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Effect of volatile fatty acids mixtures on the simultaneous photofermentative production of hydrogen and polyhydroxybutyrate

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Abstract

Purple non-sulfur bacteria generate hydrogen and polyhydroxybutyrate (PHB) as a mechanism for disposing of reducing equivalents generated during substrate consumption. However, both pathways compete for the reducing equivalents released from bacteria growing under certain substrates, thus the formation of hydrogen or PHB is detrimental to the formation of each other. The effect of mixtures of acetic, propionic and butyric acids on the formation of H2 and PHB was evaluated using Box–Behnken design. A bacterial community mainly constituted by Rhodopseudomonas palustris was used as inoculum. It was observed that the three volatile fatty acids had a significant effect on the specific PHB production. However, only the propionic acid had a significant effect on the specific H2 production activity and the highest value was observed when acetate was the main component in the mixture. The maximum values for the specific PHB and hydrogen production rates were 16.4 mg-PHB/g-TSS/day and 391 mL-H2/g-TSS/day, respectively.

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References

  1. Steinbüchel A (1992) Biodegradable plastics. Curr Opin Biotechnol 3:291–297. doi:10.1016/0958-1669(92)90107-T

    Article  Google Scholar 

  2. Kumar G, Bakonyi P, Periyasamy S et al (2015) Lignocellulose biohydrogen: practical challenges and recent progress. Renew Sustain Energy Rev 44:728–737. doi:10.1016/j.rser.2015.01.042

    Article  CAS  Google Scholar 

  3. Kumar G, Bakonyi P, Kobayashi T et al (2016) Enhancement of biofuel production via microbial augmentation: the case of dark fermentative hydrogen. Renew Sustain Energy Rev 57:879–891. doi:10.1016/j.rser.2015.12.107

    Article  CAS  Google Scholar 

  4. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Harwood CS (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22:55–61. doi:10.1038/nbt923

    Article  CAS  Google Scholar 

  5. Sasikala K, Ramana CV, Raghuveer Rao P, Kovacs KL (1993) Anoxygenic phototrophic bacteria: physiology and advances in hydrogen production technology. Adv Appl Microbiol 38:211–295. doi:10.1016/S0065-2164(08)70217-X

    Article  CAS  Google Scholar 

  6. Reddy CSK, Ghai R, Rashmi Kalia VC (2003) Polyhydroxyalkanoates: an overview. Bioresour Technol 87:137–146. doi:10.1016/S0960-8524(02)00212-2

    Article  CAS  Google Scholar 

  7. Hustede E, Steinbüchel A, Schlegel HG (1993) Relationship between the photoproduction of hydrogen and the accumulation of PHB in non-sulphur purple bacteria. Appl Microbiol Biotechnol 39:87–93. doi:10.1007/BF00166854

    Article  CAS  Google Scholar 

  8. 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 

  9. Chen YT, Wu SC, Lee CM (2012) Relationship between cell growth, hydrogen production and poly-β-hydroxybutyrate (PHB) accumulation by Rhodopseudomonas palustris WP3-5. Int J Hydrog Energy 37:13887–13894. doi:10.1016/j.ijhydene.2012.06.024

    Article  CAS  Google Scholar 

  10. Wu SC, Liou SZ, Lee CM (2012) Correlation between bio-hydrogen production and polyhydroxybutyrate (PHB) synthesis by Rhodopseudomonas palustris WP3-5. Bioresour Technol 113:44–50. doi:10.1016/j.biortech.2012.01.090

    Article  CAS  Google Scholar 

  11. Cardeña R, Moreno G, Valdez-Vazquez I, Buitrón G (2015) Optimization of volatile fatty acids concentration for photofermentative hydrogen production by a consortium. Int J Hydrog Energy 40:17212–17223. doi:10.1016/j.ijhydene.2015.10.020

    Article  Google Scholar 

  12. Li RY, Zhang T, Fang HHP (2008) Characteristics of a phototrophic sludge producing hydrogen from acetate and butyrate. Int J Hydrog Energy 33:2147–2155. doi:10.1016/j.ijhydene.2008.02.055

    Article  CAS  Google Scholar 

  13. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125. doi:10.1186/1471-2180-8-125

    Article  Google Scholar 

  14. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461

    Article  CAS  Google Scholar 

  15. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381

    Article  CAS  Google Scholar 

  16. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. doi:10.1038/nmeth.2604

    Article  CAS  Google Scholar 

  17. Ren N, Li J, Li B, Wang Y, Liu S (2006) Biohydrogen production from molasses by anaerobic fermentation with a pilot-scale bioreactor system. Int J Hydrog Energ 31:2147–2157. doi:10.1016/j.ijhydene.2006.02.011

    Article  CAS  Google Scholar 

  18. Shi X-Y, Yu H-Q (2004) Hydrogen production from propionate by Rhodopseudomonas capsulata. Appl Biochem Biotechnol 117:143–154. doi:10.1385/ABAB:117:3:143

    Article  CAS  Google Scholar 

  19. 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. Int J Hydrog Energ 32:200–206. doi:10.1016/j.ijhydene.2006.06.034

    Article  CAS  Google Scholar 

  20. De Amorim ELC, Sader LT, Silva EL (2012) Effect of substrate concentration on dark fermentation hydrogen production using an anaerobic fluidized bed reactor. Appl Biochem Biotechnol 166:1248–1263. doi:10.1007/s12010-011-9511-9

    Article  CAS  Google Scholar 

  21. Montgomery DC (2008) Design and analysis of experiments. Wiley, Oxford

    Google Scholar 

  22. Apha (2005) Standard Methods for the Examination of Water and Wastewater, American Water Works Association/American Public Works Association/Water Environment Federation

  23. Braunegg G, Sonnleitner B, Lafferty RM (1978) A rapid gas chromatographic method for the determination of poly-β-hydroxybutyric acid in microbial biomass. Eur J Appl Microbiol 6:29–37. doi:10.1007/BF00500854

    Article  CAS  Google Scholar 

  24. Mu Y, Yang HY, Wang YZ, He CS, Zhao QB, Wang Y, Yu HQ (2014) The maximum specific hydrogen-producing activity of anaerobic mixed cultures: definition and determination. Sci Rep. doi:10.1038/srep05239

    Google Scholar 

  25. Adessi A, Torzillo G, Baccetti E, De Philippis R (2012) Sustained outdoor H2 production with Rhodopseudomonas palustris cultures in a 50 L tubular photobioreactor. Int J Hydrog Energy 37:8840–8849. doi:10.1016/j.ijhydene.2012.01.081

    Article  CAS  Google Scholar 

  26. Chen CY, Lu WB, Wu JF, Chang JS (2007) Enhancing phototrophic hydrogen production of Rhodopseudomonas palustris via statistical experimental design. Int J Hydrog Energy 32:940–949. doi:10.1016/j.ijhydene.2006.09.021

    Article  CAS  Google Scholar 

  27. Jamil Z, Mohamad Annuar MS, Ibrahim S, Vikineswary S (2009) Optimization of phototrophic hydrogen production by Rhodopseudomonas palustris PBUM001 via statistical experimental design. Int J Hydrog Energy 34:7502–7512. doi:10.1016/j.ijhydene.2009.05.116

    Article  CAS  Google Scholar 

  28. Lazaro CZ, Vich DV, Hirasawa JS, Varesche MBA (2012) Hydrogen production and consumption of organic acids by a phototrophic microbial consortium. Int J Hydrog Energy 37:11691–11700. doi:10.1016/j.ijhydene.2012.05.088

    Article  CAS  Google Scholar 

  29. Tawfik A, El-Bery H, Kumari S, Bux F (2014) Use of mixed culture bacteria for photofermentive hydrogen of dark fermentation effluent. Bioresour Technol 168:119–126. doi:10.1016/j.biortech.2014.03.065

    Article  CAS  Google Scholar 

  30. Fradinho JC, Domingos JMB, Carvalho G, Oehmen A, Reis MAM (2013) Polyhydroxyalkanoates production by a mixed photosynthetic consortium of bacteria and algae. Bioresour Technol 132:146–153. doi:10.1016/j.biortech.2013.01.050

    Article  CAS  Google Scholar 

  31. Fradinho JC, Oehmen A, Reis MAM (2014) Photosynthetic mixed culture polyhydroxyalkanoate (PHA) production from individual and mixed volatile fatty acids (VFAs): substrate preferences and co-substrate uptake. J Biotechnol 185:19–27. doi:10.1016/j.jbiotec.2014.05.035

    Article  CAS  Google Scholar 

  32. Lawson PA, Falsen E, Inganäs E, Weyant RS, Collins MD (2002) Dysgonomonas mossii sp. nov., from human sources. Syst Appl Microbiol 25:194–197. doi:10.1078/0723-2020-00107

    Article  CAS  Google Scholar 

  33. Venkateswar Reddy M, Venkata Mohan S (2012) Influence of aerobic and anoxic microenvironments on polyhydroxyalkanoates (PHA) production from food waste and acidogenic effluents using aerobic consortia. Bioresour Technol 103:313–321. doi:10.1016/j.biortech.2011.09.040

    Article  CAS  Google Scholar 

  34. Chen S, Dong X (2005) Proteiniphilum acetatigenes gen. nov., sp. nov., from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol 55:2257–2261. doi:10.1099/ijs.0.63807-0

    Article  CAS  Google Scholar 

  35. Zeppilli M, Villano M, Aulenta F, Lampis S, Vallini G, Majone M (2015) Effect of the anode feeding composition on the performance of a continuous-flow methane-producing microbial electrolysis cell. Environ Sci Pollut Res 22:7349–7360. doi:10.1007/s11356-014-3158-3

    Article  CAS  Google Scholar 

  36. Yang X, Wen L, Liu X, Chen S, Wang Y, Wan C (2015) Bio-augmentative volatile fatty acid production from waste activated sludge hydrolyzed at pH 12. RSC Adv 5:50033–50039. doi:10.1039/c5ra04651c

    Article  CAS  Google Scholar 

  37. Jurtshuk P (1996) Bacterial metabolism. In Baron S (ed) Medical microbiology (4th edition). University of Texas Medical Branch at Galveston. http://www.ncbi.nlm.nih.gov/books/NBK7919/

  38. Huijberts GNM, De Rijk TC, De Waard P, Eggink G (1994) 13C nuclear magnetic resonance studies of Pseudomonas putida fatty acid metabolic routes involved in poly(3-hydroxyalkanoate) synthesis. J Bacteriol 176:1661–1666

    Article  CAS  Google Scholar 

  39. Ghimire A, Valentino S, Frunzo L, Pirozzi F, Lens PN, Esposito G (2016) Concomitant biohydrogen and poly-β-hydroxybutyrate production from dark fermentation effluents by adapted Rhodobacter sphaeroides and mixed photofermentative cultures. Bioresour Technol 217:157–164. doi:10.1016/j.biortech.2016.03.017

    Article  CAS  Google Scholar 

  40. Guevara-López E, Buitrón G (2015) Evaluation of different support materials used with a photo-fermentative consortium for hydrogen production. Int J Hydrog Energy 40:17231–17238. doi:10.1016/j.ijhydene.2015.08.057

    Article  Google Scholar 

  41. Goepfert JM, Hicks R (1969) Effect of volatile fatty acids on Salmonella typhimurium. J Bacteriol 97:956–958

    CAS  Google Scholar 

  42. Yang Y, Zhang N, Ji SQ, Lan X, Shen YL, Li FL, Ni JF (2014) Dysgonomonas macrotermitis sp. nov., isolated from the hindgut of a fungus-growing termite. Int J Syst Evol Microbiol 64:2956–2961. doi:10.1099/ijs.0.061739-0

    Article  CAS  Google Scholar 

  43. Mukhopadhyay M, Patra A, Paul AK (2005) Production of poly(3-hydroxybutyrate) and poly(3-hydroxybutyrate-co-3- hydroxyvalerate) by Rhodopseudomonas palustris SP5212. World J Microbiol Biotechnol 21:765–769. doi:10.1007/s11274-004-5565-y

    Article  CAS  Google Scholar 

  44. Carlozzi P, Pushparaj B, Degl’Innocenti A, Capperucci A (2006) Growth characteristics of Rhodopseudomonas palustris cultured outdoors, in an underwater tubular photobioreactor, and investigation on photosynthetic efficiency. Appl Microbiol Biotechnol 73:789–795. doi:10.1007/s00253-006-0550-z

    Article  CAS  Google Scholar 

  45. McKinlay JB, Oda Y, Rühl M, Posto AL, Sauer U, Harwood CS (2014) Non-growing Rhodopseudomonas palustris increases the hydrogen gas yield from acetate by shifting from the glyoxylate shunt to the tricarboxylic acid cycle. J Biol Chem 289:1960–1970. doi:10.1074/jbc.M113.527515

    Article  CAS  Google Scholar 

  46. Corneli E, Adessi A, Dragoni F, Ragaglini G, Bonari E, De Philippis R (2016) Agroindustrial residues and energy crops for the production of hydrogen and poly-β-hydroxybutyrate via photofermentation. Bioresour Technol 216:941–947. doi:10.1016/j.biortech.2016.06.046

    Article  CAS  Google Scholar 

  47. Khatipov E, Miyake M, Miyake J, Asada Y (1998) Accumulation of poly-β-hydroxybutyrate by Rhodobacter sphaeroides on various carbon and nitrogen substrates. FEMS Microbiol Lett 162:39–45. doi:10.1016/S0378-1097(98)00099-8

    CAS  Google Scholar 

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Acknowledgments

This research was supported through CONACYT (251718) and DGAPA-UNAM (IA102015) projects. The authors are grateful to Gloria Moreno and Jaime Perez for the technical support and fruitful discussions.

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Authors and Affiliations

  1. Laboratory for Research on Advanced Processes for Water Treatment, Instituto de Ingeniería, Unidad Académica Juriquilla, Universidad Nacional Autónoma de México, Blvd. Juriquilla 3001, 76230, Querétaro, QRO, Mexico

    René Cardeña, Idania Valdez-Vazquez & Germán Buitrón

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  1. René Cardeña
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  2. Idania Valdez-Vazquez
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Correspondence to Germán Buitrón.

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Cardeña, R., Valdez-Vazquez, I. & Buitrón, G. Effect of volatile fatty acids mixtures on the simultaneous photofermentative production of hydrogen and polyhydroxybutyrate. Bioprocess Biosyst Eng 40, 231–239 (2017). https://doi.org/10.1007/s00449-016-1691-9

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