Biogas production: evaluation of the influence of K2FeO4 pretreatment of maple leaves (Acer platanoides) on microbial consortia composition

  • Matej Planý
  • Marianna Czolderová
  • Lucia Kraková
  • Andrea Puškárová
  • Mária Bučková
  • Katarína Šoltys
  • Jaroslav Budiš
  • Tomáš Szemes
  • Tomáš Mackulak
  • Jer-Horng Wu
  • Domenico PangalloEmail author
Research Paper


The potential of K2FeO4 as a pretreatment agent of a lignocellulosic material was examined on leaves of Acer platanodides as the sole substrate for biogas production by anaerobic digestion carried out through modelling laboratory-scaled semi-continuous reactors differing in loading rates and substrate (pretreated and untreated leaves). The quality of bioagas produced by K2FeO4-pretreated leaves was significantly better in terms of higher methane content and lower content of H2S. K2FeO4 had no crucial influence on growth inhibition of biogas-producing bacteria, which were analysed by comprehensive culture-independent methods utilising high-throughput sequencing of specific genes [bacterial and archaeal 16S rRNA, formyltetrahydrofolate synthetase gene (fhs), methyl-coenzyme M reductase α subunit gene (mcrA) and fungal internal transcribed spacers (ITS)]. The higher amount of CH4 in biogas utilising pretreated leaves as substrate could be caused by a shift to acetoclastic methanogenesis pathway, which was indicated by the higher amount of homoacetogenic bacteria and acetotrophic methanogens detected in those reactors.


Biogas production Leaves Anaerobic digestion Microbial communities High-throughput sequencing 



This study was mainly financed by SAS-MOST Joint Research Cooperation (Bilateral project Slovakia–Taiwan) under Grant nos. MOST 104-2923-E-006-001-MY3 and SAS-MOST JRP 2014/3. This work was also supported by other projects of the Slovak Research Agencies under the contracts no. APVV-16-0124, APVV-16-0171, VEGA 1/0543/15 and VEGA 1/0558/17.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

449_2019_2112_MOESM1_ESM.pdf (397 kb)
Supplementary material 1 (PDF 396 KB)


  1. 1.
    Rouf MA, Islam MS, Rabeya T, Mondal AK (2015) Anaerobic digestion of mixed dried fallen leaves by mixing with cow dung. Bangladesh J Sci Ind Res 50:163–168CrossRefGoogle Scholar
  2. 2.
    Elghandour MMY, Vallejo LH, Salem AZM, Mellado M, Camacho LM, Cipriano M, Olafadehan OA, Olivares J, Rojas S (2017) Moringa oleifera leaf meal as an environmental friendly protein source for ruminants: biomethane and carbon dioxide production, and fermentation characteristics. J Clean Prod 165:1229–1238CrossRefGoogle Scholar
  3. 3.
    Taherzadeh MJ, Karimi K (2008) Pretreatment of lignocellulosic wastes to improve ethanol and biogas production: a Review. Int J Mol Sci 9:1621–1651CrossRefGoogle Scholar
  4. 4.
    Mtui GYS (2009) Recent advances in pretreatment of lignocellulosic wastes and production of value added products. Afr J Biotechnol 8:1398–1415Google Scholar
  5. 5.
    Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194CrossRefGoogle Scholar
  6. 6.
    Wu C, Jin LY, Zhang PY, Zhang GM (2015) Effects of potassium ferrate oxidation on sludge disintegration, dewaterability and anaerobic biodegradation. Int Biodeterior Biodegrad 102:137–142CrossRefGoogle Scholar
  7. 7.
    Ye FX, Ji HZ, Ye YF (2012) Effect of potassium ferrate on disintegration of waste activated sludge (WAS). J Hazard Mater 219–220:164–168CrossRefGoogle Scholar
  8. 8.
    Zhang XH, Lei HY, Chen K, Liu Z, Wu H, Liang HY (2012) Effect of potassium ferrate (K2FeO4) on sludge dewaterability under different pH conditions. Chem Eng J 210:467–474CrossRefGoogle Scholar
  9. 9.
    Li L, He J, Xin X, Wang M, Xu J, Zhang J (2018) Enhanced bioproduction of short-chain fatty acids from waste activated sludge by potassium ferrate pretreatment. Chem Eng J 332:456–463CrossRefGoogle Scholar
  10. 10.
    Mackulak T, Birosova L, Bodik I, Grabic R, Takacova A, Smolinska M, Hanusova A, Hives J, Gal M (2016) Zerovalent iron and iron (VI): effective means for the removal of psychoactive pharmaceuticals and illicit drugs from wastewaters. Sci Total Environ 539:420–426CrossRefGoogle Scholar
  11. 11.
    Kapp H (1984) Schlammfaulung mit hohem Feststoffgehalt. Stuttgarter Berichte zur Siedlungswasserwirtschaft. Kommissionsverlag Oldenburg, MunichGoogle Scholar
  12. 12.
    APHA/AWWA/WEF (1998) Standard methods for the examination of water and wastewater, 10th edn. American Public Health Association/American Water Works Association/Water Environment Federation, WashingtonGoogle Scholar
  13. 13.
    Kraková L, Šoltys K, Otlewska A, Pietrzak K, Purkrtová S, Savická D, Puškárová A, Bučková M, Szemes T, Budiš J, Demnerová K, Gutarowska B, Pangallo D (2018) Comparison of methods for identification of microbial communities in book collections: culture-dependent (sequencing and MALDI-TOF MS) and culture-independent (Illumina MiSeq). Int Biodeterior Biodegrad 131:51–59CrossRefGoogle Scholar
  14. 14.
    Pangallo D, Bučková M, Kraková L, Puškárová A, Šaková N, Grivalský T, Chovanová K, Zemánková M (2015) Biodeterioration of epoxy resin: a microbial survey through culture-independent and culture-dependent approaches. Environ Microbiol 17:462–479CrossRefGoogle Scholar
  15. 15.
    Kraková L, Šoltys K, Budiš J, Grivalský T, Ďuriš F, Pangallo D, Szemes T (2016) Investigation of bacterial and archaeal communities: novel protocols using modern sequencing by Illumina MiSeq and traditional DGGE-cloning. Extremophiles 20:795–808CrossRefGoogle Scholar
  16. 16.
    Leaphart AB, Lovell CR (2001) Recovery and analysis of formyltetrahydrofolate synthetase gene sequences from natural populations of acetogenic bacteria. Appl Environ Microbiol 67:1392CrossRefGoogle Scholar
  17. 17.
    Müller B, Sun L, Westerholm M, Schnürer A (2013) First insights into the syntrophic acetate-oxidizing bacteria—a genetic study. Microbiologyopen 2:35–53CrossRefGoogle Scholar
  18. 18.
    Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  19. 19.
    Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Accessed 11 Nov 2017
  20. 20.
    Xu H, Luo X, Qian J, Pang X, Song J, Qian G, Chen J, Chen S (2012) FastUniq: a fast de novo duplicates removal tool for paired short reads. PloS One 7:e52249CrossRefGoogle Scholar
  21. 21.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596CrossRefGoogle Scholar
  22. 22.
    Bengtsson-Palme J, Hartmann M, Eriksson KM, Pal C, Thorell K, Larsson DGJ, Nilsson RH (2015) METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol Ecol Resour 15:1403–1414CrossRefGoogle Scholar
  23. 23.
    Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF (2011) EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12:R44CrossRefGoogle Scholar
  24. 24.
    Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068CrossRefGoogle Scholar
  25. 25.
    Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucleic Acids Res 41:D36–D42CrossRefGoogle Scholar
  26. 26.
    Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinform 12:385CrossRefGoogle Scholar
  27. 27.
    Carrère H, Rafrafi Y, Battimelli A, Torrijos M, Delgenès JP, Ruysschaert G (2010) Methane potential of waste activated sludge and fatty residues: Impact of codigestion and alkaline pre-treatments. Open Environ Eng J 3:71–76CrossRefGoogle Scholar
  28. 28.
    Tippayawong N, Thanompongchart P (2010) Biogas quality upgrade by simultaneous removal of CO2 and H2S in a packed column reactor. Energy 35:4531–4535CrossRefGoogle Scholar
  29. 29.
    Roth SH (1993) Hydrogen sulfide. In: Handbook of hazardous materials. Academic Press, New YorkGoogle Scholar
  30. 30.
    Syed M, Soreanu G, Falletta P, Béland M (2006) Removal of hydrogen sulfide from gas streams using biological processes—a review. Can Biosyst Eng 48: 2.1–2.14Google Scholar
  31. 31.
    Abatzoglou N, Boivin S (2009) A review of biogas purification processes. Biofuels Bioprod Biorefining. 3: 42–71CrossRefGoogle Scholar
  32. 32.
    Ozekmekci M, Salkic G, Fellah MF (2015) Use of zeolites for the removal of H2S: a mini-review. Fuel Process Technol 139:49–60CrossRefGoogle Scholar
  33. 33.
    Awe OW, Zhao Y, Nzihou A, Minh DP, Lyczko N (2017) A review of biogas utilisation, purification and upgrading technologies. Waste Biomass Valor 8:267–283CrossRefGoogle Scholar
  34. 34.
    Veeken A, Hamelers B (1999) Effect of temperature on hydrolysis rates of selected biowaste components. Bioresour Technol 69:249–254CrossRefGoogle Scholar
  35. 35.
    Dohányos M, Zábranská J, Jenícek P, Fialka P, Kajan M (1998) Anaerobní cistírenské technologie, NOEL 2000s.r.o., BrnoGoogle Scholar
  36. 36.
    Manyi-Loh CE, Mamphweli SN, Meyer EL, Okoh AI, Makaka G, Simon M (2013) Microbial anaerobic digestion as an approach to the decontamination of animal wastes in pollution control and the generation of renewable energy. Int J Environ Res Public Health 10:4390–4417CrossRefGoogle Scholar
  37. 37.
    Riviere D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3:700–714CrossRefGoogle Scholar
  38. 38.
    Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sørensen SJ, Karlsson A (2013) 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 85:612–626CrossRefGoogle Scholar
  39. 39.
    De Francisci D, Kougias PG, Treu L, Campanaro S, Angelidaki I (2015) Microbial diversity and dynamicity of biogas reactors due to radical changes of feedstock composition. Bioresour Technol 176:56–64CrossRefGoogle Scholar
  40. 40.
    Delforno TP, Lacerda Júnior GV, Noronha MF, Sakamoto IK, Varesche MBA, Oliveira VM (2017) Microbial diversity of a full-scale UASB reactor applied to poultry slaughterhouse wastewater treatment: integration of 16S rRNA gene amplicon and shotgun metagenomic sequencing. Microbiologyopen 6:12CrossRefGoogle Scholar
  41. 41.
    Azman S, Khadem AF, van Lier JB, Zeeman G, Plugge CM (2015) Presence and role of anaerobic hydrolytic microbes in conversion of lignocellulosic biomass for biogas production. Crit Rev Environ Sci Technol 45:2523–2564CrossRefGoogle Scholar
  42. 42.
    Hanreich A, Schimpf U, Zakrzewski M, Schlüter A, Benndorf D, Heyer R, Rapp E, Pühler A, Reichl U, Klocke M (2013) Metagenome and metaproteome analyses of microbial communities in mesophilic biogas-producing anaerobic batch fermentations indicate concerted plant carbohydrate degradation. Syst Appl Microbiol 36:330–338CrossRefGoogle Scholar
  43. 43.
    Medie FM, Davies GJ, Drancourt M, Henrissat B (2012) Genome analyses highlight the different biological roles of cellulases. Nat Rev Micro 10:227–234CrossRefGoogle Scholar
  44. 44.
    Su JJ (2017) In: Pawlowska M (Ed.) Pawlowski A (eds) Advances in renewable energy research. CRC Press, LondonGoogle Scholar
  45. 45.
    Nishiyama T, Ueki A, Kaku N, Watanabe K, Ueki K (2009) Bacteroides graminisolvens sp. nov., a xylanolytic anaerobe isolated from a methanogenic reactor treating cattle waste. Int J Syst Evol Microbiol 59:1901–1907CrossRefGoogle Scholar
  46. 46.
    Müller B, Sun L, Westerholm M, Schnürer A (2016) Bacterial community composition and fhs profiles of low and high-ammonia biogas digesters reveal novel syntrophic acetate-oxidising bacteria. Biotechnol Biofuels 9:18CrossRefGoogle Scholar
  47. 47.
    Theuerl S, Kohrs F, Benndorf D, Maus I, Wibberg D, Schlüter A, Kausmann R, Heiermann M, Rapp E, Reichl U, Pühler A, Klocke M (2015) Community shifts in a well-operating agricultural biogas plant: how process variations are handled by the microbiome. Appl Microbiol Biotechnol 99:7791–7803CrossRefGoogle Scholar
  48. 48.
    Schlüter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann KH, Krahn I, Krause L, Krömeke H, Kruse O, Mussgnug JH, Neuweger H, Niehaus K, Pühler A, Runte KJ, Szczepanowski R, Tauch A, Tilker A, Viehöver P, Goesmann A (2008) The metagenome of a biogas-producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. J Biotechnol 136:77–90CrossRefGoogle Scholar
  49. 49.
    Drake HL, Küsel K, Matthies C (2006) In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) A handbook on the biology of bacteria, vol 3, Springer, New YorkGoogle Scholar
  50. 50.
    Yuan Z, Wu C, Ma L (2017) In: Yuan Z (ed) Bioenergy: principles and technologies. Walter de Gruyter GmbH & Co KG, BerlinGoogle Scholar
  51. 51.
    Angelidaki I, Karakashev D, Batstone DJ, Plugge CM, Stams AJM (2011) Biomethanation and its potential. Meth Enzymol 494:327–351CrossRefGoogle Scholar
  52. 52.
    Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Biotechnol 7:173–190CrossRefGoogle Scholar
  53. 53.
    Christy PM, Gopinath LR, Divya D (2014) A review on anaerobic decomposition and enhancement of biogas production through enzymes and microorganisms. Renew Sust Energ Rev 34:167–173CrossRefGoogle Scholar
  54. 54.
    Kröninger L, Gottschling J, Deppenmeier U (2017) Growth characteristics of Methanomassiliicoccus luminyensis and expression of methyltransferase encoding genes. Archaea. Google Scholar
  55. 55.
    Westerholm M, Levén L, Schnürer A (2012) Bioaugmentation of syntrophic acetate-oxidizing culture in biogas reactors exposed to increasing levels of ammonia. Appl Environ Microbiol 78:7619–7625CrossRefGoogle Scholar
  56. 56.
    Kendall MM, Boone DR (2006) In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) A handbook on the biology of bacteria, vol 3, Springer, New YorkGoogle Scholar
  57. 57.
    Karakashev D, Batstone DJ, Angelidaki I (2005) Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors. Appl Environ Microbiol 71:331–338CrossRefGoogle Scholar
  58. 58.
    Zinder SH (1993) In: Ferry JG (ed) Methanogenesis. Ecology, physiology, biochemistry and genetics. Chapman and Hall, New YorkGoogle Scholar
  59. 59.
    Ritari J, Koskinen K, Hultman J, Kurola JM, Kymäläinen M, Romantschuk M, Paulin L, Auvinen P (2012) Molecular analysis of meso- and thermophilic microbiota associated with anaerobic biowaste degradation. BMC Microbiol. Google Scholar
  60. 60.
    Fillat U, Martín-Sampedro R, Macaya-Sanz D, Martín JA, Ibarra D, Martínez MJ, Eugenio ME (2016) Screening of eucalyptus wood endophytes for laccase activity. Process Biochem 51:589–598CrossRefGoogle Scholar
  61. 61.
    Ceballos SJ, Yu C, Claypool JT, Singer SW, Simmons BA, Thelen MP, Simmons CW, VanderGheynst JS (2017) Development and characterization of a thermophilic, lignin degrading microbiota. Process Biochem 63:193–203CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Matej Planý
    • 1
  • Marianna Czolderová
    • 2
  • Lucia Kraková
    • 1
  • Andrea Puškárová
    • 1
  • Mária Bučková
    • 1
  • Katarína Šoltys
    • 3
  • Jaroslav Budiš
    • 4
    • 5
  • Tomáš Szemes
    • 3
    • 4
    • 6
  • Tomáš Mackulak
    • 7
  • Jer-Horng Wu
    • 8
  • Domenico Pangallo
    • 1
    • 9
    Email author
  1. 1.Institute of Molecular BiologySlovak Academy of ScienceBratislavaSlovakia
  2. 2.Department of Inorganic Technology, Faculty of Chemical and Food TechnologySlovak University of TechnologyBratislavaSlovakia
  3. 3.Comenius University in Bratislava, Comenius University Science ParkBratislavaSlovakia
  4. 4.Geneton s.r.o.BratislavaSlovakia
  5. 5.Department of Computer Science, Faculty of Mathematics, Physics and InformaticsComenius University in BratislavaBratislavaSlovakia
  6. 6.Department of Molecular Biology, Faculty of Natural SciencesComenius University in BratislavaBratislavaSlovakia
  7. 7.Institute of Chemical and Environmental Engineering, Faculty of Chemical and Food TechnologySlovak University of TechnologyBratislavaSlovakia
  8. 8.Department of Environmental EngineeringNational Cheng Kung UniversityTainan CityTaiwan, Republic of China
  9. 9.Caravella s.r.o.BratislavaSlovakia

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