Bioaugmentation with Enterococcus casseliflavus: A Hydrogen-Producing Strain Isolated from Citrus Peel Waste

Waste and Biomass Valorization volume 12, pages895–911(2021)Cite this article

Abstract

Purpose

To isolate, identify and characterize an anaerobic strain from in natura CPW, in relation to the consumption of different carbon sources, growth kinetics and H2 production after bioaugmentation.

Methods

Several substrates were evaluated (glucose, fructose, sucrose, xylose, starch, cellobiose, cellulose and lactose), and its optimal concentration was evaluated by Experimental Design method, besides the application of the isolated strain in citrus peel waste (CPW).

Results

A facultative anaerobic strain, similar (99%) to Enterococcus casseliflavus, was isolated from in natura citrus pulp and bagasse. Xylose was the monomer from which there was greater H2 production (10.3 mmol L−1). For 0.5 to 6.5 gxylose L−1, 3.0 to 12.9 mmol H2 L−1 was obtained, respectively. Generation time (Tg) of 0.35 h and specific growth (µ) of 1.98 h−1 for pH 7.0, 37 °C and 2 g glucose L−1 was obtained for E. casseliflavus. In bioaugmentation assays (CPW + E. casseliflavus), highest maximum H2 production potential (P = 13.9 mmol L−1), maximum H2 production rate (Rm = 1.09 mmol h−1) and time to start the H2 production (λ = 2.12 h−1) was observed when compared to glucose (P = 9.1 mmol L−1; Rm = 1.99 mmol h−1; λ = 4.08 h−1).

Conclusion

From glucose, there was prevalence of butyric acid pathway (759 mg L−1) in relation to acetic acid (303 mg L−1). From CPW, there was higher production of acetic acid (878 mg L−1) in relation to butyric (147 mg L−1). The application of E. casseliflavus by bioaugmentation is an alternative for biodigestion of complex substrates, such as CPW, to obtain products of biotechnological interest.

Graphic Abstract

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

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

References

  1. 1.

    Forster-Carneiro, T., Pérez, M., Romero, L.I.: Influence of total solid and inoculum contents on performance of anaerobic reactors treating food waste. Bioresour. Technol. 99, 6994–7002 (2008). https://doi.org/10.1016/j.biortech.2008.01.018

    Article  Google Scholar 

  2. 2.

    Leitão, R.C., Costa, A.G., Cassales, A.R., Alexandre, L.C., Pinheiro, F.G.C., Pinheiro, G.C., Viana, A.F., Santaella, S.T., Santos, A.B., de Rosa, M.F.: Biodegradabilidade Anaeróbia dos Resíduos Provenientes das Cadeias Produtivas dos Biocombustíveis: Bagaço de Cana-de-açúcar. Embrapa Agroindústria Trop. 1, 41 (2013)

    Google Scholar 

  3. 3.

    Forgács, G., Pourbafrani, M., Niklasson, C., Taherzadeh, M.J., Hováth, I.S.: Methane production from citrus wastes: process development and cost estimation. J. Chem. Technol. Biotechnol. 87, 250–255 (2012). https://doi.org/10.1002/jctb.2707

    Article  Google Scholar 

  4. 4.

    Calabrò, P.S., Pontoni, L., Porqueddu, I., Greco, R., Pirozzi, F., Malpei, F.: Effect of the concentration of essential oil on orange peel waste biomethanization: preliminary batch results. Waste Manag. 48, 440–447 (2016). https://doi.org/10.1016/j.wasman.2015.10.032

    Article  Google Scholar 

  5. 5.

    Su, H., Tan, F., Xu, Y.: Enhancement of biogas and methanization of citrus waste via biodegradation pretreatment and subsequent optimized fermentation. Fuel 181, 843–851 (2016). https://doi.org/10.1016/j.fuel.2016.05.055

    Article  Google Scholar 

  6. 6.

    Ruiz, B., Flotats, X.: Effect of limonene on batch anaerobic digestion of citrus peel waste. Biochem. Eng. J. 109, 9–18 (2016). https://doi.org/10.1016/j.bej.2015.12.011

    Article  Google Scholar 

  7. 7.

    Ruiz, B., Flotats, X.: Citrus essential oils and their influence on the anaerobic digestion process: an overview. Waste Manag. 34, 2063–2079 (2014). https://doi.org/10.1016/j.wasman.2014.06.026

    Article  Google Scholar 

  8. 8.

    López, J.Á.S., Li, Q., Thompson, I.P.: Biorefinery of waste orange peel. Crit. Rev. Biotechnol. 30, 63–69 (2010). https://doi.org/10.3109/07388550903425201

    Article  Google Scholar 

  9. 9.

    Li, Q., Siles, J.A., Thompson, I.P.: Succinic acid production from orange peel and wheat straw by batch fermentations of Fibrobacter succinogenes S85. Appl. Microbiol. Biotechnol. 88, 671–678 (2010). https://doi.org/10.1007/s00253-010-2726-9

    Article  Google Scholar 

  10. 10.

    Maintinguer, S.I., Lazaro, C.Z., Pachiega, R., Varesche, M.B.A., Sequinel, R., de Oliveira, J.E.: Hydrogen bioproduction with Enterobacter sp isolated from brewery wastewater. Int. J. Hydrogen Energy. 42, 152–160 (2017). https://doi.org/10.1016/j.ijhydene.2016.11.104

    Article  Google Scholar 

  11. 11.

    Kumar, G., Bakonyi, P., Kobayashi, T., Xu, K.Q., Sivagurunathan, P., Kim, S.H., Buitrón, G., Nemestóthy, N., Bélafi-Bakó, K.: Enhancement of biofuel production via microbial augmentation: the case of dark fermentative hydrogen. Renew. Sustain. Energy Rev. 57, 879–891 (2016). https://doi.org/10.1016/j.rser.2015.12.107

    Article  Google Scholar 

  12. 12.

    Ecem Öner, B., Akyol, Ç., Bozan, M., Ince, O., Aydin, S., Ince, B.: Bioaugmentation with Clostridium thermocellum to enhance the anaerobic biodegradation of lignocellulosic agricultural residues. Bioresour. Technol. 249, 620–625 (2018). https://doi.org/10.1016/j.biortech.2017.10.040

    Article  Google Scholar 

  13. 13.

    Valdez-vazquez, I., Castillo-rubio, L.G., Pérez-rangel, M., Sepúlveda-gálvez, A., Vargas, A.: Enhanced hydrogen production from lignocellulosic substrates via bioaugmentation with Clostridium strains. Ind. Crop. Prod. 137, 105–111 (2019). https://doi.org/10.1016/j.indcrop.2019.05.023

    Article  Google Scholar 

  14. 14.

    Lin, C., Lay, C., Sung, I., Sen, B., Chen, C., Al, L.I.N.E.T., Ioeng, J.B.I.B.: Anaerobic hydrogen production from unhydrolyzed mushroom farm waste by indigenous microbiota. J. Biosci. Bioeng. 124, 425–429 (2017). https://doi.org/10.1016/j.jbiosc.2017.05.001

    Article  Google Scholar 

  15. 15.

    Rabelo, C.A.B.S., Soares, L.A., Sakamoto, I.K., Varesche, M.B.A.: Bioconversion of cellulose into hydrogen, biogas and organic acids using microbial consortium from pulp and paper mill wastewater treatment plant. Quim. Nova. 41, 169–175 (2018)

    Google Scholar 

  16. 16.

    Ács, N., Bagi, Z., Rákhely, G., Minárovics, J., Nagy, K., Kovács, K.L.: Bioaugmentation of biogas production by a hydrogen-producing bacterium. Bioresour. Technol. 186, 286–293 (2015). https://doi.org/10.1016/j.biortech.2015.02.098

    Article  Google Scholar 

  17. 17.

    Hawkes, F.R., Dinsdale, R., Hawkes, D.L., Hussy, I.: Sustainable fermentative hydrogen production: challenges for process optimisation. Int. J. Hydrogen Energy. 27, 1339–1347 (2002). https://doi.org/10.1016/S0360-3199(02)00090-3

    Article  Google Scholar 

  18. 18.

    John, U.V., Carvalho, J.: Enterococcus: Review of its physiology, pathogenesis, diseases and the challenges it poses for clinical microbiology. Front. Biol. 6, 357–366 (2011). https://doi.org/10.1007/s11515-011-1167-x

    Article  Google Scholar 

  19. 19.

    Mubarak, Z., Soraya, C.: The acid tolerance response and pH adaptation of Enterococcus faecalis in extract of lime Citrus aurantiifolia from Aceh Indonesia. F1000Research 7, 287 (2018)

    Article  Google Scholar 

  20. 20.

    Huycke, M.M.: Physiology of Enterococci. In: Al, M.S.G., et al. (eds.) The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resist, pp. 133–175. ASM Press, Washington (2002)

    Google Scholar 

  21. 21.

    Cibis, K.G., Gneipel, A., König, H.: Isolation of acetic, propionic and butyric acid-forming bacteria from biogas plants. J. Biotechnol. 220, 51–63 (2016)

    Article  Google Scholar 

  22. 22.

    Yun, J.S., Wee, Y.J., Ryu, H.W.: Production of optically pure L(+)-lactic acid from various carbohydrates by batch fermentation of Enterococcus faecalis RKY1. Enzyme Microb. Technol. 33, 416–423 (2003). https://doi.org/10.1016/S0141-0229(03)00139-X

    Article  Google Scholar 

  23. 23.

    Choi, I.S., Lee, Y.G., Khanal, S.K., Park, B.J., Bae, H.J.: A low-energy, cost-effective approach to fruit and citrus peel waste processing for bioethanol production. Appl. Energy. 140, 65–74 (2015). https://doi.org/10.1016/j.apenergy.2014.11.070

    Article  Google Scholar 

  24. 24.

    Łukajtis, R., Hołowacz, I., Kucharska, K., Glinka, M., Rybarczyk, P., Przyjazny, A., Kamiński, M.: Hydrogen production from biomass using dark fermentation. Renew. Sustain. Energy Rev. 91, 665–694 (2018). https://doi.org/10.1016/j.rser.2018.04.043

    Article  Google Scholar 

  25. 25.

    Nation, J.L.: A new method using hexamethyldisilazane for preparation of soft insect tissues for scanning electron microscopy. Stain Technol. 58, 347–351 (1983)

    Article  Google Scholar 

  26. 26.

    Camargo, F.P., Sakamoto, I.K., Duarte, I.C.S., Varesche, M.B.A.: Influence of alkaline peroxide assisted and hydrothermal pretreatment on biodegradability and bio-hydrogen formation from citrus peel waste. Int. J. Hydrogen Energy. (2019). https://doi.org/10.1016/j.ijhydene.2019.07.011

    Article  Google Scholar 

  27. 27.

    Haruta, S., Cui, Z., Huang, Z., Li, M., Ishii, M., Igarashi, Y.: Construction of a stable microbial community with high cellulose-degradation ability. Appl. Microbiol. Biotechnol. 59, 529–534 (2002). https://doi.org/10.1007/s00253-002-1026-4

    Article  Google Scholar 

  28. 28.

    Wang, W., Yan, L., Cui, Z., Gao, Y., Wang, Y., Jing, R.: Characterization of a microbial consortium capable of degrading lignocellulose. Bioresour. Technol. 102, 9321–9324 (2011). https://doi.org/10.1016/j.biortech.2011.07.065

    Article  Google Scholar 

  29. 29.

    Green, M.R., Sambrook, J.: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York (2012)

    Google Scholar 

  30. 30.

    Weisburg, W.G., Barns, S.M., Pelletier, D.A., Lane, D.J.: 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173, 697–703 (1991)

    Article  Google Scholar 

  31. 31.

    Rodrigues, M.I., Iemma, A.F.: Planejamento de Experimentos e Otimização de Processos. Casa do Espírito Amigo Fraternidade Fé e Amor, Campinas (2014)

    Google Scholar 

  32. 32.

    APHA, AWWA, WEF: Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC (2012)

    Google Scholar 

  33. 33.

    Blundi, C., Gardêlha, R.: Método para determinação de matéria orgânica específica em águas residuárias. In: Chernicharo, C.A.L. (ed.) Pós tratamento de efluentes de reatores anaeróbios: aspectos metodológicos, pp. 9–17. Universidade Federal de Minas Gerais, Belo Horizonte (2001)

    Google Scholar 

  34. 34.

    Dubois, M., Gilles, K., Hamilton, J., Rebers, P., Smith, F.: Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356 (1956). https://doi.org/10.1021/ac60111a017

    Article  Google Scholar 

  35. 35.

    Buchanan, I.D., Nicell, J.A.: Model development for horseradish peroxidase catalyzed removal of aqueous phenol. Biotechnol. Bioeng. 54, 251–261 (1997). https://doi.org/10.1002/(SICI)1097-0290(19970505)54:3%3c251:AID-BIT6%3e3.0.CO;2-E

    Article  Google Scholar 

  36. 36.

    Taylor, K.A.C.: A simple colorimetric assay for muramic acid and lactic acid. Appl. Biochem. Biotechnol. 56, 49–58 (1996). https://doi.org/10.1007/BF02787869

    Article  Google Scholar 

  37. 37.

    Adorno, M.A.T., Hirasawa, J.S., Varesche, M.B.A.: Development and Validation Of Two Methods To Quantify Volatile Acids (C2–C6) by GC/FID: headspace (automatic and manual) and liquid-liquid extraction (LLE). Am. J. Anal. Chem. 05, 406–414 (2014). https://doi.org/10.4236/ajac.2014.57049

    Article  Google Scholar 

  38. 38.

    Zwietering, M.H., De Wit, J.C., Cuppers, H.G.A.M., Van’t-Riet, K.: Modeling of bacterial growth with shifts in temperature. Appl. Environ. Microbiol. 60, 204–213 (1994)

    Article  Google Scholar 

  39. 39.

    Hammer, R., Harper, D., Ryan, P.: Past paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9 (2001)

    Google Scholar 

  40. 40.

    De-Vos, P., Garrity, G.M., Jones, D., Krieg, N.R., Ludwig, W., Rainey, F.A., Whitman, R., Schleifer, K.-H., Whitman, W.B. (2009) The firmicutes. In: Whitman, W.B. (ed.) Bergey’s Manual of Systematic Bacteriology, p. 1450. Springer, Athens

  41. 41.

    Li, D., Jiao, C., He, W., Yan, Z., Yuan, Y., Li, Z., Guo, Y., Liu, X.: Comparison of micro-aerobic and anaerobic fermentative hydrogen production from corn straw. Int. J. Hydrogen Energy. 41, 5456–5464 (2016). https://doi.org/10.1016/j.ijhydene.2016.01.141

    Article  Google Scholar 

  42. 42.

    Wang, A., Gao, L., Ren, N., Xu, J., Liu, C.: Bio-hydrogen production from cellulose by sequential co-culture of cellulosic hydrogen bacteria of Enterococcus gallinarum G1 and Ethanoigenens harbinense B49. Biotechnol. Lett. 31, 1321–1326 (2009). https://doi.org/10.1007/s10529-009-0028-z

    Article  Google Scholar 

  43. 43.

    Herdian, H., Istiqomah, L., Damayanti, E., Suryani, A.E., Anggraeni, A.S., Rosyada, N., Susilowati, A.: Isolation of cellulolytic lactic-acid bacteria from mentok (Anas moschata) gastro-intestinal tract. Trop. Anim. Sci. J. 41, 200–206 (2018). https://doi.org/10.5398/tasj.2018.41.3.200

    Article  Google Scholar 

  44. 44.

    Parente, E., Brienza, C., Ricciardi, A., Addario, G.: Growth and bacteriocin production by Enterococcus faecium DPC1146 in batch and continuous culture. J. Ind. Microbiol. Biotechnol. 18, 62–67 (1997)

    Article  Google Scholar 

  45. 45.

    Orandi, S.M., Rasca, M.B., Lfieri, P.A., Odi, R.L., Amburini, A.T.: Original article Influence of pH and temperature on the growth of Enterococcus faecium and Enterococcus faecalis. Le Lait 85, 181–192 (2005). https://doi.org/10.1051/lait

    Article  Google Scholar 

  46. 46.

    Martínez, S., López, M., Bernardo, A.: Thermal inactivation of Enterococcus faecium: effect of growth temperature and physiological state of microbial cells. Lett. Appl. Microbiol. 37, 475–481 (2003). https://doi.org/10.1046/j.1472-765X.2003.01431.x

    Article  Google Scholar 

  47. 47.

    Zheng, Y., Zhao, J., Xu, F., Li, Y.: Pretreatment of lignocellulosic biomass for enhanced biogas production. Prog. Energy Combust. Sci. 42, 35–53 (2014). https://doi.org/10.1016/j.pecs.2014.01.001

    Article  Google Scholar 

  48. 48.

    Da-Mazareli, R.C.S., Sakamoto, I.K., Silva, E.L., Varesche, M.B.A.: Bacillus sp isolated from banana waste and analysis of metabolic pathways in acidogenic systems in hydrogen production. J. Environ. Manag. 247, 178–186 (2019). https://doi.org/10.1016/j.jenvman.2019.06.040

    Article  Google Scholar 

  49. 49.

    An, D., Li, Q., Wang, X., Yang, H., Guo, L.: Characterization on hydrogen production performance of a newly isolated Clostridium beijerinckii YA001 using xylose. Int. J. Hydrogen Energy. 39, 19928–19936 (2014). https://doi.org/10.1016/j.ijhydene.2014.10.014

    Article  Google Scholar 

  50. 50.

    Choi, I.S., Kim, J.H., Wi, S.G., Kim, K.H., Bae, H.J.: Bioethanol production from mandarin (Citrus unshiu) peel waste using popping pretreatment. Appl. Energy 102, 204–210 (2013). https://doi.org/10.1016/j.apenergy.2012.03.066

    Article  Google Scholar 

  51. 51.

    Wilkins, M.R., Widmer, W.W., Grohmann, K., Cameron, R.G.: Hydrolysis of grapefruit peel waste with cellulase and pectinase enzymes. Bioresour. Technol. 98, 1596–1601 (2007). https://doi.org/10.1016/j.biortech.2006.06.022

    Article  Google Scholar 

  52. 52.

    Mäkinen, A.E., Nissilä, M.E., Puhakka, J.A.: Dark fermentative hydrogen production from xylose by a hot spring enrichment culture. Int. J. Hydrogen Energy 37, 12234–12240 (2012). https://doi.org/10.1016/j.ijhydene.2012.05.158

    Article  Google Scholar 

  53. 53.

    Yin, Y., Wang, J.: Characterization and hydrogen production performance of a novel strain Enterococcus faecium INET2 isolated from gamma irradiated sludge. Int. J. Hydrogen Energy 41, 22793–22801 (2016). https://doi.org/10.1016/j.ijhydene.2016.10.059

    Article  Google Scholar 

  54. 54.

    Tapia-Venegas, E., Ramirez, J.E., Donoso-Bravo, A., Jorquera, L., Steyer, J.P., Ruiz-Filippi, G.: Bio-hydrogen production during acidogenic fermentation in a multistage stirred tank reactor. Int. J. Hydrogen Energy 38, 2185–2190 (2013). https://doi.org/10.1016/j.ijhydene.2012.11.077

    Article  Google Scholar 

  55. 55.

    Palomo-Briones, R., Celis, L.B., Méndez-Acosta, H.O., Bernet, N., Trably, E., Razo-Flores, E.: Enhancement of mass transfer conditions to increase the productivity and efficiency of dark fermentation in continuous reactors. Fuel 254, 115648 (2019). https://doi.org/10.1016/j.fuel.2019.115648

    Article  Google Scholar 

  56. 56.

    Bakonyi, P., Buitrón, G., Valdez-Vazquez, I., Nemestóthy, N., Bélafi- Bakó, K.: A novel gas separation integrated membrane bioreactor to evaluate the impact of self-generated biogas recycling on continuous hydrogen fermentation. Appl. Energy 190, 813–823 (2017). https://doi.org/10.1016/j.apenergy.2016.12.151

    Article  Google Scholar 

  57. 57.

    Ghimire, A., Frunzo, L., Pirozzi, F., Trably, E., Escudie, R., Lens, P.N.L., Esposito, G.: A review on dark fermentative biohydrogen production from organic biomass: process parameters and use of by-products. Appl. Energy 144, 73–95 (2015). https://doi.org/10.1016/j.apenergy.2015.01.045

    Article  Google Scholar 

  58. 58.

    Li, C., Fang, H.H.P.: Fermentative hydrogen production from wastewater and solid wastes by mixed cultures. Crit. Rev. Environ. Sci. Technol. 37, 1–39 (2007). https://doi.org/10.1080/10643380600729071

    MathSciNet  Article  Google Scholar 

  59. 59.

    Sinha, P., Pandey, A.: Biohydrogen production from various feedstocks by Bacillus firmus NMBL-03. Int. J. Hydrogen Energy 39, 7518–7525 (2014). https://doi.org/10.1016/j.ijhydene.2013.08.134

    Article  Google Scholar 

  60. 60.

    Infantes, D., del Campo, A.G., Villaseñor, J., Fernández, F.J.: Influence of pH, temperature and volatile fatty acids on hydrogen production by acidogenic fermentation. Int. J. Hydrogen Energy 6, 15595–15601 (2011). https://doi.org/10.1016/j.ijhydene.2011.09.061

    Article  Google Scholar 

  61. 61.

    Ahmad, F., Silva, E.L., Varesche, M.B.A.: Hydrothermal processing of biomass for anaerobic digestion—a review. Renew. Sustain. Energy Rev. 98, 108–124 (2018). https://doi.org/10.1016/j.rser.2018.09.008

    Article  Google Scholar 

  62. 62.

    Rosa, P.R.F., Silva, E.L.: Review of Continuous Fermentative Hydrogen- Producing Bioreactors from Complex Wastewater. Front. Bioenergy Biofuels Hydrog. (2017). https://doi.org/10.5772/65548

    Article  Google Scholar 

  63. 63.

    Fonseca, B.C., Schmidell, W., Reginatto, V.: Impact of glucose concentration on productivity and yield of hydrogen production by the new isolate Clostridium beijerinckii Br 21. Can. J. Chem. Eng. 9999, 1–8 (2018). https://doi.org/10.1002/cjce.23327

    Article  Google Scholar 

  64. 64.

    Valdez-Vazquez, I., Pérez-Rangel, M., Tapia, A., Buitrón, G., Molina, C., Hernández, G., Amaya-Delgado, L.: Hydrogen and butanol production from native wheat straw by synthetic microbial consortia integrated by species of Enterococcus and Clostridium. Fuel 159, 214–222 (2015). https://doi.org/10.1016/j.fuel.2015.06.052

    Article  Google Scholar 

  65. 65.

    Braga, J.K., Abreu, A.A., Motteran, F., Pereira, M.A., Alves, M.M., Varesche, M.B.A.: Hydrogen production by clostridium cellulolyticum a cellulolytic and hydrogen-producing bacteria using sugarcane bagasse. Waste Biomass Valoriz. 1–11 (2017). https://doi.org/10.1007/s12649-017-0105-9

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the technical support of Dr. Maria Angela Adorno and Dr. Carolina Sabatini. This work was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (processes 2017/01722-0 and 2015/06246-7) and was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Affiliations

  1. Department of Hydraulics and Sanitation, School of Engineering of São Carlos, University of São Paulo, Av. Trabalhador São Carlense, 400, São Carlos, SP, 13566-590, Brazil

    Franciele Pereira Camargo, Isabel Kimiko Sakamoto & Maria Bernadete Amâncio Varesche

  2. Department of Chemical Engineering, Federal University of São Carlos, Rod Washington Luiz, Km 235, SP 310, São Carlos, SP, 13565-905, Brazil

    Edson Luiz Silva

  3. Department of Biology, Federal University of São Carlos - UFSCar, João Leme Dos Santos Highway, Km 101, Sorocaba, São Paulo, 18052-780, Brazil

    Iolanda Cristina Silveira Duarte

Authors
  1. Franciele Pereira Camargo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabel Kimiko Sakamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edson Luiz Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Iolanda Cristina Silveira Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Bernadete Amâncio Varesche
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Bernadete Amâncio Varesche.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Camargo, F.P., Sakamoto, I.K., Silva, E.L. et al. Bioaugmentation with Enterococcus casseliflavus: A Hydrogen-Producing Strain Isolated from Citrus Peel Waste. Waste Biomass Valor 12, 895–911 (2021). https://doi.org/10.1007/s12649-020-01049-7

Download citation

Keywords

  • Lignocellulosic biomass
  • Autochthonous consortia
  • Agro-industrial waste
  • Nutritional evaluation