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Microbial community composition and dynamics in high-temperature biogas reactors using industrial bioethanol waste as substrate

  • Environmental biotechnology
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Abstract

Stillage, which is generated during bioethanol production, constitutes a promising substrate for biogas production within the scope of an integrated biorefinery concept. In this study, a microbial community was grown on thin stillage as mono-substrate in a continuous stirred tank reactor (CSTR) at a constant temperature of 55 °C, at an organic loading rate of 1.5 goTS/L*d and a retention time of 25 days. Using an amplicon-based dataset of 17,400 high-quality sequences of 16S rRNA gene fragments (V2–V3 regions), predominance of Bacteria assigned to the families Thermotogaceae and Elusimicrobiaceae was detected. Dominant members of methane-producing Euryarchaeota within the CSTR belonged to obligate acetoclastic Methanosaetaceae and hydrogenotrophic Methanobacteriaceae. In order to investigate population dynamics during reactor acidification, the organic loading rate was increased abruptly, which resulted in an elevated concentration of volatile fatty acids. Acidification led to a decrease in relative abundance of Bacteria accompanied with stable numbers of Archaea. Nevertheless, the abundance of Methanosaetaceae increased while that of Methanobacteriales decreased successively. These findings demonstrate that a profound intervention to the biogas process may result in persistent community changes and reveals uncommon bacterial families as process-relevant microorganisms.

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References

  • Ahring BK (1995) Methanogenesis in thermophilic biogas reactors. Antonie Van Leeuwenhoek 67:91–102

    Article  PubMed  CAS  Google Scholar 

  • Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770

    PubMed  CAS  PubMed Central  Google Scholar 

  • Baker GC, Cowan DA (2004) 16S rDNA primers and the unbiased assessment of thermophile diversity. Biochem Soc Trans 32:218–221

    Article  PubMed  CAS  Google Scholar 

  • Balk M, Weijma J, Stams AJ (2002) Thermotoga lettingae sp. nov., a novel thermophilic, methanol-degrading bacterium isolated from a thermophilic anaerobic reactor. Int J Syst Evol Microbiol 52:1361–1368

    Article  PubMed  CAS  Google Scholar 

  • Ben Hania W, Godbane R, Postec A, Hamdi M, Ollivier B, Fardeau ML (2012) Defluviitoga tunisiensis gen. nov., sp nov., a thermophilic bacterium isolated from a mesothermic and anaerobic whey digester. Int J Syst Evol Microbiol 62:1377–1382. doi:10.1099/ijs.0.033720-0

    Article  PubMed  CAS  Google Scholar 

  • Boone DR, Whitman WB, Rouvière P (1993) Diversity and taxonomy of methanogens. In: Ferry JG (ed) Methanogenesis: ecology, physiology, biochemistry & genetics, vol. 1. Chapman & Hall, New York, pp 35–80

    Chapter  Google Scholar 

  • Burtscher C, Fall PA, Christ O, Wilderer PA, Wuertz S (1998) Detection and survival of pathogens during two-stage thermophilic/mesophilic anaerobic treatment of suspended organic waste. Water Sci Technol 38:123–126. doi:10.1016/S0273-1223(98)00812-9

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chakravorty S, Helb D, Burday M, Connell N, Alland D (2007) A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Meth 69:330–339. doi:10.1016/j.mimet.2007.02.005

    Article  CAS  Google Scholar 

  • Chao A, Bunge J (2002) Estimating the number of species in a stochastic abundance model. Biometrics 58:531–539

    Article  PubMed  Google Scholar 

  • Chen M (1983) Adaptation of mesophilic anaerobic sewage fermentor populations to thermophilic temperatures. Appl Environ Microbiol 45:1271–1276

    PubMed  CAS  PubMed Central  Google Scholar 

  • Danhorn T, Young CR, DeLong EF (2012) Comparison of large-insert, small-insert and pyrosequencing libraries for metagenomic analysis. ISME J 6:2152–2152. doi:10.1038/ismej.2012.35

    Article  Google Scholar 

  • Davey ME, Wood WA, Key R, Nakamura K, Stahl DA (1993) Isolation of three species of Geotoga and Petrotoga: two new genera, representing a new lineage in the bacterial line of descent distantly related to the Thermotogales. Syst Appl Microbiol 16:191–200

    Article  Google Scholar 

  • 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 7:173–190. doi:10.1007/s11157-008-9131-1

    Article  CAS  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • DiPippo JL, Nesbø CL, Dahle H, Doolittle WF, Birkland NK, Noll KM (2009) Kosmotoga olearia gen. nov., sp nov., a thermophilic, anaerobic heterotroph isolated from an oil production fluid. Int J Syst Evol Microbiol 59:2991–3000. doi:10.1099/ijs.0.008045-0

    Article  PubMed  CAS  Google Scholar 

  • Dong X, Plugge CM, Stams AJ (1994) Anaerobic degradation of propionate by a mesophilic acetogenic bacterium in coculture and triculture with different methanogens. Appl Environ Microbiol 60:2834–2838

    PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  PubMed Central  Google Scholar 

  • España-Gamboa EI, Mijangos-Cortés JO, Hernández-Zárate G, Maldonado JAD, Alzate-Gaviria LM (2012) Methane production by treating vinasses from hydrous ethanol using a modified UASB reactor. Biotechnol Biofuels 5:82. doi:10.1186/1754-6834-5-82

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng YX, Cheng L, Zhang XX, Li X, Deng Y, Zhang H (2010) Thermococcoides shengliensis gen. nov., sp nov., a new member of the order Thermotogales isolated from oil-production fluid. Int J Syst Evol Microbiol 60:932–937. doi:10.1099/ijs.0.013912-0

    Article  PubMed  CAS  Google Scholar 

  • Ferry JG (1999) Enzymology of one-carbon metabolism in methanogenic pathways. FEMS Microbiol Rev 23:13–38

    Article  PubMed  CAS  Google Scholar 

  • Geissinger O, Herlemann DPR, Mörschel E, Maier UG, Brune A (2009) The ultramicrobacterium “Elusimicrobium minutum” gen. nov., sp nov., the first cultivated representative of the Termite Group 1 phylum. Appl Environ Microbiol 75:2831–2840. doi:10.1128/Aem.02697-08

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Griffin ME, McMahon KD, Mackie RI, Raskin L (1998) Methanogenic population dynamics during start-up of anaerobic digesters treating municipal solid waste and biosolids. Biotechnol Bioeng 57:342–355

    Article  PubMed  CAS  Google Scholar 

  • Herlemann DPR, Geissinger O, Brune A (2007) The Termite Group I phylum is highly diverse and widespread in the environment. Appl Environ Microbiol 73:6682–6685. doi:10.1128/Aem.00712-07

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hongoh Y, Ohkuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44:231–242. doi:10.1016/S0168-6496(03)00026-6

    Article  PubMed  CAS  Google Scholar 

  • Hori T, Haruta S, Ueno Y, Ishii M, Igarashi Y (2006) Dynamic transition of a methanogenic population in response to the concentration of volatile fatty acids in a thermophilic anaerobic digester. Appl Environ Microbiol 72:1623–1630. doi:10.1128/Aem.72.2.1623-1630.2006

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • IEA (2010) Sustainable production of second-generation biofuels. Potential and perspectives in major economies and developing countries. IEA/OECD. Paris. http://www.iea.org/publications/freepublications/publication/second_generation_biofuels.pdf

  • Jaenicke S, Ander C, Bekel T, Bisdorf R, Dröge M, Gartemann KH, Jünemann S, Kaiser O, Krause L, Tille F, Zakrzewski M, Pühler A, Schlüter A, Goesmann A (2011) Comparative and joint analysis of two metagenomic datasets from a biogas fermenter obtained by 454-pyrosequencing. PLoS ONE 6:e14519. doi:10.1371/journal.pone.0014519

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jetten MS, Stams AJ, Zehnder AJ (1992) Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Lett 88:181–197

    Article  CAS  Google Scholar 

  • Karakashev D, Batstone DJ, Trably E, Angelidaki I (2006) Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Appl Environ Microbiol 72:5138–5141. doi:10.1128/Aem.00489-06

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kardos L, Juhász A, Palkó G, Oláh J, Barkács K, Záray G (2011) Comparing of mesophilic and thermophilic anaerobic fermented sewage sludge based on chemical and biochemical tests. Appl Ecol Environ Res 9:293–302

    Article  Google Scholar 

  • Kim S, Hwang MH, Jang NJ, Hyun SH, Lee ST (2003) Effect of low pH on the activity of hydrogen utilizing methanogen in bio-hydrogen process. Int J Hydrogen Energy 29:1133–1140. doi:10.1016/j.ijhydene.2003.08.017

    Google Scholar 

  • Kim Y, Mosier NS, Hendrickson R, Ezeji T, Blaschek H, Dien B, Cotta M, Dale B, Ladisch MR (2008) Composition of corn dry-grind ethanol by-products: DDGS, wet cake, and thin stillage. Bioresour Technol 99:5165–5176. doi:10.1016/j.biortech.2007.09.028

    Article  PubMed  CAS  Google Scholar 

  • Krakat N, Westphal A, Schmidt S, Scherer P (2010) Anaerobic digestion of renewable biomass: thermophilic temperature governs methanogen population dynamics. Appl Environ Microbiol 76:1842–1850. doi:10.1128/Aem.02397-09

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kreipe H (1982) Getreide- und Kartoffelbrennerei, vol. 3. Eugen Ulmer, Stuttgart

    Google Scholar 

  • Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehover P, Pühler A, Schlüter A (2009) Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. J Biotechnol 142:38–49. doi:10.1016/J.Jbiotec.2009.02.010

    Article  PubMed  Google Scholar 

  • Kumar PS, Brooker MR, Dowd SE, Camerlengo T (2011) Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS ONE 6:e20956. doi:10.1371/journal.pone.0020956

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lee C, Kim J, Hwang K, O'Flaherty V, Hwang S (2009) Quantitative analysis of methanogenic community dynamics in three anaerobic batch digesters treating different wastewaters. Water Res 43:157–165. doi:10.1016/J.Watres.2008.09.032

    Article  PubMed  CAS  Google Scholar 

  • Leitão RC, van Haandel AC, Zeeman G, Lettinga G (2006) The effects of operational and environmental variations on anaerobic wastewater treatment systems: a review. Bioresour Technol 97:1105–1118. doi:10.1016/j.biortech.2004.12.007

    Article  PubMed  Google Scholar 

  • Lie TJ, Costa KC, Lupa B, Korpole S, Whitman WB, Leigh JA (2012) Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc Natl Acad Sci U S A 109:15473–15478. doi:10.1073/Pnas.1208779109

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lin CY, Chen CC (1999) Effect of heavy metals on the methanogenic UASB granule. Water Res 33:409–416. doi:10.1016/S0043-1354(98)00211-5

    Article  CAS  Google Scholar 

  • Liu YC, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189. doi:10.1196/Annals.1419.019

    Article  PubMed  CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. doi:10.14806/ej.17.1.200

    Article  Google Scholar 

  • McMahon KD, Stroot PG, Mackie RI, Raskin L (2001) Anaerobic codigestion of municipal solid waste and biosolids under various mixing conditions - II: microbial population dynamics. Water Res 35:1817–1827. doi:10.1016/S0043-1354(00)00438-3

    Article  PubMed  CAS  Google Scholar 

  • Miranda-Tello E, Fardeau M-L, Joulian C, Magot M, Thomas P, Tholozan J-L, Ollivier B (2007) Petrotoga halophila sp. nov., a thermophilic, moderately halophilic, fermentative bacterium isolated from an offshore oil well in Congo. Int J Syst Evol Microbiol 57:40–44

    Article  PubMed  CAS  Google Scholar 

  • Munk B, Bauer C, Gronauer A, Lebuhn M (2010) Population dynamics of methanogens during acidification of biogas fermenters fed with maize silage. Eng Life Sci 10:496–508. doi:10.1002/Elsc.201000056

    Article  CAS  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141. doi:10.1023/A:1000669317571

    Article  PubMed  CAS  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  PubMed Central  Google Scholar 

  • Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel-electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172. doi:10.1007/Bf02529967

    Article  PubMed  CAS  Google Scholar 

  • Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schöning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS ONE 6:e17000. doi:10.1371/journal.pone.0017000

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Newton RJ, VandeWalle JL, Borchardt MA, Gorelick MH, McLellan SL (2011) Lachnospiraceae and Bacteroidales alternative fecal indicators reveal chronic human sewage contamination in an urban harbor. Appl Environ Microbiol 77:6972–6981. doi:10.1128/Aem.05480-11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nosrati M, Shojaosadati SA, Sreekrishnan TR (2006) Thermophilic aerobic digestion of activated sludge; reduction of solids and pathogenic microorganisms. Iran J Chem Chem Eng Int Engl Ed 25:67–71

    CAS  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. doi:10.1093/nar/gkm864

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rademacher A, Nolte C, Schönberg M, Klocke M (2012a) Temperature increases from 55 to 75 °C in a two-phase biogas reactor result in fundamental alterations within the bacterial and archaeal community structure. Appl Microbiol Biotechnol 96:565–576. doi:10.1007/S00253-012-4348-X

    Article  PubMed  CAS  Google Scholar 

  • Rademacher A, Zakrzewski M, Schlüter A, Schönberg M, Szczepanowski R, Goesmann A, Pühler A, Klocke M (2012b) Characterization of microbial biofilms in a thermophilic biogas system by high-throughput metagenome sequencing. FEMS Microbiol Ecol 79:785–799. doi:10.1111/J.1574-6941.2011.01265.X

    Article  PubMed  CAS  Google Scholar 

  • Raskin L, Poulsen LK, Noguera DR, Rittmann BE, Stahl DA (1994) Quantification of methanogenic groups in anaerobic biological reactors by oligonucleotide probe hybridization. Appl Environ Microbiol 60:1241–1248

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ravot G, Ollivier B, Fardeau ML, Patel BKC, Andrews KT, Magot M, Garcia JL (1996) L-Alanine production from glucose fermentation by hyperthermophilic members of the domains Bacteria and Archaea: a remnant of an ancestral metabolism? Appl Environ Microbiol 62:2657–2659

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rivière 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 3:700–714. doi:10.1038/ismej.2009.2

    Article  PubMed  Google Scholar 

  • Sahm K, John P, Nacke H, Wemheuer B, Grote R, Daniel R, Antranikian G (2013) High abundance of heterotrophic prokaryotes in hydrothermal springs of the Azores as revealed by a network of 16S rRNA gene-based methods. Extremophiles 17:649–662. doi:10.1007/s00792-013-0548-2

    Article  PubMed  CAS  Google Scholar 

  • Sasaki K, Sasaki D, Morita M, Hirano S, Matsumoto N, Ohmura N, Igarashi Y (2010) Bioelectrochemical system stabilizes methane fermentation from garbage slurry. Bioresour Technol 101:3415–3422. doi:10.1016/j.biortech.2009.12.076

    Article  PubMed  CAS  Google Scholar 

  • Sasaki D, Sasaki K, Watanabe A, Morita M, Igarashi Y, Ohmura N (2013) Efficient production of methane from artificial garbage waste by a cylindrical bioelectrochemical reactor containing carbon fiber textiles. AMB Express 3:17. doi:10.1186/2191-0855-3-17

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 136:77–90. doi:10.1016/J.Jbiotec.2008.05.008

    Article  PubMed  Google Scholar 

  • Schnürer A, Zellner G, Svensson BH (1999) Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol 29:249–261. doi:10.1111/j.1574-6941.1999.tb00616.x

    Article  Google Scholar 

  • Scholten JCM, Conrad R (2000) Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Appl Environ Microbiol 66:2934–2942. doi:10.1128/Aem.66.7.2934-2942.2000

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sheffield VC, Cox DR, Lerman LS, Myers RM (1989) Attachment of a 40-base-pair G + C-rich sequence (GC-clamp) to genomic DNA fragments by the polymerase chain reaction results in improved detection of single-base changes. Proc Natl Acad Sci U S A 86:232–236

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Snaidr J, Amann R, Huber I, Ludwig W, Schleifer KH (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63:2884–2896

    PubMed  CAS  PubMed Central  Google Scholar 

  • Stams AJ, Dijkema C, Plugge CM, Lens P (1998) Contribution of 13C-NMR spectroscopy to the elucidation of pathways of propionate formation and degradation in methanogenic environments. Biodegradation 9:463–473

    Article  CAS  Google Scholar 

  • Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sorensen SJ, Karlsson A (2013) 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 85:612–626. doi:10.1111/1574-6941.12148

    Article  PubMed  CAS  Google Scholar 

  • Wallner G, Amman R, Beisker W (1993) Optimizing fluorescent in situ hybridization of suspended cells with rRNA-targeted oligonucleotide probes for the flow cytometric identification of microorganisms. Cytometry 14:136–143

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Asakawa S, Nakamura A, Nagaoka K, Kimura M (2004) DGGE method for analyzing 16S rDNA of methanogenic archaeal community in paddy field soil. FEMS Microbiol Lett 232:153–163. doi:10.1016/S0378-1097(04)00045-X

    Article  PubMed  CAS  Google Scholar 

  • Wilkie AC, Riedesel KJ, Owens JM (2000) Stillage characterization and anaerobic treatment of ethanol stillage from conventional and cellulosic feedstocks. Biomass Bioenergy 19:63–102

    Article  CAS  Google Scholar 

  • Wirth R, Kovács E, Maroti G, Bagi Z, Rákhely G, Kovács KL (2012) Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing. Biotechnol Biofuels 5:41. doi:10.1186/1754-6834-5-41

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xu SY, He PJ, Lu F, Li M, Shao LM (2009) Transformation of organic matters in fresh leachate during anaerobic degradation under long hydraulic retention time. J Environ Sci (China) 21:1302–1308. doi:10.1016/S1001-0742(08)62419-5

    Article  CAS  Google Scholar 

  • Ye L, Zhang T (2013) Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing. Appl Microbiol Biotechnol 97:2681–2690. doi:10.1007/S00253-012-4082-4

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang R, Tao J, Dugba P (2000) Evaluation of two-stage anaerobic sequencing batch reactor systems for animal wastewater treatment. Trans ASAE 43:1795–1802

    Article  CAS  Google Scholar 

  • Zhang T, Liu H, Fang HHP (2003) Biohydrogen production from starch in wastewater under thermophilic condition. J Environ Manag 69:149–156. doi:10.1016/S0301-4797(03)00141-5

    Article  Google Scholar 

  • Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhu H, Beland M (2006) Evaluation of alternative methods of preparing hydrogen producing seeds from digested wastewater sludge. Int J Hydrogen Energy 31:1980–1988. doi:10.1016/j.ijhydene.2006.01.019

    Article  CAS  Google Scholar 

  • Ziganshin AM, Schmidt T, Scholwin F, Il’inskaya ON, Harms H, Kleinsteuber S (2011) Bacteria and archaea involved in anaerobic digestion of distillers grains with solubles. Appl Microbiol Biotechnol 89:2039–2052. doi:10.1007/S00253-010-2981-9

    Article  PubMed  CAS  Google Scholar 

  • Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis: ecology, physiology, biochemistry & genetics, vol. 1. Chapman & Hall, New York, pp 128–206

    Chapter  Google Scholar 

  • Zinder SH (1995) Syntrophic acetate oxidation and “reversible acetogenesis”. In: Drake HL (ed) Acetogenesis. Chapman & Hall, New York, pp 386–415

    Google Scholar 

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Acknowledgments

This project was funded by the German Federal Ministry for Education and Research (BMBF) through the Project Management Jülich (PtJ) as part of the Cluster Biorefinery2021 (grant no. 0315559A). I. Röske and W. Sabra gratefully acknowledge the receipt of a scholarship and the SynBio grant from the State Excellence Initiative Hamburg.

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Röske, I., Sabra, W., Nacke, H. et al. Microbial community composition and dynamics in high-temperature biogas reactors using industrial bioethanol waste as substrate. Appl Microbiol Biotechnol 98, 9095–9106 (2014). https://doi.org/10.1007/s00253-014-5906-1

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