Coupling Syntrophic Acetate Oxidation and Anaerobic Ammonium Oxidation When Treating Nitrogen-Rich Organic Wastes for Energy Recovery and Nitrogen Removal: Overview and Prospects

  • Albert MagríEmail author
  • Belén Fernández
  • Francesc X. Prenafeta-Boldú
  • Josep Ruiz-Sánchez
Part of the Biofuel and Biorefinery Technologies book series (BBT, volume 9)


There is high interest in applying anaerobic digestion to organic wastes for the recovery of biogas as a renewable energy source. In the case of protein-rich residues, the performance of anaerobic digesters might be affected by the accumulation of ammonia and volatile fatty acids. High concentrations of these compounds impact negatively on the activity of the acetotrophic methanogenic archaea (AMA). This limitation can be overcome by promoting the enrichment within digesters of syntrophic acetate-oxidizing bacteria (SAOB) in conjunction with certain groups of hydrogenotrophic methanogenic archaea (HMA). These two microbial populations have a relatively high tolerance towards the aforementioned inhibitory compounds. Hence, when the partial pressure of hydrogen is low enough, SAOB metabolize acetate to carbon dioxide and hydrogen, which are syntrophically consumed by HMA. Once the organic matter has been biodegraded, the remaining nitrogen can be biologically removed from digester supernatants by the anaerobic ammonium oxidation (anammox). This pathway consists of the simultaneous conversion of ammonium and nitrite to (di)nitrogen gas, and, therefore, a previous partial oxidation of ammonium to nitrite under aerobic conditions is required. Interestingly, the whole process constitutes a completely autotrophic nitrogen removal strategy. This chapter compiles the current knowledge on the syntrophic oxidation of acetate and on the anaerobic oxidation of ammonium, mostly focusing on technological aspects in view of a sequential bioreactor implementation.


Anaerobic digestion Syntrophic acetate oxidation Methanogenesis Biogas Autotrophic nitrogen removal Partial nitritation Anaerobic ammonium oxidation 



This overview has been carried out within the framework of the research project PIONER, financially supported by the Spanish Government [MINECO-INIA, RTA2015-00093-00-00], on the integration of SAO and anammox for treating N-rich organic wastes. The authors are members of the Consolidated Research Group TERRA [Generalitat de Catalunya, 2017 SGR 1290]. Josep Ruiz Sánchez received a grant from the Spanish Government [FPI-INIA RTA2012-00098-00-00]. IRTA thanks the CERCA Program of the Generalitat de Catalunya for the financial support.


  1. Abbasi T, Tauseef SM, Abbasi SA (2012) Biogas energy. SpringerBriefs in environmental science 2. Springer, New York, USACrossRefGoogle Scholar
  2. Abma WR, Driessen W, Haarhuis R et al (2010) Upgrading of sewage treatment plant by sustainable and cost-effective separate treatment of industrial wastewater. Water Sci Technol 61:1715–1722CrossRefGoogle Scholar
  3. Abouelenien F, Nakashimada Y, Nishio N (2009) Dry mesophilic fermentation of chicken manure for production of methane by repeated batch culture. J Biosci Bioeng 107:293–295CrossRefGoogle Scholar
  4. Ahammad SZ, Davenport RJ, Read LF et al (2013) Rational immobilization of methanogens in high cell density bioreactors. RSC Adv 3:774–781CrossRefGoogle Scholar
  5. Anthonisen AC, Loehr RC, Prakasam TBS et al (1976) Inhibition of nitrification by ammonia and nitrous acid. J Water Pollut Control Fed 48:835–852Google Scholar
  6. Baek G, Jung H, Kim J et al (2017) A long-term study on the effect of magnetite supplementation in continuous anaerobic digestion of dairy effluent—magnetic separation and recycling of magnetite. Bioresour Technol 241:830–840CrossRefGoogle Scholar
  7. Balk M, Weijma J, Stams AJM (2002) Thermotoga lettingae sp. nov., a novel thermophilic, methanol-degrading bacterium isolated from a thermophilic anaerobic reactor. Int J Syst Evol Microbiol 52:1361–1368Google Scholar
  8. Banks CJ, Zhang Y, Jiang Y et al (2012) Trace element requirements for stable food waste digestion at elevated ammonia concentrations. Bioresour Technol 104:127–135CrossRefGoogle Scholar
  9. Batstone DJ, Keller J, Angelidaki I et al (2002) Anaerobic digestion model no. 1 (ADM1). Scientific and technical report 13. IWA Publishing, LondonGoogle Scholar
  10. Borja R, Banks CJ, Wang Z et al (1998) Anaerobic digestion of slaughterhouse wastewater using a combination sludge blanket and filter arrangement in a single reactor. Bioresour Technol 65:125–133CrossRefGoogle Scholar
  11. Calli B, Mertoglu B, Inanc B et al (2005) Methanogenic diversity in anaerobic bioreactors under extremely high ammonia levels. Enzyme Microb Technol 37:448–455CrossRefGoogle Scholar
  12. Campos JL, Valenzuela-Heredia D, Pedrouso A et al (2016) Greenhouse gases emissions from wastewater treatment plants: minimization, treatment, and prevention. J Chem. ID 3796352. Scholar
  13. Cao Y, van Loosdrecht MCM, Daigger GT (2017) Mainstream partial nitritation-anammox in municipal wastewater treatment: status, bottlenecks, and further studies. Appl Microbiol Biotechnol 101:1365–1383CrossRefGoogle Scholar
  14. Capson-Tojo G, Moscoviz R, Ruiz D et al (2018) Addition of granular activated carbon and trace elements to favor volatile fatty acid consumption during anaerobic digestion of food waste. Bioresour Technol 260:157–168CrossRefGoogle Scholar
  15. Chauhan A, Ogram A (2005) Evaluation of support matrices for immobilization of anaerobic consortia for efficient carbon cycling in waste regeneration. Biochem Biophys Res Commun 327:884–893CrossRefGoogle Scholar
  16. Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: A review. Bioresour Technol 99:4044–4064CrossRefGoogle Scholar
  17. Connan R, Dabert P, Khalil H et al (2016) Batch enrichment of anammox bacteria and study of the underlying microbial community dynamics. Chem Eng J 297:217–228CrossRefGoogle Scholar
  18. Connan R, Dabert P, Le Roux S et al (2017) Characterization of a combined batch-continuous procedure for the culture of anammox biomass. Ecol Eng 106:231–241CrossRefGoogle Scholar
  19. Connan R, Dabert P, Moya-Espinosa M et al (2018) Coupling of partial nitritation and anammox in two- and one-stage systems: process operation, N2O emission and microbial community. J Clean Prod 203:559–573CrossRefGoogle Scholar
  20. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202CrossRefGoogle Scholar
  21. Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752CrossRefGoogle Scholar
  22. Costa A, Tangorra FM, Zaninelli M et al (2016) Evaluating an e-nose ability to detect biogas plant efficiency: a case study. Ital J Anim Sci 15:116–123CrossRefGoogle Scholar
  23. Cruz-Viggi C, Rossetti S, Fazi S et al (2014) Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ Sci Technol 48:7536–7543CrossRefGoogle Scholar
  24. Cuetos MJ, Martinez EJ, Moreno R et al (2017) Enhancing anaerobic digestion of poultry blood using activated carbon. J Adv Res 8:297–307CrossRefGoogle Scholar
  25. Daigger GT, Sanjines P, Pallansch K et al (2011) Implementation of a full-scale anammox-based facility to treat an anaerobic digestion sidestream at the Alexandria sanitation authority water resource facility. Water Pract Technol 6.
  26. de Almeida NM, Maalcke WJ, Keltjens JT et al (2011) Proteins and protein complexes involved in the biochemical reactions of anaerobic ammonium-oxidizing bacteria. Biochem Soc Trans 39:303–308CrossRefGoogle Scholar
  27. De Prá MC, Kunz A, Bortoli M et al (2012) Simultaneous removal of TOC and TSS in swine wastewater using the partial nitritation process. J Chem Technol Biotechnol 87:1641–1647CrossRefGoogle Scholar
  28. De Vrieze J, Hennebel T, Boon N et al (2012) Methanosarcina: the rediscovered methanogen for heavy duty biomethanation. Bioresour Technol 112:1–9CrossRefGoogle Scholar
  29. Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Bio-Technol 7:173–190CrossRefGoogle Scholar
  30. Dosta J, Fernández I, Vázquez-Padín JR et al (2008) Short- and long-term effects of temperature on the Anammox process. J Hazard Mat 154:688–693CrossRefGoogle Scholar
  31. Dytczak MA, Londry KL, Oleszkiewicz JA (2008) Nitrifying genera in activated sludge may influence nitrification rates. Water Environ Res 80:388–396CrossRefGoogle Scholar
  32. Ek A, Hallin S, Vallin L et al (2011) Slaughterhouse waste co-digestion—experiences from 15 years of full-scale operation. In: Proceedings of the world renewable energy congress. Linköping University, Linköping, Sweden, 8–13 May 2011Google Scholar
  33. Ellison WJ, Pedarros-Caubet F, Caubet R (2007) Automatic and rapid measurement of microbial suspension growth parameters: application to the evaluation of effector agents. J Rapid Methods Autom Microbiol 15:369–410CrossRefGoogle Scholar
  34. Feitkenhauer H, von Sachs J, Meyer U (2002) On-line titration of volatile fatty acids for the process control of anaerobic digestion plants. Water Res 36:212–218CrossRefGoogle Scholar
  35. Flemming H-C, Wingender J, Szewzyk U et al (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575CrossRefGoogle Scholar
  36. Fotidis IA, Karakashev D, Kotsopoulos TA et al (2013) Effect of ammonium and acetate on methanogenic pathway and methanogenic community composition. FEMS Microbiol Ecol 83:38–48CrossRefGoogle Scholar
  37. Fotidis IA, Karakashev D, Angelidaki I (2014) The dominant acetate degradation pathway/methanogenic composition in full-scale anaerobic digesters operating under different ammonia levels. Int J Environ Sci Technol 11:2087–2094CrossRefGoogle Scholar
  38. Furukawa K, Inatomi Y, Qiao S et al (2009) Innovative treatment system for digester liquor using anammox process. Bioresour Technol 100:5437–5443CrossRefGoogle Scholar
  39. Fux C, Boehler M, Huber P et al (2002) Biological treatment of ammonium-rich wastewater by partial nitritation and subsequent anaerobic ammonium oxidation (anammox) in a pilot plant. J Biotechnol 99:295–306CrossRefGoogle Scholar
  40. Gabarró J, González-Cárcamo P, Ruscalleda M et al (2014) Anoxic phases are the main N2O contributor in partial nitritation reactors treating high nitrogen loads with alternate aeration. Bioresour Technol 163:92–99CrossRefGoogle Scholar
  41. Gao S, Zhao M, Chen Y et al (2015) Tolerance response to in situ ammonia stress in a pilot-scale anaerobic digestion reactor for alleviating ammonia inhibition. Bioresour Technol 198:372–379CrossRefGoogle Scholar
  42. Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18:1049–1056CrossRefGoogle Scholar
  43. Geets J, Boon N, Verstraete W (2006) Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen fluctuations. FEMS Microbiol Ecol 58:1–13CrossRefGoogle Scholar
  44. Gehring T, Klang J, Niedermayr A et al (2015) Determination of methanogenic pathways through carbon isotope (δ13C) analysis for the two-stage anaerobic digestion of high-solids substrates. Environ Sci Technol 49:4705–4714CrossRefGoogle Scholar
  45. Gehring T, Niedermayr A, Berzio S et al (2016) Determination of the fractions of syntrophically oxidized acetate in a mesophilic methanogenic reactor through a 12C and 13C isotope-based kinetic model. Water Res 102:362–373CrossRefGoogle Scholar
  46. Giustinianovich EA, Campos J-L, Roeckel MD (2016) The presence of organic matter during autotrophic nitrogen removal: Problem or opportunity? Sep Purif Technol 166:102–108CrossRefGoogle Scholar
  47. Habouzit F, Hamelin J, Santa-Catalina G et al (2014) Biofilm development during the start-up period of anaerobic biofilm reactors: the biofilm Archaea community is highly dependent on the support material. Microb Biotechnol 7:257–264CrossRefGoogle Scholar
  48. Hansen KH, Angelidaki I, Ahring BK (1998) Anaerobic digestion of swine manure: Inhibition by ammonia. Water Res 32:5–12CrossRefGoogle Scholar
  49. Hansen KH, Angelidaki I, Ahring BK (1999) Improving thermophilic anaerobic digestion of swine manure. Water Res 33:1805–1810CrossRefGoogle Scholar
  50. Hao L-P, Lü F, He P-J et al (2011) Predominant contribution of syntrophic acetate oxidation to thermophilic methane formation at high acetate concentrations. Environ Sci Technol 45:508–513CrossRefGoogle Scholar
  51. Hao L, Lü F, Mazéas L et al (2015) Stable isotope probing of acetate fed anaerobic batch incubations shows a partial resistance of acetoclastic methanogenesis catalyzed by Methanosarcina to sudden increase of ammonia level. Water Res 69:90–99CrossRefGoogle Scholar
  52. Hattori S (2008) Syntrophic acetate-oxidizing microbes in methanogenic environments. Microbes Environ 23:118–127CrossRefGoogle Scholar
  53. Hattori S, Kamagata Y, Hanada S et al (2000) Thermacetogenium phaeum gen. nov., sp. nov., a strictly anaerobic, thermophilic, syntrophic acetate-oxidizing bacterium. Int J Syst Evol Microbiol 50:1601–1609CrossRefGoogle Scholar
  54. Hellman J, Ek A, Sundberg C et al (2010) Mechanisms of increased methane production through re-circulation of magnetic biomass carriers in an experimental continuously stirred tank reactor. In: AD12: 12th World Congress on anaerobic digestion, IWA, Guadalajara, Mexico, 31 Oct–4 Nov 2010Google Scholar
  55. Henze M, Harremoës P, Jansen JlC et al (1995) Wastewater treatment: biological and chemical processes. Springer, BerlinGoogle Scholar
  56. Ho DP, Jensen PD, Batstone DJ (2013) Methanosarcinaceae and acetate-oxidizing pathways dominate in high-rate thermophilic anaerobic digestion of waste-activated sludge. Appl Environ Microbiol 79:6491–6500CrossRefGoogle Scholar
  57. Holmes DE, Dang Y, Walker DJF et al (2016) The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microbial Genomics 2.
  58. Huang X-L, Gao D-W, Tao Y et al (2014) C2/C3 fatty acid stress on anammox consortia dominated by Candidatus Jettenia asiatica. Chem Eng J 253:402–407CrossRefGoogle Scholar
  59. Hunik JH, Hamelers HVM, Koster IW (1990) Growth-rate inhibition of acetoclastic methanogens by ammonia and pH in poultry manure digestion. Biol Wastes 32:285–297CrossRefGoogle Scholar
  60. Jaroszynski LW, Oleszkiewicz JA (2011) Autotrophic ammonium removal from reject water: partial nitrification and anammox in one-reactor versus two-reactor systems. Environ Technol 32:289–294CrossRefGoogle Scholar
  61. Jetten MSM, Stams AJM, Zehnder AJB (1992) Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Rev 88:181–198CrossRefGoogle Scholar
  62. Jia M, Castro-Barros CM, Winkler MKH et al (2018) Effect of organic matter on the performance and N2O emission of a granular sludge anammox reactor. Environ Sci Water Res Technol 4:1035–1046CrossRefGoogle Scholar
  63. Jimenez J, Latrille E, Harmand J et al (2015) Instrumentation and control of anaerobic digestion processes: a review and some research challenges. Rev Environ Sci Bio-Technol 14:615–648CrossRefGoogle Scholar
  64. Jin R-C, Yang G-F, Yu J-J et al (2012) The inhibition of the Anammox process: a review. Chem Eng J 197:67–79CrossRefGoogle Scholar
  65. Kampschreur MJ, Temmink H, Kleerebezem R et al (2009) Nitrous oxide emission during wastewater treatment. Water Res 43:4093–4103CrossRefGoogle Scholar
  66. Kato S, Yoshida R, Yamaguchi T et al (2014) The effects of elevated CO2 concentration on competitive interaction between aceticlastic and syntrophic methanogenesis in a model microbial consortium. Front Microbiol 5:575. Scholar
  67. Kayhanian M (1994) Performance of a high-solids anaerobic digestion process under various ammonia concentrations. J Chem Technol Biotechnol 59:349–352CrossRefGoogle Scholar
  68. Koster IW, Lettinga G (1984) The influence of ammonium-nitrogen on the specific activity of pelletized methanogenic sludge. Agric Wastes 9:205–216CrossRefGoogle Scholar
  69. Kothari R, Pandey AK, Kumar S et al (2014) Different aspects of dry anaerobic digestion for bio-energy: an overview. Renew Sustain Energy Rev 39:174–195CrossRefGoogle Scholar
  70. Kretzschmar J, Koch C, Liebetrau J et al (2017) Electroactive biofilms as sensor for volatile fatty acids: cross sensitivity, response dynamics, latency and stability. Sens Actuator B-Chem 241:466–472CrossRefGoogle Scholar
  71. Kumar M, Lin J-G (2010) Co-existence of anammox and denitrification for simultaneous nitrogen and carbon removal—strategies and issues. J Hazard Mat 178:1–9CrossRefGoogle Scholar
  72. Labatut RA, Angenent LT, Scott NR (2014) Conventional mesophilic vs. thermophilic anaerobic digestion: a trade-off between performance and stability? Water Res 53:249–258CrossRefGoogle Scholar
  73. Lackner S, Gilbert EM, Vlaeminck SE et al (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303CrossRefGoogle Scholar
  74. Lalov IG, Krysteva MA, Phelouzat J-L (2001) Improvement of biogas production from vinasse via covalently immobilized methanogens. Bioresour Technol 79:83–85CrossRefGoogle Scholar
  75. Leigh JA (2002) Evolution of energy metabolism. In: Staley JT, Reysenbach A-L (eds) Biodiversity of microbial life: foundation of earth’s biosphere. Wiley, New York, pp 103–120Google Scholar
  76. Li J, Elliott D, Nielsen M et al (2011) Long-term partial nitrification in an intermittently aerated sequencing batch reactor (SBR) treating ammonium-rich wastewater under controlled oxygen-limited conditions. Biochem Eng J 55:215–222CrossRefGoogle Scholar
  77. Li L-L, Tong Z-H, Fang C-Y et al (2015) Response of anaerobic granular sludge to single-wall carbon nanotube exposure. Water Res 70:1–8CrossRefGoogle Scholar
  78. Li Y, Zhang Y, Yang Y et al (2017) Potentially direct interspecies electron transfer of methanogenesis for syntrophic metabolism under sulfate reducing conditions with stainless steel. Bioresour Technol 234:303–309CrossRefGoogle Scholar
  79. Li J, Li J, Gao R et al (2018) A critical review of one-stage anammox processes for treating industrial wastewater: optimization strategies based on key functional microorganisms. Bioresour Technol 265:498–505CrossRefGoogle Scholar
  80. Liang B, Wang L-Y, Zhou Z et al (2016) High frequency of Thermodesulfovibrio spp. and Anaerolineaceae in association with Methanoculleus spp. in a long-term incubation of n-alkanes-degrading methanogenic enrichment culture. Front Microbiol 7:1431.
  81. Lin L, Wan C, Liu X et al (2013) Anaerobic digestion of swine manure under natural zeolite addition: VFA evolution, cation variation, and related microbial diversity. Appl Microbiol Biotechnol 97:10575–10583CrossRefGoogle Scholar
  82. Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann NY Acad Sci 1125:171–189CrossRefGoogle Scholar
  83. Liu F, Rotaru A-E, Shrestha PM et al (2015) Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ Microbiol 17:648–655CrossRefGoogle Scholar
  84. Lotti T, van der Star WRL, Kleerebezem R et al (2012) The effect of nitrite inhibition on the anammox process. Water Res 46:2559–2569CrossRefGoogle Scholar
  85. Lotti T, Kleerebezem R, Lubello C et al (2014) Physiological and kinetic characterization of a suspended cell anammox culture. Water Res 60:1–14CrossRefGoogle Scholar
  86. Lu T, George B, Zhao H et al (2016) A case study of coupling upflow anaerobic sludge blanket (UASB) and ANITATM Mox process to treat high-strength landfill leachate. Water Sci Technol 73:662–668CrossRefGoogle Scholar
  87. Lü F, Hao L, Guan D et al (2013) Synergetic stress of acids and ammonium on the shift in the methanogenic pathways during thermophilic anaerobic digestion of organics. Water Res 47:2297–2306CrossRefGoogle Scholar
  88. Lv Z, Hu M, Harms H et al (2014) Stable isotope composition of biogas allows early warning of complete process failure as a result of ammonia inhibition in anaerobic digesters. Bioresour Technol 167:251–259CrossRefGoogle Scholar
  89. Madsen M, Holm-Nielsen JB, Esbensen KH (2011) Monitoring of anaerobic digestion processes: A review perspective. Renew Sustain Energy Rev 15:3141–3155CrossRefGoogle Scholar
  90. Magrí A, Corominas L, López H et al (2007a) A model for the simulation of the SHARON process: pH as a key factor. Environ Technol 28:255–265CrossRefGoogle Scholar
  91. Magrí A, Sole-Mauri F, Colprim J et al (2007b) Evaluation of the SHARON process (partial nitritation in a chemostat) using simulation. Afinidad 64:378–383Google Scholar
  92. Magrí A, Vanotti MB, Szögi AA (2012a) Anammox sludge immobilized in polyvinyl alcohol (PVA) cryogel carriers. Bioresour Technol 114:231–240CrossRefGoogle Scholar
  93. Magrí A, Vanotti MB, Szögi AA et al (2012b) Partial nitritation of swine wastewater in view of its coupling with the anammox process. J Environ Qual 41:1989–2000CrossRefGoogle Scholar
  94. Magrí A, Béline F, Dabert P (2013) Feasibility and interest of the anammox process as treatment alternative for anaerobic digester supernatants in manure processing—An overview. J Environ Manage 131:170–184CrossRefGoogle Scholar
  95. Magrí A, Giovannini F, Connan R et al (2017) Nutrient management from biogas digester effluents: a bibliometric-based analysis of publications and patents. Int J Environ Sci Technol 14:1739–1756CrossRefGoogle Scholar
  96. Makádi M, Tomócsik A, Orosz V (2012) Digestate: a new nutrient source—review. In: Kumar S (ed) Biogas. InTech, Rijeka, pp 295–310Google Scholar
  97. Massara TM, Malamis S, Guisasola A et al (2017) A review on nitrous oxide (N2O) emissions during biological nutrient removal from municipal wastewater and sludge reject water. Sci Total Environ 596–597:106–123CrossRefGoogle Scholar
  98. Mata-Alvarez J, Dosta J, Romero-Güiza MS et al (2014) A critical review on anaerobic co-digestion achievements between 2010 and 2013. Renew Sustain Energy Rev 36:412–427CrossRefGoogle Scholar
  99. Matsui H, Kojima N, Tajima K (2008) Diversity of the formyltetrahydrofolate synthetase gene (fhs), a key enzyme for reductive acetogenesis, in the bovine rumen. Biosci Biotechnol Biochem 72:3273–3276CrossRefGoogle Scholar
  100. McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632CrossRefGoogle Scholar
  101. Morris BEL, Henneberger R, Huber H et al (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37:384–406CrossRefGoogle Scholar
  102. Mosbæk F, Kjeldal H, Mulat DG et al (2016) Identification of syntrophic acetate-oxidizing bacteria in anaerobic digesters by combined protein-based stable isotope probing and metagenomics. ISME J 10:2405–2418CrossRefGoogle Scholar
  103. Mosquera-Corral A, González F, Campos JL et al (2005) Partial nitrification in a SHARON reactor in the presence of salts and organic carbon compounds. Process Biochem 40:3109–3118CrossRefGoogle Scholar
  104. Müller V (2003) Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69:6345–6353CrossRefGoogle Scholar
  105. Müller B, Sun L, Schnürer A (2013) First insights into the syntrophic acetate-oxidizing bacteria—a genetic study. MicrobiologyOpen 2:35–53CrossRefGoogle Scholar
  106. Muñoz MA, Sanchez JM, Rodríguez-Maroto JM et al (1997) Methane production in anaerobic sludges supplemented with two support materials and different levels of acetate and sulphate. Water Res 31:1236–1242CrossRefGoogle Scholar
  107. Nagao N, Tajima N, Kawai M et al (2012) Maximum organic loading rate for the single-stage wet anaerobic digestion of food waste. Bioresour Technol 118:210–218CrossRefGoogle Scholar
  108. Ni S-Q, Ni J-Y, Hu D-L et al (2012) Effect of organic matter on the performance of granular anammox process. Bioresour Technol 110:701–705CrossRefGoogle Scholar
  109. Niu Q, Takemura Y, Kubota K et al (2015) Comparing mesophilic and thermophilic anaerobic digestion of chicken manure: microbial community dynamics and process resilience. Waste Manage 43:114–122CrossRefGoogle Scholar
  110. Nkoa R (2014) Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agron Sustain Dev 34:473–492CrossRefGoogle Scholar
  111. Nobu MK, Narihiro T, Rinke C et al (2015) Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J 9:1710–1722CrossRefGoogle Scholar
  112. Palacio-Barco E, Robert-Peillard F, Boudenne J-L et al (2010) On-line analysis of volatile fatty acids in anaerobic treatment processes. Anal Chim Acta 668:74–79CrossRefGoogle Scholar
  113. Pereira AD, Cabezas A, Etchebehere C et al (2017) Microbial communities in anammox reactors: a review. Environ Technol Rev 6:74–93CrossRefGoogle Scholar
  114. Pintucci C, Carballa M, Varga S et al (2017) The ManureEcoMine pilot installation: advanced integration of technologies for the management of organics and nutrients in livestock waste. Water Sci Technol 75:1281–1293CrossRefGoogle Scholar
  115. Poirier S, Madigou C, Bouchez T et al (2017) Improving anaerobic digestion with support media: Mitigation of ammonia inhibition and effect on microbial communities. Bioresour Technol 235:229–239CrossRefGoogle Scholar
  116. Polag D, May T, Müller L et al (2015) Online monitoring of stable carbon isotopes of methane in anaerobic digestion as a new tool for early warning of process instability. Bioresour Technol 197:161–170CrossRefGoogle Scholar
  117. Puyol D, Carvajal-Arroyo JM, Li GB et al (2014) High pH (and not free ammonia) is responsible for Anammox inhibition in mildly alkaline solutions with excess of ammonium. Biotechnol Lett 36:1981–1986CrossRefGoogle Scholar
  118. Pynaert K, Smets BF, Beheydt D et al (2004) Start-up of autotrophic nitrogen removal reactors via sequential biocatalyst addition. Environ Sci Technol 38:1228–1235CrossRefGoogle Scholar
  119. Qiao S, Nishiyama T, Fujii T et al (2012) Rapid startup and high rate nitrogen removal from anaerobic sludge digester liquor using a SNAP process. Biodegradation 23:157–164CrossRefGoogle Scholar
  120. Qureshi N, Annous BA, Ezeji TC et al (2005) Biofilm reactors for industrial bioconversion processes: employing potential of enhanced reaction rates. Microb Cell Fact 4:24. Scholar
  121. Ragsdale SW (2008) Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann NY Acad Sci 1125:129–136CrossRefGoogle Scholar
  122. Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898CrossRefGoogle Scholar
  123. Rajagopal R, Massé DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour Technol 143:632–641CrossRefGoogle Scholar
  124. Rajakumar R, Meenambal T, Saravanan PM et al (2012) Treatment of poultry slaughterhouse wastewater in hybrid upflow anaerobic sludge blanket reactor packed with pleated poly vinyl chloride rings. Bioresour Technol 103:116–122CrossRefGoogle Scholar
  125. Regueiro L, Carballa M, Lema JM (2016) Microbiome response to controlled shifts in ammonium and LCFA levels in co-digestion systems. J Biotechnol 220:35–44CrossRefGoogle Scholar
  126. Romero-Güiza MS, Astals S, Mata-Alvarez J et al (2015) Feasibility of coupling anaerobic digestion and struvite precipitation in the same reactor: evaluation of different magnesium sources. Chem Eng J 270:542–548CrossRefGoogle Scholar
  127. Romero-Güiza MS, Vila J, Mata-Alvarez J et al (2016) The role of additives on anaerobic digestion: a review. Renew Sustain Energy Rev 58:1486–1499CrossRefGoogle Scholar
  128. Rotaru A-E, Shrestha PM, Liu F et al (2014) 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. Scholar
  129. Rudnitskaya A, Legin A (2008) Sensor systems, electronic tongues and electronic noses, for the monitoring of biotechnological processes. J Ind Microbiol Biotechnol 35:443–451CrossRefGoogle Scholar
  130. Ruiz-Sánchez J, Campanaro S, Guivernau M et al (2018) Effect of ammonia on the active microbiome and metagenome from stable full-scale digesters. Bioresour Technol 250:513–522CrossRefGoogle Scholar
  131. Ruiz-Sánchez J, Guivernau M, Fernández B et al (2019) Functional biodiversity and plasticity of methanogenic biomass from a full-scale mesophilic anaerobic digester treating nitrogen-rich agricultural wastes. Sci Total Environ 649:760–769CrossRefGoogle Scholar
  132. Scaglione D, Tornotti G, Teli A et al (2013) Nitrification denitrification via nitrite in a pilot-scale SBR treating the liquid fraction of co-digested piggery/poultry manure and agro-wastes. Chem Eng J 228:935–943CrossRefGoogle Scholar
  133. Scaglione D, Ficara E, Corbellini V et al (2015) Autotrophic nitrogen removal by a two-step SBR process applied to mixed agro-digestate. Bioresour Technol 176:98–105CrossRefGoogle Scholar
  134. Schievano A, Colombo A, Cossettini A et al (2018) Single-chamber microbial fuel cells as on-line shock-sensors for volatile fatty acids in anaerobic digesters. Waste Manage 71:785–791CrossRefGoogle Scholar
  135. Schink B, Montag D, Keller A et al (2017) Hydrogen or formate: Alternative key players in methanogenic degradation. Environ Microbiol Rep 9:189–202CrossRefGoogle Scholar
  136. Schnürer A, Houwen FP, Svensson BH (1994) Mesophilic syntrophic acetate oxidation during methane formation by a triculture at high ammonium concentration. Arch Microbiol 162:70–74CrossRefGoogle Scholar
  137. 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 46:1145–1152CrossRefGoogle Scholar
  138. Schnürer A, Zellner G, Svensson BH (1999) Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microb Ecol 29:249–261CrossRefGoogle Scholar
  139. Schnürer A, Nordberg Å (2008) Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature. Water Sci Technol 57:735–740CrossRefGoogle Scholar
  140. Seuntjens D, Carvajal-Arroyo JM, Ruopp M et al (2018) High-resolution mapping and modeling of anammox recovery from recurrent oxygen exposure. Water Res 144:522–531CrossRefGoogle Scholar
  141. Siles JA, Brekelmans J, Martín MA et al (2010) Impact of ammonia and sulphate concentration on thermophilic anaerobic digestion. Bioresour Technol 101:9040–9048CrossRefGoogle Scholar
  142. Silva AJ, Hirasawa JS, Varesche MB et al (2006) Evaluation of support materials for the immobilization of sulfate-reducing bacteria and methanogenic archaea. Anaerobe 12:93–98CrossRefGoogle Scholar
  143. Stams AJM (1994) Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie Van Leeuwenhoek 66:271–294CrossRefGoogle Scholar
  144. St-Pierre B, Wright A-DG (2014) Comparative metagenomic analysis of bacterial populations in three full-scale mesophilic anaerobic manure digesters. Appl Microbiol Biotechnol 98:2709–2717CrossRefGoogle Scholar
  145. Strous M, van Gerven E, Kuenen JG et al (1997) Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (anammox) sludge. Appl Environ Microbiol 63:2446–2448Google Scholar
  146. Strous M, Heijnen JJ, Kuenen JG et al (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50:589–596CrossRefGoogle Scholar
  147. Sun L, Müller B, Westerholm M et al (2014) Syntrophic acetate oxidation in industrial CSTR biogas digesters. J Biotechnol 171:39–44CrossRefGoogle Scholar
  148. Sun C, Cao W, Banks CJ et al (2016) Biogas production from undiluted chicken manure and maize silage: a study of ammonia inhibition in high solids anaerobic digestion. Bioresour Technol 218:1215–1223CrossRefGoogle Scholar
  149. Sung S, Liu T (2003) Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere 53:43–52CrossRefGoogle Scholar
  150. Tang C-J, Zheng P, Wang C-H et al (2011) Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res 45:135–144CrossRefGoogle Scholar
  151. Tang C-J, Zheng P, Chai L-Y et al (2013) Thermodynamic and kinetic investigation of anaerobic bioprocesses on ANAMMOX under high organic conditions. Chem Eng J 230:149–157CrossRefGoogle Scholar
  152. Udert KM, Fux C, Münster M et al (2003) Nitrification and autotrophic denitrification of source-separated urine. Water Sci Technol 48(1):119–130CrossRefGoogle Scholar
  153. van der Star WRL, Abma WR, Blommers D et al (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41:4149–4163CrossRefGoogle Scholar
  154. van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON®-Anammox® process for treatment of ammonium rich wastewater. Water Sci Technol 44(1):153–160CrossRefGoogle Scholar
  155. Van Hulle SWH, Vandeweyer HJP, Meesschaert BD et al (2010) Engineering aspects and practical application of autotrophic nitrogen removal from nitrogen rich streams. Chem Eng J 162:1–20CrossRefGoogle Scholar
  156. van Niftrik L, Jetten MSM (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76:585–596CrossRefGoogle Scholar
  157. Vanwonterghem I, Evans PN, Parks DH et al (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1:16170. Scholar
  158. Vázquez-Padín JR, Morales N, Gutiérrez R et al (2014) Implications of full-scale implementation of an anammox-based process as post-treatment of a municipal anaerobic sludge digester operated with co-digestion. Water Sci Technol 69:1151–1158CrossRefGoogle Scholar
  159. Vlaeminck SE, Terada A, Smets BF et al (2009) Nitrogen removal from digested black water by one-stage partial nitritation and anammox. Environ Sci Technol 43:5035–5041CrossRefGoogle Scholar
  160. Vlaeminck SE, De Clippeleir H, Verstraete W (2012) Microbial resource management of one-stage partial nitritation/anammox. Microb Biotechnol 5:433–448CrossRefGoogle Scholar
  161. Walker M, Iyer K, Heaven S et al (2011) Ammonia removal in anaerobic digestion by biogas stripping: An evaluation of process alternatives using a first order rate model based on experimental findings. Chem Eng J 178:138–145CrossRefGoogle Scholar
  162. Wang H, Fotidis IA, Angelidaki I (2015) Ammonia effect on hydrogenotrophic methanogens and syntrophic acetate-oxidizing bacteria. FEMS Microbiol Ecol 91:fiv130. Scholar
  163. Wang Y, Hu X, Jiang B et al (2016a) Symbiotic relationship analysis of predominant bacteria in a lab-scale anammox UASB bioreactor. Environ Sci Pollut Res 23:7615–7626CrossRefGoogle Scholar
  164. Wang H, Zhang Y, Angelidaki I (2016b) Ammonia inhibition on hydrogen enriched anaerobic digestion of manure under mesophilic and thermophilic conditions. Water Res 105:314–319CrossRefGoogle Scholar
  165. 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 309:100–104Google Scholar
  166. Westerholm M, Dolfing J, Sherry A et al (2011) Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes. Environ Microbiol Rep 3:500–505CrossRefGoogle Scholar
  167. 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
  168. Westerholm M, Moestedt J, Schnürer A (2016) Biogas production through syntrophic acetate oxidation and deliberate operating strategies for improved digester performance. Appl Energy 179:124–135CrossRefGoogle Scholar
  169. Wett B (2006) Solved upscaling problems for implementing deammonification of rejection water. Water Sci Technol 53(12):121–128CrossRefGoogle Scholar
  170. Yamamoto T, Takaki K, Koyama T et al (2008) Long-term stability of partial nitritation of swine wastewater digester liquor and its subsequent treatment by Anammox. Bioresour Technol 99:6419–6425CrossRefGoogle Scholar
  171. Yang S, Phan HV, Bustamante H et al (2017) Effects of shearing on biogas production and microbial community structure during anaerobic digestion with recuperative thickening. Bioresour Technol 234:439–447CrossRefGoogle Scholar
  172. Ye L, Zhang T (2011) Ammonia-oxidizing bacteria dominates over ammonia-oxidizing archaea in a saline nitrification reactor under low DO and high nitrogen loading. Biotechnol Bioeng 108:2544–2552CrossRefGoogle Scholar
  173. Yenigün O, Demirel B (2013) Ammonia inhibition in anaerobic digestion: a review. Process Biochem 48:901–911CrossRefGoogle Scholar
  174. Zhang L, Yang J, Hira D et al (2011) High-rate partial nitrification treatment of reject water as a pretreatment for anaerobic ammonium oxidation (anammox). Bioresour Technol 102:3761–3767CrossRefGoogle Scholar
  175. Zhang Z, Li Y, Chen S et al (2012) Simultaneous nitrogen and carbon removal from swine digester liquor by the Canon process and denitrification. Bioresour Technol 114:84–89CrossRefGoogle Scholar
  176. Zhang C, Su H, Tan T (2013) Batch and semi-continuous anaerobic digestion of food waste in a dual solid-liquid system. Bioresour Technol 145:10–16CrossRefGoogle Scholar
  177. Zhang F, Zhang Y, Ding J et al (2014) Stable acetate production in extreme-thermophilic (70°C) mixed culture fermentation by selective enrichment of hydrogenotrophic methanogens. Sci Rep 4:5268. Scholar
  178. Zhang L, Narita Y, Gao L et al (2017) Maximum specific growth rate of anammox bacteria revisited. Water Res 116:296–303CrossRefGoogle Scholar
  179. Zhao Z, Zhang Y, Woodard TL et al (2015) Enhancing syntrophic metabolism in up-flow anaerobic sludge blanket reactors with conductive carbon materials. Bioresour Technol 191:140–145CrossRefGoogle Scholar
  180. Zhao Z, Zhang Y, Holmes DE et al (2016) Potential enhancement of direct interspecies electron transfer for syntrophic metabolism of propionate and butyrate with biochar in up-flow anaerobic sludge blanket reactors. Bioresour Technol 209:148–156CrossRefGoogle Scholar
  181. Zhao Y, Liu S, Jiang B et al (2018) Genome-centered metagenomics analysis reveals the symbiotic organisms possessing ability to cross-feed with anammox bacteria in anammox consortia. Environ Sci Technol 52:11285–11296CrossRefGoogle Scholar
  182. Zhuang L, Tang J, Wang Y et al (2015) Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. J Hazard Mater 293:37–45CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Albert Magrí
    • 1
    • 2
    Email author
  • Belén Fernández
    • 3
  • Francesc X. Prenafeta-Boldú
    • 3
  • Josep Ruiz-Sánchez
    • 3
  1. 1.LEQUIA, Institute of the EnvironmentUniversity of GironaGirona, CataloniaSpain
  2. 2.Department of Agri-Food Engineering and Biotechnology (DEAB)Universitat Politècnica de Catalunya (UPC) BarcelonaTechCastelldefels (Barcelona)Spain
  3. 3.Integral Management of Organic Waste (GIRO)Institute of Agrifood Research and Technology (IRTA)Caldes de Montbui (Barcelona)Spain

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