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Microbial community structure and dynamics during anaerobic digestion of various agricultural waste materials

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Abstract

The influence of the feedstock type on the microbial communities involved in anaerobic digestion was investigated in laboratory-scale biogas reactors fed with different agricultural waste materials. Community composition and dynamics over 2 months of reactors’ operation were investigated by amplicon sequencing and profiling terminal restriction fragment length polymorphisms of 16S rRNA genes. Major bacterial taxa belonged to the Clostridia and Bacteroidetes, whereas the archaeal community was dominated by methanogenic archaea of the orders Methanomicrobiales and Methanosarcinales. Correlation analysis revealed that the community composition was mainly influenced by the feedstock type with the exception of a temperature shift from 38 to 55 °C which caused the most pronounced community shifts. Bacterial communities involved in the anaerobic digestion of conventional substrates such as maize silage combined with cattle manure were relatively stable and similar to each other. In contrast, special waste materials such as chicken manure or Jatropha press cake were digested by very distinct and less diverse communities, indicating partial ammonia inhibition or the influence of other inhibiting factors. Anaerobic digestion of chicken manure relied on syntrophic acetate oxidation as the dominant acetate-consuming process due to the inhibition of aceticlastic methanogenesis. Jatropha as substrate led to the enrichment of fiber-degrading specialists belonging to the genera Actinomyces and Fibrobacter.

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References

  • Abdo Z, Schütte UM, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938

    Article  Google Scholar 

  • Ariesyady HD, Ito T, Okabe S (2007) Functional bacterial and archaeal community structures of major trophic groups in a full-scale anaerobic digester. Water Res 41:1554–1568

    Article  CAS  Google Scholar 

  • Asakawa S, Nagaoka K (2003) Methanoculleus bourgensis, Methanoculleus olentangyi and Methanoculleus oldenburgensis are subjective synonyms. Int J Syst Evol Microbiol 53:1551–1552

    Article  CAS  Google Scholar 

  • Béra-Maillet C, Ribot Y, Forano E (2004) Fiber-degrading system of different strains of the genus Fibrobacter. Appl Environ Microbiol 70:2172–2179

    Article  Google Scholar 

  • Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064

    Article  CAS  Google Scholar 

  • Cheng L, Qiu TL, Li X, Wang WD, Deng Y, Yin XB, Zhang H (2008) Isolation and characterization of Methanoculleus receptaculi sp. nov. from Shengli oil field, China. FEMS Microbiol Lett 285:65–71

    Article  CAS  Google Scholar 

  • Das D, Veziroglu TN (2001) Hydrogen production by biological processes: a survey of literature. Int J Hydrogen Energy 26:13–28

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Dianou D, Miyaki T, Asakawa S, Morii H, Nagaoka K, Oyaizu H, Matsumoto S (2001) Methanoculleus chikugoensis sp. nov., a novel methanogenic archaeon isolated from paddy field soil in Japan, and DNA-DNA hybridization among Methanoculleus species. Int J Syst Evol Microbiol 51:1663–1669

    Article  CAS  Google Scholar 

  • Elberson MA, Sowers KR (1997) Isolation of an aceticlastic strain of Methanosarcina siciliae from marine canyon sediments and emendation of the species description for Methanosarcina siciliae. Int J Syst Bacteriol 47:1258–1261

    Article  CAS  Google Scholar 

  • El-Mashad HM, Zhang R (2010) Biogas production from co-digestion of dairy manure and food waste. Bioresour Technol 101:4021–4028

    Article  CAS  Google Scholar 

  • Fontes CM, Gilbert HJ (2010) Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79:655–681

    Article  CAS  Google Scholar 

  • Gerardi MH (2003) The microbiology of anaerobic digesters. Wiley, Hoboken

    Book  Google Scholar 

  • Goberna M, Insam H, Franke-Whittle IH (2009) Effect of biowaste sludge maturation on the diversity of thermophilic bacteria and archaea in an anaerobic reactor. Appl Environ Microbiol 75:2566–2572

    Article  CAS  Google Scholar 

  • Hattori S (2008) Syntrophic acetate-oxidizing microbes in methanogenic environments. Microbes Environ 2:118–127

    Article  Google Scholar 

  • Hattori S, Kamagata Y, Hanada S, Shoun H (2000) Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol 50:1601–1609

    Article  CAS  Google Scholar 

  • Holm-Nielsen JB, Al Seadi T, Oleskowicz-Popiel P (2009) The future of anaerobic digestion and biogas utilization. Bioresour Technol 100:5478–5484

    Article  CAS  Google Scholar 

  • Karlsson A, Einarsson P, Schnürer A, Sundberg C, Ejlertsson J, Svensson B (2012) Impact of trace element addition on degradation efficiency of volatile fatty acids, oleic acid and phenyl acetate and on microbial populations in a biogas digester. J Biosci Bioeng 114:446–452

    Article  CAS  Google Scholar 

  • Kendall MM, Boone DR (2006) The order Methanosarcinales. Prokaryotes 3:244–256

    Article  Google Scholar 

  • Kim MD, Song M, Jo M, Shin SG, Khim JH, Hwang S (2010) Growth condition and bacterial community for maximum hydrolysis of suspended organic materials in anaerobic digestion of food waste-recycling wastewater. Appl Microbiol Biotechnol 85:1611–1618

    Article  CAS  Google Scholar 

  • Klocke M, Mähnert P, Mundt K, Souidi K, Linke B (2007) Microbial community analysis of a biogas-producing completely stirred tank reactor fed continuously with fodder beet silage as mono-substrate. Syst Appl Microbiol 30:139–151

    Article  CAS  Google Scholar 

  • Krause L, Diaz NN, Edwards RA, Gartemann KH, Krömeke H, Neuweger H, Pühler A, Runte KJ, Schlüter A, Stoye J, Szczepanowski R, Tauch A, Goesmann A (2008) Taxonomic composition and gene content of a methane-producing microbial community isolated from a biogas reactor. J Biotechnol 136:91–101

    Article  CAS  Google Scholar 

  • Kröber M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehöver 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

    Article  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

    Article  CAS  Google Scholar 

  • Lomans BP, Maas R, Luderer R, Op den Camp HJM, Pol A, van der Drift C, Vogels GD (1999) Isolation and characterization of Methanomethylovorans hollandica gen. nov., sp. nov., isolated from freshwater sediment, a methylotrophic methanogen able to grow on dimethyl sulfide and methanethiol. Appl Environ Microbiol 65:3641–3650

    CAS  Google Scholar 

  • Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    Article  CAS  Google Scholar 

  • Maestrojuan GM, Boone DR (1991) Characterization of Methanosarcina barkeri MST and 227, Methanosarcina mazei S-6T, and Methanosarcina vacuolata Z-761T. Int J Syst Bacteriol 41:267–274

    Article  Google Scholar 

  • Morrison M, Miron J (2000) Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? FEMS Microbiol Lett 185:109–115

    CAS  Google Scholar 

  • Narihiro T, Sekiguchi Y (2007) Microbial communities in anaerobic digestion processes for waste and wastewater treatment: a microbiological update. Curr Opin Biotechnol 18:273–278

    Article  CAS  Google Scholar 

  • Ntaikou I, Gavala HN, Kornaros M, Lyberatos G (2008) Hydrogen production from sugars and sweet sorghum biomass using Ruminococcus albus. Int J Hydrog Energy 33:1153–1163

    CAS  Google Scholar 

  • O’Reilly J, Lee C, Collins G, Chinalia F, Mahony T, O’Flaherty V (2009) Quantitative and qualitative analysis of methanogenic communities in mesophilically and psychrophilically cultivated anaerobic granular biofilms. Water Res 43:3365–3374

    Article  Google Scholar 

  • Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. Publisher Univ Oulu Comput Serv Cent 83:1–43

    Google Scholar 

  • Ollivier BM, Mah RA, Garcia JL, Boone DR (1986) Isolation and characterization of Methanogenium bourgense sp. nov. Int J Syst Bacteriol 36:297–301

    Article  CAS  Google Scholar 

  • Patel GB, Sprott GD (1990) Methanosaeta concilii gen. nov., sp. nov. (“Methanothrix concilii”) and Methanosaeta thermoacetophila nom. rev., comb. nov. Int J Syst Bacteriol 40:79–82

    Article  Google Scholar 

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

    Article  CAS  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

    Article  Google Scholar 

  • Sasaki K, Morita M, Hirano S, Ohmura N, Igarashi Y (2011) Decreasing ammonia inhibition in thermophilic methanogenic bioreactors using carbon fiber textiles. Appl Microbiol Biotechnol 90:1555–1561

    Article  CAS  Google Scholar 

  • Schnürer A, Nordberg A (2008) Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature. Water Sci Technol 57:735–740

    Article  Google Scholar 

  • Schnürer A, Schink B, Svensson BH (1996) Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 46:1145–1152

    Article  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

    Article  Google Scholar 

  • Sowers KR, Baron SF, Ferry JG (1984) Methanosarcina acetivorans sp. nov., an acetotrophic methane-producing bacterium isolated from marine sediments. Appl Environ Microbiol 47:971–978

    CAS  Google Scholar 

  • Steinberg LM, Regan JM (2009) mcrA-targeted real-time quantitative PCR method to examine methanogen communities. Appl Environ Microbiol 75:4435–4442

    Article  CAS  Google Scholar 

  • Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860

    Article  CAS  Google Scholar 

  • Westerholm M, Roos S, Schnürer A (2010) Syntrophaceticus schinkii gen. nov., sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from a mesophilic anaerobic filter. FEMS Microbiol Lett 309:100–104

    CAS  Google Scholar 

  • Westerholm M, Roos S, Schnürer A (2011) Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonia-enriched mesophilic methanogenic processes. Syst Appl Microbiol 34:260–266

    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

    Article  CAS  Google Scholar 

  • Ziganshin AM, Ziganshina EE, Kleinsteuber S, Pröter J, Ilinskaya ON (2012) Methanogenic community dynamics during anaerobic utilization of agricultural wastes. Acta Naturae 4:91–97

    CAS  Google Scholar 

  • Zinder SH, Sowers KR, Ferry JG (1985) Methanosarcina thermophila sp. nov., a thermophilic, acetotrophic, methane-producing bacterium. Int J Syst Bacteriol 35:522–523

    Article  Google Scholar 

  • Zverlov VV, Hiegl W, Köck DE, Kellermann J, Köllmeier T, Schwarz WH (2010) Hydrolytic bacteria in mesophilic and thermophilic degradation of plant biomass. Eng Life Sci 10:528–536

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge the technicians and students from the Department of Biochemical Conversion (DBFZ) for running the reactors and performing chemical analyses. We also thank Ute Lohse from the Department of Environmental Microbiology (UFZ) for technical assistance.

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Authors and Affiliations

  1. Department of Microbiology, Kazan (Volga Region) Federal University, Kazan, 420008, Russia

    Ayrat M. Ziganshin

  2. Department of Biochemical Conversion, Deutsches Biomasseforschungszentrum (DBFZ), Torgauer Str. 116, 04347, Leipzig, Germany

    Jan Liebetrau & Jürgen Pröter

  3. Department of Environmental Microbiology, Helmholtz Centre for Environmental Research (UFZ), Permoserstr. 15, 04318, Leipzig, Germany

    Sabine Kleinsteuber

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  1. Ayrat M. Ziganshin
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  2. Jan Liebetrau
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  4. Sabine Kleinsteuber
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Correspondence to Sabine Kleinsteuber.

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Ziganshin, A.M., Liebetrau, J., Pröter, J. et al. Microbial community structure and dynamics during anaerobic digestion of various agricultural waste materials. Appl Microbiol Biotechnol 97, 5161–5174 (2013). https://doi.org/10.1007/s00253-013-4867-0

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