinhardtii. Energy Environ Sci 11:1431–1436.  https://doi.org/10.1039/C8EE00054A CrossRefGoogle Scholar
  23. Kosourov SN, Seibert M (2009) Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions. Biotechnol Bioeng 102:50–58.  https://doi.org/10.1002/bit.22050 CrossRefPubMedGoogle Scholar
  24. Krujatz F, Härtel P, Helbig K, Haufe N, Thierfelder S, Bley T, Weber J (2015) Hydrogen production by Rhodobacter sphaeroides DSM 158 under intense irradiation. Bioresour Technol 175:82–90.  https://doi.org/10.1016/j.biortech.2014.10.061 CrossRefPubMedGoogle Scholar
  25. Kwon S-m, Kim MJ, Kang S, Kim T (2019) Development of a high-storage-density hydrogen generator using solid-state NaBH4 as a hydrogen source for unmanned aerial vehicles. Appl Energy 251:113331.  https://doi.org/10.1016/j.apenergy.2019.113331 CrossRefGoogle Scholar
  26. Lecker B, Illi L, Lemmer A, Oechsner H (2017) Biological hydrogen methanation—a review. Bioresour Technol 245:1220–1228.  https://doi.org/10.1016/j.biortech.2017.08.176 CrossRefPubMedGoogle Scholar
  27. Li H et al (2018) Improved photobio-H2 production regulated by artificial miRNA targeting psbA in green microalga Chlamydomonas reinhardtii. Biotechnology Biofuels 11:36.  https://doi.org/10.1186/s13068-018-1030-2 CrossRefGoogle Scholar
  28. Li Y, Yang HY, Shen JY, Mu Y, Yu HQ (2016) Enhancement of azo dye decolourization in a MFC-MEC coupled system. Bioresour Technol 202:93–100.  https://doi.org/10.1016/j.biortech.2015.11.079 CrossRefPubMedGoogle Scholar
  29. Ma D, Zhai S, Wang Y, Liu A, Chen C (2019) TiO(2) photocatalysis for transfer hydrogenation. Molecules 24(2):330.  https://doi.org/10.3390/molecules24020330 CrossRefPubMedCentralGoogle Scholar
  30. Mahidhara G, Ch ChS, Ch VR (2017) Comparative metabolomic studies of Alkanivorax xenomutans showing differential power output in a three chambered microbial fuel cell. World J Microbiol Biotechnol 33(6):102.  https://doi.org/10.1007/s11274-017-2268-8 CrossRefPubMedGoogle Scholar
  31. Mahidhara G, Chintalapati VR (2015) Eco-physiological and interdisciplinary approaches for empowering biobatteries. Ann Microbiol 66(2):543.  https://doi.org/10.1007/s13213-015-1148-4 CrossRefGoogle Scholar
  32. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086.  https://doi.org/10.1007/s00425-007-0609-9 CrossRefPubMedGoogle Scholar
  33. Milrad Y, Schweitzer S, Feldman Y, Yacoby I (2018) Green algal hydrogenase activity is outcompeted by carbon fixation before inactivation by oxygen takes place. Plant Physiol 177:918–926.  https://doi.org/10.1104/pp.18.00229 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mishra P, Krishnan S, Rana S, Singh L, Sakinah M, Ab Wahid Z (2019) Outlook of fermentative hydrogen production techniques: an overview of dark, photo and integrated dark-photo fermentative approach to biomass. Energy Strateg Rev 24:27–37.  https://doi.org/10.1016/j.esr.2019.01.001 CrossRefGoogle Scholar
  35. Mishra P, Thakur S, Singh L, Ab Wahid Z, Sakinah M (2016) Enhanced hydrogen production from palm oil mill effluent using two stage sequential dark and photo fermentation. Int J Hydrog Energy 41:18431–18440.  https://doi.org/10.1016/j.ijhydene.2016.07.138 CrossRefGoogle Scholar
  36. Morsy FM (2011) Acetate versus sulfur deprivation role in creating anaerobiosis in light for hydrogen production by Chlamydomonas reinhardtii and Spirulina platensis: two different organisms and two different mechanisms. Photochem Photobiol 87:137–142.  https://doi.org/10.1111/j.1751-1097.2010.00823.x CrossRefPubMedGoogle Scholar
  37. Nagarajan D, Lee D-J, Kondo A, Chang J-S (2017) Recent insights into biohydrogen production by microalgae—from biophotolysis to dark fermentation. Bioresour Technol 227:373–387.  https://doi.org/10.1016/j.biortech.2016.12.104 CrossRefGoogle Scholar
  38. Nagy V et al (2018) Water-splitting-based, sustainable and efficient H2 production in green algae as achieved by substrate limitation of the Calvin–Benson–Bassham cycle. Biotechnol Biofuel 11:69.  https://doi.org/10.1186/s13068-018-1069-0 CrossRefGoogle Scholar
  39. Nikolaidis P, Poullikkas A (2017) A comparative overview of hydrogen production processes. Elsevier, AmsterdamCrossRefGoogle Scholar
  40. Oh S, Logan BE (2005) Hydrogen and electricity production from a food processing wastewater using fermentation and microbial fuel cell technologies. Water Res 39:4673–4682.  https://doi.org/10.1016/j.watres.2005.09.019 CrossRefPubMedGoogle Scholar
  41. Oh Y-K, Raj SM, Jung GY, Park S (2011) Current status of the metabolic engineering of microorganisms for biohydrogen production. Bioresour Technol 102:8357–8367.  https://doi.org/10.1016/j.biortech.2011.04.054 CrossRefPubMedGoogle Scholar
  42. Pachapur VL, Sarma SJ, Brar SK, Le Bihan Y, Buelna G, Verma M (2015) Biohydrogen production by co-fermentation of crude glycerol and apple pomace hydrolysate using co-culture of Enterobacter aerogenes and Clostridium butyricum. Bioresour Technol 193:297–306.  https://doi.org/10.1016/j.biortech.2015.06.095 CrossRefPubMedGoogle Scholar
  43. Polle JEW, Kanakagiri S, Jin E, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems—a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrog Energy 27:1257–1264.  https://doi.org/10.1016/S0360-3199(02)00116-7 CrossRefGoogle Scholar
  44. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Micro 8:1740CrossRefGoogle Scholar
  45. Ramaprasad EVV, Mahidhara G, Sasikala C, Ramana CV (2018) Rhodococcus electrodiphilus sp. nov., a marine electro active actinobacterium isolated from coral reef. Int J Syst Evol Microbiol 68:2644–2649.  https://doi.org/10.1099/ijsem.0.002895 CrossRefPubMedGoogle Scholar
  46. Rivera I, Bakonyi P, Cuautle-Marin MA, Buitron G (2017) Evaluation of various cheese whey treatment scenarios in single-chamber microbial electrolysis cells for improved biohydrogen production. Chemosphere 174:253–259.  https://doi.org/10.1016/j.chemosphere.2017.01.128 CrossRefPubMedGoogle Scholar
  47. Sadaghiani MS, Mehrpooya M (2017) Introducing and energy analysis of a novel cryogenic hydrogen liquefaction process configuration. Int J Hydrog Energy 42:6033–6050.  https://doi.org/10.1016/j.ijhydene.2017.01.136 CrossRefGoogle Scholar
  48. Santoro C et al (2016) Co-generation of hydrogen and power/current pulses from supercapacitive MFCs using novel HER iron-based catalysts. Electrochim Acta 220:672–682.  https://doi.org/10.1016/j.electacta.2016.10.154 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Sasikala C, Ramana CV (1994) Growth and H2 production by Synechococcus spp. using organic/inorganic electron donors. World J Microbiol Biotechnol 10:531–533.  https://doi.org/10.1007/bf00367660 CrossRefPubMedGoogle Scholar
  50. Sasikala K, Ramana CV, Raghuveer Rao P (1992) Photoproduction of hydrogen from the waste water of a distillery by Rhodobacter sphaeroides O.U. 001. Int J Hydrog Energy 17:23–27.  https://doi.org/10.1016/0360-3199(92)90217-K CrossRefGoogle Scholar
  51. Sasikala K, Ramana CV, Raghuveer Rao P, Subrahmanyam M (1990) Effect of gas phase on the photoproduction of hydrogen and substrate conversion efficiency in the photosynthetic bacterium Rhodobacter sphaeroides O.U. 001. Int J Hydrog Energy 15:795–797.  https://doi.org/10.1016/0360-3199(90)90015-Q CrossRefGoogle Scholar
  52. Sasikala CH, Ramana CHV, Rao PR (1995) Regulation of simultaneous hydrogen photoproduction during growth by pH and glutamate in Rhodobacter sphaeroides O.U. 001. Int J Hydrog Energy 20:123–126.  https://doi.org/10.1016/0360-3199(94)E0009-N CrossRefGoogle Scholar
  53. Schneemann A, White JL (2018) Nanostructured metal hydrides for hydrogen storage. Chem Rev 118:10775–10839.  https://doi.org/10.1021/acs.chemrev.8b00313 CrossRefPubMedGoogle Scholar
  54. Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant. J Biotechnol 157:613–619.  https://doi.org/10.1016/j.jbiotec.2011.06.019 CrossRefPubMedGoogle Scholar
  55. Seenithurai S, Chai JD (2018) Electronic and hydrogen storage properties of Li-terminated linear boron chains studied by TAO-DFT. Sci Rep 8:13538.  https://doi.org/10.1038/s41598-018-31947-9 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Seifert K, Zagrodnik R, Stodolny M, Łaniecki M (2018) Biohydrogen production from chewing gum manufacturing residue in a two-step process of dark fermentation and photofermentation. Renew Energy 122:526–532.  https://doi.org/10.1016/j.renene.2018.01.105 CrossRefGoogle Scholar
  57. da Silva Veras T, Mozer TS, da Silva César A (2017) Hydrogen: trends, production and characterization of the main process worldwide. Int J Hydrog Energy 42:2018–2033.  https://doi.org/10.1016/j.ijhydene.2016.08.219 CrossRefGoogle Scholar
  58. Singh H, Das D (2018) Biofuels from microalgae: biohydrogen. In: Jacob-Lopes E, Queiroz Zepka L, Queiroz MI (eds) Energy from microalgae. Springer, Cham, pp 201–228.  https://doi.org/10.1007/978-3-319-69093-3_10 CrossRefGoogle Scholar
  59. Singh L, Wahid ZA (2015) Methods for enhancing bio-hydrogen production from biological process: a review. J Ind Eng Chem 21:70–80.  https://doi.org/10.1016/j.jiec.2014.05.035 CrossRefGoogle Scholar
  60. Song Y-H, Hidayat S, Kim H-K, Park J-Y (2016) Hydrogen production in microbial reverse-electrodialysis electrolysis cells using a substrate without buffer solution. Bioresour Technol 210:56–60.  https://doi.org/10.1016/j.biortech.2016.02.021 CrossRefPubMedGoogle Scholar
  61. Stephen AJ, Archer SA, Orozco RL, Macaskie LE (2017) Advances and bottlenecks in microbial hydrogen production. Microbial Biotechnol 10:1120–1127.  https://doi.org/10.1111/1751-7915.12790 CrossRefGoogle Scholar
  62. Stripp ST et al (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Proc Natl Acad Sci 106:17331–17336.  https://doi.org/10.1073/pnas.0905343106 CrossRefPubMedGoogle Scholar
  63. Sun M et al (2008) An MEC-MFC-coupled system for biohydrogen production from acetate. Environ Sci Technol 42:8095–8100CrossRefGoogle Scholar
  64. Sundara Sekar B, Seol E, Park S (2017) Co-production of hydrogen and ethanol from glucose in Escherichia coli by activation of pentose-phosphate pathway through deletion of phosphoglucose isomerase (pgi) and overexpression of glucose-6-phosphate dehydrogenase (zwf) and 6-phosphogluconate dehydrogenase (gnd). Biotechnol Biofuels 10:85.  https://doi.org/10.1186/s13068-017-0768-2 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Tremblay PL, Zhang T (2015) Electrifying microbes for the production of chemicals. Front Microbiol 6:201.  https://doi.org/10.3389/fmicb.2015.00201 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Uyar B, Gurgan M, Ozgur E, Gunduz U, Yucel M, Eroglu I (2015) Hydrogen production by hup(−) mutant and wild-type strains of Rhodobacter capsulatus from dark fermentation effluent of sugar beet thick juice in batch and continuous photobioreactors. Bioprocess Biosyst Eng 38:1935–1942.  https://doi.org/10.1007/s00449-015-1435-2 CrossRefPubMedGoogle Scholar
  67. Vinokurov VA et al (2017) Halloysite nanoclay based CdS formulations with high catalytic activity in hydrogen evolution reaction under visible light irradiation. ACS Sustain Chem Eng 5:11316–11323.  https://doi.org/10.1021/acssuschemeng.7b02272 CrossRefGoogle Scholar
  68. Volgusheva AA et al (2017) Comparative analyses of H2 photoproduction in magnesium- and sulfur-starved Chlamydomonas reinhardtii cultures. Physiol Plant 161:124–137.  https://doi.org/10.1111/ppl.12576 CrossRefPubMedGoogle Scholar
  69. Volgusheva A, Kukarskikh G, Krendeleva T, Rubin A, Mamedov F (2015) Hydrogen photoproduction in green algae Chlamydomonas reinhardtii under magnesium deprivation. RSC Adv 5:5633–5637.  https://doi.org/10.1039/C4RA12710B CrossRefGoogle Scholar
  70. Wang A, Sun D, Cao G, Wang H, Ren N, Wu WM, Logan BE (2011) Integrated hydrogen production process from cellulose by combining dark fermentation, microbial fuel cells, and a microbial electrolysis cell. Bioresour Technol 102:4137–4143.  https://doi.org/10.1016/j.biortech.2010.10.137 CrossRefPubMedGoogle Scholar
  71. Wang J, Yin Y (2018) Fermentative hydrogen production using various biomass-based materials as feedstock. Renew Sustain Energy Rev 92:284–306.  https://doi.org/10.1016/j.rser.2018.04.033 CrossRefGoogle Scholar
  72. Wang B, Zeng C, Chu KH, Wu D, Yip HY, Ye L, Wong PK (2017) Enhanced biological hydrogen production from Escherichia coli with surface precipitated cadmium sulfide nanoparticles. Adv Energy Mater 7:1700611.  https://doi.org/10.1002/aenm.201700611 CrossRefGoogle Scholar
  73. Wei W et al (2018) A surface-display biohybrid approach to light-driven hydrogen production in air. Sci Adv 4:eaap9253.  https://doi.org/10.1126/sciadv.aap9253 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wenzel J, Fuentes L, Cabezas A (2017) Microbial fuel cell coupled to biohydrogen reactor: a feasible technology to increase energy yield from cheese whey. Bioprocess Biosyst Eng 40:807–819.  https://doi.org/10.1007/s00449-017-1746-6 CrossRefPubMedGoogle Scholar
  75. Wong YM et al (2018) Evaluating new bio-hydrogen producers: Clostridium perfringens strain JJC, Clostridium bifermentans strain WYM and Clostridium sp. strain Ade. TY. J Biosci Bioeng 125:590–598.  https://doi.org/10.1016/j.jbiosc.2017.12.012 CrossRefPubMedGoogle Scholar
  76. Wood BC et al (2017) Nanointerface-driven reversible hydrogen storage in the nanoconfined Li–N–H system. Adv Mater Interfaces 4:1600803.  https://doi.org/10.1002/admi.201600803 CrossRefGoogle Scholar
  77. Wu S, Li X, Yu J, Wang Q (2012) Increased hydrogen production in co-culture of Chlamydomonas reinhardtii and Bradyrhizobium japonicum. Bioresour Technol 123:184–188.  https://doi.org/10.1016/j.biortech.2012.07.055 CrossRefPubMedGoogle Scholar
  78. Wu S, Xu L, Huang R, Wang Q (2011) Improved biohydrogen production with an expression of codon-optimized hemH and lba genes in the chloroplast of Chlamydomonas reinhardtii. Bioresour Technol 102:2610–2616.  https://doi.org/10.1016/j.biortech.2010.09.123 CrossRefPubMedGoogle Scholar
  79. Zahnle KJ, Catling DC (2009) Our planet’s leaky atmosphere. Sci Am 300(5):35–43Google Scholar
  80. Zeng X, Borole AP, Pavlostathis SG (2015) Biotransformation of furanic and phenolic compounds with hydrogen gas production in a microbial electrolysis. Cell Environ Sci Technol 49:13667–13675.  https://doi.org/10.1021/acs.est.5b02313 CrossRefPubMedGoogle Scholar
  81. Zhang Y, Angelidaki I (2012) Innovative self-powered submersible microbial electrolysis cell (SMEC) for biohydrogen production from anaerobic reactors. Water Res 46:2727–2736.  https://doi.org/10.1016/j.watres.2012.02.038 CrossRefPubMedGoogle Scholar
  82. Zhang T, Jiang D, Zhang H, Jing Y, Tahir N, Zhang Y, Zhang Q (2019) Comparative study on bio-hydrogen production from corn stover: photo-fermentation, dark-fermentation and dark-photo co-fermentation. Int J Hydrog Energy.  https://doi.org/10.1016/j.ijhydene.2019.04.170 CrossRefGoogle Scholar
  83. Zhang J, Zhang Y, Quan X, Chen S, Afzal S (2013) Enhanced anaerobic digestion of organic contaminants containing diverse microbial population by combined microbial electrolysis cell (MEC) and anaerobic reactor under Fe(III) reducing conditions. Bioresour Technol 136:273–280.  https://doi.org/10.1016/j.biortech.2013.02.103 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Ganesh Mahidhara
    • 1
  • Hannah Burrow
    • 2
  • Ch. Sasikala
    • 3
  • Ch. V. Ramana
    • 1
    Email author
  1. 1.Department of Plant Sciences, School of Life SciencesUniversityof Hyderabad, P.O Central UniversityHyderabadIndia
  2. 2.Trility Water Pty Ltd, BWBMPConnewarreAustralia
  3. 3.Bacterial Discovery Laboratory, Centre for Environment, Institute of Science and TechnologyJ.N.T. University HyderabadHyderabadIndia

Personalised recommendations