Improved Methanogenic Communities for Biogas Production

  • Cristina Rossi Nakayama
  • Eduardo Dellosso Penteado
  • Rubens Tadeu Delgado Duarte
  • Admir José Giachini
  • Flávia Talarico Saia
Part of the Biofuel and Biorefinery Technologies book series (BBT, volume 9)


Last decade advances on methane microbial ecology in natural environments and man-made systems have introduced possibilities and challenges to biogas-producing processes. Mostly restricted to anaerobic environments, methanogens have also been detected in aerobic desertic soils, and their presence in extreme environments, such as hydrothermal vents, soda lakes, and Antarctic sediments, shows how ubiquitous and adapted they are to different environmental conditions. Most known methanogens belong to Euryarchaeota classes, producing methane from acetoclastic, hydrogenotrophic, or methylotrophic pathways. Recently discovered representatives in Thermoplasmata and Halobacteria classes, as well as in Bathyarchaeota and Vestretearchaeota, Phyla brought new insights on methanogenic diversity and their metabolic pathways. Biotechnological application of methanogens has been studied in bioreactors used for treatment of wastewater and waste. These bioreactors can be operated with acidogenesis and methanogenesis occurring in one stage or, with phase separation, acidogenesis followed by methanogenesis, with suspended and/or attached cells. Several factors have been studied to understand and optimize biogas production in bioreactors, such as temperature, organic load, and type of wastewater input. The biogas-producing communities received special attention following the development of metagenomics, metatranscriptomics, and single-cell genomic approaches. Coupled to the discovery of new methanogenic lineages, these methods revealed the complexity of microbial community structure and functions in both natural environments and bioreactors. However, a comprehensive view of these communities is still needed to improve current biogas-producing processes.


Biogas Methanogenic archaea Anaerobic digestion High-rate anaerobic bioreactor Biodiversity Ecology 


  1. Adam PS, Borrel G, Brochier-Armanet C, Gribaldo S (2017) The growing tree of archaea: new perspectives on their diversity, evolution and ecology. ISME J 11:2407–2425CrossRefGoogle Scholar
  2. Ahmad F, Sakamoto IK, Adorno MAT, et al (2018) Methane production from hydrogen peroxide assisted hydrothermal pretreatment of solid fraction sugarcane bagasse. Waste Biomass Valoriz 1–20Google Scholar
  3. Amani T, Nosrati M, Sreekrishnan TR (2010) Anaerobic digestion from the viewpoint of microbiological, chemical, and operational aspects—a review. Environ Rev 18:255–278CrossRefGoogle Scholar
  4. Amann R, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925Google Scholar
  5. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  6. Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847CrossRefGoogle Scholar
  7. Angle JC, Morin TH, Solden LM et al (2017) Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. Nat Commun 8:1–9.
  8. Antony CP, Colin Murrell J, Shouche YS (2012) Molecular diversity of methanogens and identification of Methanolobus sp. as active methylotrophic archaea in Lonar crater lake sediments. FEMS Microbiol Ecol 81:43–51CrossRefGoogle Scholar
  9. Aquino S, Mockaitis G, Pires EC (2014) Comparative study between a ABFSB and a APBB for digestion of vinasse. XI Simposio Latinoamericano de Digestión Anaerobia At, La Habana, CubaGoogle Scholar
  10. Araújo JC, Schneider RP (2008) DGGE with genomic DNA: suitable for detection of numerically important organisms but not for identification of the most abundant organisms. Water Res 42:5002–5010CrossRefGoogle Scholar
  11. Banach A, Ciesielski S, Bacza T, Pieczykolan M, Ziembińska-Buczyńska A (2018) Microbial community composition and methanogens’ biodiversity during a temperature shift in a methane fermentation chamber. Environ Technol (UK) 3330:1–12Google Scholar
  12. Banning N, Brock F, Fry JC, Parkes RJ, Hornibrook ERC, Weightman AJ (2005) Investigation of the methanogen population structure and activity in a brackish lake sediment. Environ Microbiol 7:947–960CrossRefGoogle Scholar
  13. Barbier BA, Dziduch I, Liebner S, Ganzert L, Lantuit H, Pollard W, Wagner D (2012) Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes. FEMS Microbiol Ecol 82:287–302CrossRefGoogle Scholar
  14. Beckmann S, Lueders T, Krüger M, von Netzer F, Engelen B, Cypionka H (2011) Acetogens and acetoclastic Methanosarcinales govern methane formation in abandoned coal mines. Appl Environ Microbiol 77:3749–3756. Scholar
  15. Bizic-Ionescu M, Klintzch T, Ionescu D, et al (2018) Widespread formation of methane by Cyanobacteria in aquatic and terrestrial environments. bioRxiv 398958Google Scholar
  16. Boetius A, Anesio AM, Deming JW et al (2015) Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat Rev Microbiol 13:677CrossRefGoogle Scholar
  17. Bonacker LG, Baudner S, Mörschel E, Böcher R, Thauer RK (1993) Properties of the two isoenzymes of methyl-coenzyme M reductase in Methanobacterium thermoautotrophicum. Eur J Biochem 217:587–595CrossRefGoogle Scholar
  18. Boon N, Windt W, Verstraete W, Top EM (2002) Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol Ecol 39:101–112Google Scholar
  19. Borrel G, Harris HMB, Tottey W et al (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 194:6944–6945CrossRefGoogle Scholar
  20. Bühligen F, Lucas R, Nikolausz M, Kleinsteuber S (2016) A T-RFLP database for the rapid profiling of methanogenic communities in anaerobic digesters. Anaerobe 39:114–116CrossRefGoogle Scholar
  21. Calli B, Mertoglu B, Tas N, Inanc B, Yenigun O, Ozturk I (2003) Investigation of variations in microbial diversity in anaerobic reactors treating landfill leachate. Water Sci Technol 48:105–112CrossRefGoogle Scholar
  22. Camiloti PR, Mockaitis G, Rodrigues JAD, Damianovic MHRZ, Foresti E, Zaiat M (2014) Innovative anaerobic bioreactor with fixed-structured bed (ABFSB) for simultaneous sulfate reduction and organic matter removal. J Chem Technol Biotechnol 89:1044–1050CrossRefGoogle Scholar
  23. Carr SA, Schubotz F, Dunbar RB, Mills CT, Dias R, Summons RE, Mandernack KW (2018) Acetoclastic Methanosaeta are dominant methanogens in organic-rich Antarctic marine sediments. ISME J 12:330–342CrossRefGoogle Scholar
  24. Casserly C, Erijman L (2003) Molecular monitoring of microbial diversity in an UASB reactor. Int Biodeterior Biodegrad 52:7–12CrossRefGoogle Scholar
  25. Centurion VB, Moura AGL, Delforno TP, Okada DY, Dos Santos VP, Varesche MBA, Oliveira VM (2018) Anaerobic co-digestion of commercial laundry wastewater and domestic sewage in a pilot-scale EGSB reactor: the influence of surfactant concentration on microbial diversity. Int Biodeterior Biodegrad 127:77–86CrossRefGoogle Scholar
  26. Chatila S, Amparo MR, Carvalho LS, Penteado ED, Tomita ISN, Santos-Neto AJ, Lima Gomes PCF, Zaiat M (2015) Sulfamethoxazole and ciprofloxacin removal using a horizontal-flow anaerobic immobilized biomass reactor. Environ Technol 37:847–853CrossRefGoogle Scholar
  27. Cheng H, Whang L, Yi T, Liu C, Lin T (2018) Pilot study of cold-rolling wastewater treatment using single-stage anaerobic fluidized membrane bioreactor. Bioresour Technol 263:418–424CrossRefGoogle Scholar
  28. Chew YM, Lye S, Salleh M, Yahya A (2018) 16S rRNA metagenomic analysis of the symbiotic community structures of bacteria in foregut, midgut, and hindgut of the wood-feeding termite Bulbitermes sp. Symbiosis 76:187–197CrossRefGoogle Scholar
  29. Chin KJ, Lukow T, Conrad R (1999) Effect of temperature on structure and function of the methanogenic archaeal community in an anoxic rice field soil. Appl Environ Microbiol 65:2341–2349Google Scholar
  30. Chojnacka A, Szczęsny P, Błaszczyk MK, Zielenkiewicz U, Detman A, Salamon A, Sikora A (2015) Noteworthy facts about a methane-producing microbial community processing acidic effluent from sugar beet molasses fermentation. PLoS ONE 10:1–23Google Scholar
  31. Chong S, Sen TK, Kayaalp A, Ang HM (2012) The performance enhancements of upflow anaerobic sludge blanket (UASB) reactors for domestic sludge treatment—a state-of-the-art review. Water Res 46:3434–3470CrossRefGoogle Scholar
  32. Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Advances 96:1–63. Scholar
  33. Costa KC, Leigh JA (2014) Metabolic versatility in methanogens. Curr Opin Biotechnol 29:70–75CrossRefGoogle Scholar
  34. Diekert G, Wohlfarth G (1994) Metabolism of homoacetogens. Antonie Van Leeuwenhoek 66:209–221. Scholar
  35. De Lima E, Silva MR, Correa RC, Sakamoto IK, Varesche MBA (2018) Microbial characterization of methanogenic iron-reducing consortium in reactors with polychlorinated biphenyls. Curr Microbiol 75:666–676CrossRefGoogle Scholar
  36. De Nardi I, Varesche MBA, Zaiat M, Foresti E (2002) Anaerobic degradation of BTEX in a packed-bed reactor. Water Sci Technol 45(10):175–180CrossRefGoogle Scholar
  37. De Vrieze J, Christiaens MER, Walraedt D et al (2017) Microbial community redundancy in anaerobic digestion drives process recovery after salinity exposure. Water Res 111:109–117CrossRefGoogle Scholar
  38. Delforno TP, Moura AGL, Okada DY, Varesche MBA (2014) Effect of biomass adaptation to the degradation of anionic surfactants in laundry wastewater using EGSB reactors. Bioresour Technol 154:114–121CrossRefGoogle Scholar
  39. 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(3):e00443. Scholar
  40. Deublein D, Steinhauser A (2008) Biogas from waste and renewable resources: an introduction, 1st edn. Wiley VCH Verlag GmbH & Co. KGaAGoogle Scholar
  41. Dridi B, Fardeau M-L, Ollivier B et al (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62:1902–1907CrossRefGoogle Scholar
  42. Dworkin MM, Falkow S, Rosenberg E et al (2006) The prokaryotes. In: Archaea and bacteria: firmicutes, vol 3. Actinomycetes. Springer, New York, NYGoogle Scholar
  43. Earl J, Hall G, Pickup RW, Ritchie DA, Edwards C (2003) Analysis of methanogen diversity in a hypereutrophic lake using PCR-RFLP analysis of mcr sequences. Microb Ecol 46:270–278CrossRefGoogle Scholar
  44. Ellermann J, Hedderich R, BoÈcher R, Thauer RK (1988) The final step in methane formation-investigations with highly purified methyl-CoM reductase (component-C) from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem 172:669–677CrossRefGoogle Scholar
  45. Enzmann F, Mayer F, Rother M, Holtmann D (2018) Methanogens: biochemical background and biotechnological applications. AMB Express 8:1CrossRefGoogle Scholar
  46. Ferraz ADN Jr, Koyama MH, Araújo MM Jr, Zaiat M (2016) Thermophilic anaerobic digestion of raw sugarcane vinasse. Renew Energy 89:245–252CrossRefGoogle Scholar
  47. Foresti E, Zaiat M, Cabral AKA, Del Nery V (1995) Horizontal-flow anaerobic immobilized sludge (hais) reactor for paper industry wastewater treatment. Braz J Chem Eng 12:235–239Google Scholar
  48. Fuess LT, Kiyuna LSM, Ferraz Júnior ADN, Persinoti GF, Squina FM , Garcia ML , Zaiat M (2017) Thermophilic anaerobic biodigestion of vinasse in combined acidogenic-methanogenic systems to enhance bioenergy recovery in first generation sugarcane biorefineries. Appl Energy 189:480–491. Scholar
  49. Ganzert L, Jurgens G, Münster U, Wagner D (2007) Methanogenic communities in permafrost-affected soils of the Laptev Sea coast, Siberian Arctic, characterized by 16S rRNA gene fingerprints. FEMS Microbiol Ecol 59:476–488CrossRefGoogle Scholar
  50. Garcia J, Patel BKC, Ollivier B (2000) Taxonomic, phylogenetic, and ecological diversity of methanogenic archaea. Archaea. Scholar
  51. García-Maldonado JQ, Bebout BM, Celis LB, López-Cortés A (2012) Phylogenetic diversity of methyl-coenzyme M reductase (mcrA) gene and methanogenesis from trimethylamine in hypersaline environments. Int Microbiol 15:33–41Google Scholar
  52. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359CrossRefGoogle Scholar
  53. Grohmann A, Fehrmann S, Vainshtein Y, Haag NL, Wiese F, Stevens P, Naegele HJ, Oechsner H, Hartsch T, Sohn K, Grumaz C (2018) Microbiome dynamics and adaptation of expression signatures during methane production failure and process recovery. Bioresour Technol 247:347–356CrossRefGoogle Scholar
  54. Gryta A, Oszust K, Brzezińska M, Ziemiński K, Bilińska-Wielgus N, Frąc M (2017) Methanogenic community composition in an organic waste mixture in an anaerobic bioreactor. Int Agrophys 31:327–338CrossRefGoogle Scholar
  55. Güllert S, Fischer MA, Turaev D, Noebauer B, Ilmberger N, Wemheuer B, Alawi M, Rattei T, Daniel R, Schmitz RA, Grundhoff A, Streit WR (2016) Deep metagenome and metatranscriptome analyses of microbial communities affiliated with an industrial biogas fermenter, a cow rumen, and elephant feces reveal major differences in carbohydrate hydrolysis strategies. Biotechnol Biofuels 9:121CrossRefGoogle Scholar
  56. Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol 69:5483–5491CrossRefGoogle Scholar
  57. Hernández M, Dumont MG, Yuan Q, Conrad R (2015) Different bacterial populations associated with the roots and rhizosphere of rice incorporate plant-derived carbon. Appl Environ Microbiol 81:2244–2253CrossRefGoogle Scholar
  58. Hulshoff Pol LW, De Castro Lopes SI, Lettinga G, Lens PNL (2004) Anaerobic sludge granulation. Water Res 38:1376–1389CrossRefGoogle Scholar
  59. Iino T, Tamaki H, Tamazawa S et al (2013) Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 28:244–250. Scholar
  60. 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:e14519CrossRefGoogle Scholar
  61. Jensen S, Øvreås L, Daae FL, Torsvik V (1998) Diversity in methane enrichments from agricultural soil revealed by DGGE separation of PCR amplified 16S rDNA fragments. FEMS Microbiol Ecol 26:17–26CrossRefGoogle Scholar
  62. Kallistova AY, Merkel AY, Tarnovetskii IY, Pimenov NV (2017) Methane formation and oxidation by prokaryotes. Microbiology 86:671–691CrossRefGoogle Scholar
  63. Kamke J, Kittelmann S, Soni P, Li Y, Tavendale M, Ganesh S, Janssen PH, Shi W, Froula J, Rubin EM, Attwood GT (2016) Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4:1–16CrossRefGoogle Scholar
  64. Karr EA, Ng JM, Belchik SM, Sattley WM, Madigan MT, Achenbach LA (2006) Biodiversity of methanogenic and other archaea in the permanently. Appl Environ Microbiol 72:1663–1666CrossRefGoogle Scholar
  65. Keyser M, Witthuhn RC, Lamprecht C, Coetzee MPA, Britz TJ (2006) PCR-based DGGE fingerprinting and identification of methanogens detected in three different types of UASB granules. Syst Appl Microbiol 29:77–84CrossRefGoogle Scholar
  66. Klocke M, Nettmann E, Bergmann I, Mundt K, Souidi K, Mumme J, Linke B (2008) Characterization of the methanogenic archaea within two-phase biogas reactor systems operated with plant biomass. Syst Appl Microbiol 31:190–205CrossRefGoogle Scholar
  67. Kouzuma A, Tsutsumi M, Ishii S et al (2017a) Non-autotrophic methanogens dominate in anaerobic digesters. Sci Rep 7:1510CrossRefGoogle Scholar
  68. Kouzuma A, Tsutsumi M, Ishii S, Ueno Y, Abe T, Watanabe K (2017b) Non-autotrophic methanogens dominate in anaerobic digesters. Sci Rep 7:1–13CrossRefGoogle Scholar
  69. Kovács E, Wirth R, Maroti G, Bagi Z, Rakhely G, Kovács KL (2013) Biogas production from protein-rich biomass: fed-batch anaerobic fermentation of casein and of pig blood and associated changes in microbial community composition. PLoS ONE 8:e77265CrossRefGoogle Scholar
  70. 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 136:91–101CrossRefGoogle Scholar
  71. 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 142:38–49CrossRefGoogle Scholar
  72. Kröninger L, Gottschling J, Deppenmeier U (2017) Growth characteristics of Methanomassiliicoccus luminyensis and expression of methyltransferase encoding genes. Archaea 2017Google Scholar
  73. Kudo Y (1997) Methanogen flora of paddy soils in Japan. FEMS Microbiol Ecol 22:39–48CrossRefGoogle Scholar
  74. Kymäläinen M, Lähde K, Arnold M, Kurola JM, Romantschuk M, Kautola H (2012) Biogasification of biowaste and sewage sludge—measurement of biogas quality. J Environ Manag 95:S122–S127CrossRefGoogle Scholar
  75. Lettinga G, Hulshoff Pol LW (1991) UASB-process design for various type of wastewater. Water Sci Technol 24:87–107CrossRefGoogle Scholar
  76. Li A, Chu Y, Wang X, Ren L, Yu J, Liu X, Yan J, Zhang L, Wu S, Li S (2013) A pyrosequencing-based metagenomic study of methane-producing microbial community in solid-state biogas reactor. Biotechnol Biofuels 6:3CrossRefGoogle Scholar
  77. Li H, Han K, Li Z, Zhang J, Li H, Huang Y, Shen L, Li Q, Wang Y (2018) Perfomance, granule conductivity and microbial community analysis of upflow anaerobic sludge blanket system (UASB) reactors from mesophilic to thermophilic operation. Biochem Eng J 133:59–65CrossRefGoogle Scholar
  78. Lima CAA, Ribeiro R, Foresti E, Zaiat M (2005) Morphological study of biomass during the start-up period of a fixed-bed anaerobic bioreactor treating domestic sewage. Braz Arch Biol Technol 48:841–849CrossRefGoogle Scholar
  79. Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189. Scholar
  80. Liu WT, Chan OC, Fang HHP (2002) Characterization of microbial community in granular sludge treating brewery wastewater. Water Res 36:1767–1775CrossRefGoogle Scholar
  81. Liu Y, Beer LL, Whitman WB (2012) Methanogens: a window into ancient sulfur metabolism. Trends Microbiol 20:251–258CrossRefGoogle Scholar
  82. Liu D, Nishida M, Takahashi T, Asakawa S (2018) Transcription of mcrA gene decreases upon prolonged non-flooding period in a methanogenic archaeal community of a paddy-upland rotational field soil. Microb Ecol 75:751–760CrossRefGoogle Scholar
  83. Lovley DR (2017) Happy together: microbial communities that hook up to swap electrons. ISME J 11:327–336. Scholar
  84. Lu X, Ni J, Zhen G, Kubota K, Li Y (2018) Response of morphology and microbial community structure of granules to influent COD/SO42− ratios in an upflow anaerobic sludge blanket (UASB) reactor treating starch wastewater. Bioresour Technol 256:456–465CrossRefGoogle Scholar
  85. Lucas R, Kuchenbuch A, Fetzer I, Harms H, Kleinsteuber S (2015) Long-term monitoring reveals stable and remarkably similar microbial communities in parallel full-scale biogas reactors digesting energy crops. FEMS Microbiol Ecol 91:1–11CrossRefGoogle Scholar
  86. Lueders T, Chin KJ, Conrad R, Friedrich M (2001) Molecular analyses of methyl-coenzyme M reductase α-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 3:194–204CrossRefGoogle Scholar
  87. Luo G, Xie L, Zhou Q, Angelidaki I (2011) Enhancement of bioenergy production from organic wastes by two-stage anaerobic hydrogen and methane production process. Bioresour Technol 102:8700–8706CrossRefGoogle Scholar
  88. Luo G, Fotidis IA, Angelidaki I (2016) Biotechnology for biofuels comparative analysis of taxonomic, functional, and metabolic patterns of microbiomes from 14 full-scale biogas reactors by metagenomic sequencing and radioisotopic analysis. Biotechnol Biofuels:1–12Google Scholar
  89. Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530CrossRefGoogle Scholar
  90. Lv Z, Leite AF, Harms H, Richnow HH, Liebetrau J, Nikolausz M (2014) Influences of the substrate feeding regime on methanogenic activity in biogas reactors approached by molecular and stable isotope methods. Anaerobe 29:91–99CrossRefGoogle Scholar
  91. Lynd LR, Weimer PJ, Van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577CrossRefGoogle Scholar
  92. Ma K, Conrad R, Lu Y (2012) Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil. Appl Environ Microbiol 78:445–454CrossRefGoogle Scholar
  93. Marchesi JR, Weightman AJ, Cragg BA, John Parkes R, Fry JC (2000) Methanogen and bacterial diversity and distribution in deep gas hydrate sediments from the Cascadia Margin as revealed by 16S rRNA molecular analysis. FEMS Microbiol Ecol 34:221–228CrossRefGoogle Scholar
  94. Martin W, Baross J, Kelley D, Russell MJ (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol 6:805CrossRefGoogle Scholar
  95. Meng LW, Li XK, Wang ST, Liu LL, Ma KL, Zhang J (2017) The Long-term impact of cefalexin on organic substrat degradation and microbial community structure in EGSB system. Chemosphere 184:215–223CrossRefGoogle Scholar
  96. Meyer KM, Klein AM, Rodrigues JLM, Nüsslein K, Tringe SG, Mirza BS, Tiedje JM, Bohannan BJM (2017) Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms. Mol Ecol 26:1547–1556CrossRefGoogle Scholar
  97. Mirzoyan N, Gross A (2013) Use of UASB reactors for brackish aquaculture sludge digestion under different conditions. Water Res 47:2843–2850CrossRefGoogle Scholar
  98. Mockaitis G, Pantoja JLR, Rodrigues JAD, Foresti E, Zaiat M (2014) Continuous anaerobic bioreactor with a fixed-structure bed (ABFSB) for wastewater treatment with low solids and low applied organic loading content. Bioprocess Biosyst Eng 37:1361–1368CrossRefGoogle Scholar
  99. Moissl-Eichinger C, Pausan M, Taffner J, et al (2018) Archaea are interactive components of complex microbiomes. Trends Microbiol 26:70–85. Scholar
  100. Mondav R, Woodcroft BJ, Kim E-H et al (2014) Discovery of a novel methanogen prevalent in thawing permafrost. Nat Commun 5:3212CrossRefGoogle Scholar
  101. Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37:384–406CrossRefGoogle Scholar
  102. Morris RL, Tale VP, Mathai PP, Zitomer DH, Maki JS (2016) mcrA Gene abundance correlates with hydrogenotrophic methane production rates in full-scale anaerobic waste treatment systems. Lett Appl Microbiol 62:111–118CrossRefGoogle Scholar
  103. 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 Microb 59:695–700Google Scholar
  104. Na JG, Lee MK, Yun YM, Moon C, Kim MS, Kim DH (2016) Microbial community analysis of anaerobic granules in phenol degrading UASB by next generation sequencing. Biochem Eng J 112:241–248CrossRefGoogle Scholar
  105. Nakayama CR, Kuhn E, Araújo ACV, Alvalá PC, Ferreira WJ, Vazoller RF, Pellizari VH (2011) Revealing archaeal diversity patterns and methane fluxes in Admiralty Bay, King George Island, and their association to Brazilian Antarctic Station activities. Deep Sea Res Part II Top Stud Oceanogr 58:128–138CrossRefGoogle Scholar
  106. Nettmann E, Bergmann I, Mundt K, Linke B, Klocke M (2008) Archaea diversity within a commercial biogas plant utilizing herbal biomass determined by 16S rDNA and mcrA analysis. J Appl Microbiol 105:1835–1850CrossRefGoogle Scholar
  107. Nikolausz M, Walter RFH, Sträuber H, Liebetrau J, Schmidt T, Kleinsteuber S, Bratfisch F, Günther U, Richnow HH (2013) Evaluation of stable isotope fingerprinting techniques for the assessment of the predominant methanogenic pathways in anaerobic digesters. Appl Microbiol Biotechnol 97:2251–2262CrossRefGoogle Scholar
  108. Nolla-Ardèvol V, Peces M, Strous M, Tegetmeyer HE (2015) Metagenome from a Spirulina digesting biogas reactor: analysis via binning of contigs and classification of short reads. BMC Microbiol 15:1–16CrossRefGoogle Scholar
  109. Nölling J, Elfner A, Palmer JR, Steigerwald VJ, Pihl TD, Lake JA, Reeve JN (1996) Phylogeny of Methanopyrus kandleri based on methyl coenzyme M reductase operons. Int J Syst Bacteriol 46:1170–1173CrossRefGoogle Scholar
  110. Oliveira SVWB, Moraes EM, Adorno MAT, Varesche MBA, Foresti E, Zaiat M (2004) Formaldehyde degradation in an anaerobic packed bed bioreactor. Water Res 38:1685–1694CrossRefGoogle Scholar
  111. Park J, Park J, Je H, Jun W, Jin K (2018) Metagenomic insight into methanogenic reactors promoting direct interspecies electron transfer via granular activated carbon. Bioresour Technol 259:414–422CrossRefGoogle Scholar
  112. Popp D, Schrader S, Kleinsteuber S, Harms H, Sträuber H (2015) Biogas production from coumarin-rich plants—inhibition by coumarin and recovery by adaptation of the bacterial community. FEMS Microbiol Ecol 91:fiv103CrossRefGoogle Scholar
  113. 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 79:785–799CrossRefGoogle Scholar
  114. Repeta DJ, Ferrón S, Sosa OA et al (2016) Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nat Geosci 9:884CrossRefGoogle Scholar
  115. Reveillaud J, Reddington E, McDermott J, Algar C, Meyer JL, Sylva S, Seewald J, German CR, Huber JA (2016) Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman rise. Environ Microbiol 18:1970–1987CrossRefGoogle Scholar
  116. Ribeiro R, Varesche MBA, Foresti E, Zaiat M (2003) Influence of extracellular polymeric substances on anaerobic biofilms supported by polyurethane foam matrices. Environ Eng Sci 20:249–255CrossRefGoogle Scholar
  117. Riesenfeld CS, Schloss PD, Handelsman J (2004) Metagenomics: genomic analysis of microbial communities. Annu Rev Genet 38:525–552CrossRefGoogle Scholar
  118. Rotaru A-E, Shrestha PM, Liu F et al (2014a) A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci 7:408–415CrossRefGoogle Scholar
  119. Rotaru A-E, Shrestha PM, Liu F, et al (2014) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol:AEM-00895Google Scholar
  120. Saia FT, Damianovic MHZ, Cattony EB, Brucha G, Foresti E, Vazoller RF (2007) Anaerobic biodegradation of pentachlorophenol in a fixed-film reactor inoculated with polluted sediment from Santos São Vicente Estuary, Brazil. Appl Microbiol Biotechnol 75:665–672CrossRefGoogle Scholar
  121. Saia FT, Araujo AC, Nakayama CR das Graças DA, Chaparro JP, Andreote F, Taketani R, Piza F, Silva A, Pellizari VH, Soares I, Manfio G, Vazoller RF (2011) Archaea diversity in Brazilian aquatic ecosystems. In: Archaea structure habitats ecological significance. Nov Sci Publ, New York, pp 95–120Google Scholar
  122. Sakai S, Imachi H, Hanada S et al (2008) Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage ‘Rice Cluster I’, and proposal of the new archaeal order Methanocellales ord. nov. Int J Syst Evol Microbiol 58:929–936CrossRefGoogle Scholar
  123. 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
  124. Seghezzo L, Zeeman G, Van Liel J, Hamelers HVM, Lettinga G (1998) A review: the anaerobic treatment of sewage in UASB and EGSB reactor. Bioresour Technol 65:175–190CrossRefGoogle Scholar
  125. Semrau JD (2011) Current knowledge of microbial community structures in landfills and its cover soils. Appl Microbiol Biotechnol 89:961–969CrossRefGoogle Scholar
  126. Singh-Wissmann K, Ingram-Smith C, Miles RD, Ferry JG (1998) Identification of essential glutamates in the acetate kinase from Methanosarcina thermophila. J Bacteriol 180:1129–1134Google Scholar
  127. Skillman LC, Evans PN, Strömpl C, Joblin KN (2006) 16S rDNA directed PCR primers and detection of methanogens in the bovine rumen. Lett Appl Microbiol 42:222–228CrossRefGoogle Scholar
  128. Soares LA, Rabelo CABS, Sakamoto IK, Delforno TP, Silva EL, Varesche MBA (2018) Metagenomic analysis and optimization of hydrogen production from sugarcane bagasse. Biomass Bioenerg 117:78–85CrossRefGoogle Scholar
  129. Solli L, Havelsrud OE, Horn SJ, Rike AG (2014) A metagenomic study of the microbial communities in four parallel biogas reactors. Biotechnol Biofuels 7:146CrossRefGoogle Scholar
  130. Song L, Wang Y, Tang W, Lei Y (2015) Archaeal community diversity in municipal waste landfill sites. Appl Microbiol Biotechnol 99:6125–6137CrossRefGoogle Scholar
  131. Sorokin DY, Makarova KS, Abbas B et al (2017) Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nat Microbiol 2:17081CrossRefGoogle Scholar
  132. Spang A, Caceres EF, Ettema TJG (2017) Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357(80):eaaf3883CrossRefGoogle Scholar
  133. Springer E, Sachs MS, Woese CR, Boone DR (1995) Partial gene sequences for the A subunit of methyl-coenzyme M reductase (mcrI) as a phylogenetic tool for the family Methanosarcinaceae. Int J Syst Bacteriol 45:554–559CrossRefGoogle Scholar
  134. Staley JT, Konopka A (1985) Microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346CrossRefGoogle Scholar
  135. Stolze Y, Zakrzewski M, Maus I, Eikmeyer F, Jaenicke S, Rottmann N, Siebner C, Pühler A, Schlüter A (2015) Comparative metagenomics of biogas-producing microbial communities from production-scale biogas plants operating under wet or dry fermentation conditions. Biotechnol Biofuels 8:14CrossRefGoogle Scholar
  136. Tabatabaei M, Zakaria MR, Rahim RA, Wright ADG, Shirai Y, Abdullah N, Sakai K, Ikeno S, Mori M, Kazunori N, Sulaiman A, Hassan MA (2009) PCR-based DGGE and FISH analysis of methanogens in an anaerobic closed digester tank for treating palm oil mill effluent. Electron J Biotechnol 12:1–12CrossRefGoogle Scholar
  137. Takai K, Nakamura K, Toki T et al (2008) Cell proliferation at 122 C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Natl Acad Sci 105:10949–10954CrossRefGoogle Scholar
  138. Tanikkul P, Phalakornkule C, Champreda V (2016) Comparative granular characteristics of mesophilic and thermophilic UASB producing biogas from palm oil mill effluent. Chem Eng J 50:205–210Google Scholar
  139. Thauer RK, Kaster A-K, Seedorf H et al (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591. Scholar
  140. Thomas T, Gilbert J, Meyer F (2012) Metagenomics—a guide from sampling to data analysis. Microb Inform Exp 2:3CrossRefGoogle Scholar
  141. Timmers PHA, Welte CU, Koehorst JJ, et al (2017) Reverse methanogenesis and respiration in methanotrophic archaea. Archaea 2017. Scholar
  142. Tiwari MK, Guha S, Harendranath CS, Tripathi S (2005) Enhanced granulation by natural ionic polymer additives in UASB reactor treating low-strength wastewater. Water Res 39:3801–3810CrossRefGoogle Scholar
  143. Vavourakis CD, Andrei A, Mehrshad M, Ghai R, Sorokin DY, Muyzer G (2018) A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments. Microbiome 6:168CrossRefGoogle Scholar
  144. Von Sperling M, Chernicharo CAL (2005) Biological wastewater treatment in warm climate regions. IWA PublishingGoogle Scholar
  145. Wang G, Watanabe T, Jin J, Liu X, Kimura M, Asakawa S (2010) Methanogenic archaeal communities in paddy field soils in north-east China as evaluated by PCR-DGGE, sequencing and real-time PCR analyses. Soil Sci Plant Nutr 56:831–838CrossRefGoogle Scholar
  146. Wang J, Liu H, Fu B, et al (2013) Trophic link between syntrophic acetogens and homoacetogens during the anaerobic acidogenic fermentation of sewage sludge. Biochem Eng J 70:1–8. Scholar
  147. West WE, Coloso JJ, Jones SE (2012) Effects of algal and terrestrial carbon on methane production rates and methanogen community structure in a temperate lake sediment. Freshw Biol 57:949–955CrossRefGoogle Scholar
  148. Whalen SC (2005) Biogeochemistry of methane exchange between natural wetlands and the atmosphere. Environ Eng Sci 22:73–94CrossRefGoogle Scholar
  149. Wirth R, Lakatos G, Bojti T, Maróti G, Bagi Z, Kis M, Kovács A, Acs N, Rakhely G, Kovács KL (2015) Metagenome changes in the mesophilic biogas-producing community during fermentation of the green alga Scenedesmus obliquus. J Biotechnol 215:52–61CrossRefGoogle Scholar
  150. Wong MT, Zhang D, Li J, Hui RK, Tun HM, Brar MS, Park TJ, Chen Y, Leung FC (2013) Towards a metagenomic understanding on enhanced biomethane production from waste activated sludge after pH 10 pretreatment. Biotechnol Biofuels 6:38CrossRefGoogle Scholar
  151. Yadav S, Kundu S, Ghosh SK, Maitra SS (2015) Molecular analysis of methanogen richness in landfill and marshland targeting 16S rDNA sequences. Archaea 2015:1–9CrossRefGoogle Scholar
  152. Yan Z, Ferry JG (2018) Electron bifurcation and confurcation in methanogenesis and reverse methanogenesis. Front Microbiol 9:1322.
  153. Yang Y, Yu K, Xia Y, Lau FT, Tang DT, Fung WC, Fang HH, Zhang T (2014) Metagenomic analysis of sludge from full-scale anaerobic digesters operated in municipal wastewater treatment plants. Appl Microbiol Biotechnol 98:5709–5718CrossRefGoogle Scholar
  154. Yu D, Kurola JM, Lähde K, Kymäläinen M, Sinkkonen A, Romantschuk M (2014) Biogas production and methanogenic archaeal community in mesophilic and thermophilic anaerobic co-digestion processes. J Environ Manag 143:54–60CrossRefGoogle Scholar
  155. Zaiat M, Vieira LGT, Foresti E (1997) Spatial and temporal variations in monitoring performance parameters in horizontal-flow anaerobic immobilized sludge (HAIS) reactor treating synthetic substrate. Water Res 31:1760–1766CrossRefGoogle Scholar
  156. Zakrzewski M, Goesmann A, Jaenicke S, Jünemann S, Eikmeyer F, Szczepanowski R, Al-Soud WA, Sørensen S, Pühler A, Schlüter A (2012) Profiling of the metabolically active community from a production-scale biogas plant by means of high-throughput metatranscriptome sequencing. J Biotechnol 158:248–258CrossRefGoogle Scholar
  157. Zhang C, Yuan Q, Lu Y (2014) Inhibitory effects of ammonia on methanogen mcrA transcripts in anaerobic digester sludge. FEMS Microbiol Ecol 87:368–377CrossRefGoogle Scholar
  158. Zhang C, Ang A, Jia J, Zhao L, Song W (2017) Effect of parameters on anaerobic digestion EGSB reactor for producing biogas. Procedia Eng 205:3749–3754CrossRefGoogle Scholar
  159. Zhou J, He Z, Yang Y, Deng Y, Tringe SG, Alverez-Cohen L (2015) High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio 6:e02288CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Cristina Rossi Nakayama
    • 1
  • Eduardo Dellosso Penteado
    • 3
  • Rubens Tadeu Delgado Duarte
    • 2
  • Admir José Giachini
    • 2
  • Flávia Talarico Saia
    • 3
  1. 1.Department of Environmental SciencesFederal University of São PauloDiademaBrazil
  2. 2.Department of Microbiology, Immunology and Parasitology (MIP)Federal University of Santa Catarina—UFSC, CCB-MIPFlorianópolisBrazil
  3. 3.Department of Marine ScienceFederal University of São PauloSantosBrazil

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