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

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Improving Biogas Production

Part of the book series: Biofuel and Biorefinery Technologies ((BBT,volume 9))

Abstract

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.

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Notes

  1. 1.

    The use of methyl or carboxyl labelled acetate isotopes is based on the fact that in the acetotrophic methanogenesis (Equation A), CH4 originates only from the methyl C in the acetate molecule. Differently, after acetate oxidation, both atoms of C (methyl and carboxyl) are available for the hydrogenotrophic methanogenesis (Equation B) in the form of CO2. Reactions A and B finally provide the same products (two moles of CH4 and two moles of CO2), but only the conversion of labelled 13C-acetate, or 14C-acetate, (identified by the underlined C atom in both Equations) by AMA yields two moles of labelled CH4 (Reaction A). In contrast, the SAO process (Reaction B) yields a uniform distribution of the labelled C as CH4 and CO2 (Gehring et al. 2016).

    $$2{\underline{\text{C}}\text{H}}_{3} {\text{COOH}}\rightarrow 2{\underline{\text{C}}\text{H}}_{4} + 2{\text{CO}}_{2} $$
    (A)
    $$2{\underline{\text{C}}\text{H}}_{3} {\text{COOH}} + 4{\text{H}}_{2} {\text{O}}\rightarrow 2{\underline{\text{C}}\text{O}}_{2} + 2{\text{CO}}_{2} + 8{\text{H}}_{2} \rightarrow {\underline{\text{C}}\text{H}}_{4} + {\text{CH}}_{4} + {\underline{\text{C}}\text{O}}_{2} + {\text{CO}}_{2} + 4{\text{H}}_{2} {\text{O}}$$
    (B)
  2. 2.

    Carbon isotopic ratio: (\({\updelta }^{ 1 3} {\text{C}} = \left( {\frac{{\left( {{}^{ 1 3}{\text{C}}/{}^{12}{\text{C}}} \right)_{\text{sample}} }}{{\left( {{}^{ 1 3}{\text{C}}/^{ 1 2} {\text{C}}} \right)_{\text{standard}} }} - 1} \right)\cdot 10^{3}\) (‰)); Fractionation factor: \(\left( {{\alpha }_{\text{C}} = \frac{{{\updelta }^{ 1 3} {\text{CO}}_{ 2} { + 10}^{ 3} }}{{{\updelta }^{ 1 3} {\text{CH}}_{ 4} { + 10}^{ 3} }}} \right)\)

  3. 3.

    Biomass acclimation refers to reversible physiological adjustments of microorganisms in response to rather short-term/limited perturbances in the environment, whereas biomass adaptation usually refers to changes in the microbial community structure and function in response to more intense/persistent environmental changes.

References

  • Abbasi T, Tauseef SM, Abbasi SA (2012) Biogas energy. SpringerBriefs in environmental science 2. Springer, New York, USA

    Book  Google Scholar 

  • 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 61:1715–1722

    Article  Google Scholar 

  • Abouelenien F, Nakashimada Y, Nishio N (2009) Dry mesophilic fermentation of chicken manure for production of methane by repeated batch culture. J Biosci Bioeng 107:293–295

    Article  Google Scholar 

  • Ahammad SZ, Davenport RJ, Read LF et al (2013) Rational immobilization of methanogens in high cell density bioreactors. RSC Adv 3:774–781

    Article  Google Scholar 

  • Anthonisen AC, Loehr RC, Prakasam TBS et al (1976) Inhibition of nitrification by ammonia and nitrous acid. J Water Pollut Control Fed 48:835–852

    Google Scholar 

  • 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 241:830–840

    Article  Google Scholar 

  • 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 52:1361–1368

    Google Scholar 

  • Banks CJ, Zhang Y, Jiang Y et al (2012) Trace element requirements for stable food waste digestion at elevated ammonia concentrations. Bioresour Technol 104:127–135

    Article  Google Scholar 

  • Batstone DJ, Keller J, Angelidaki I et al (2002) Anaerobic digestion model no. 1 (ADM1). Scientific and technical report 13. IWA Publishing, London

    Google Scholar 

  • 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 65:125–133

    Article  Google Scholar 

  • Calli B, Mertoglu B, Inanc B et al (2005) Methanogenic diversity in anaerobic bioreactors under extremely high ammonia levels. Enzyme Microb Technol 37:448–455

    Article  Google Scholar 

  • 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. https://doi.org/10.1155/2016/3796352

    Google Scholar 

  • Cao Y, van Loosdrecht MCM, Daigger GT (2017) Mainstream partial nitritation-anammox in municipal wastewater treatment: status, bottlenecks, and further studies. Appl Microbiol Biotechnol 101:1365–1383

    Article  Google Scholar 

  • 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 260:157–168

    Article  Google Scholar 

  • 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 327:884–893

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 297:217–228

    Article  Google Scholar 

  • 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 106:231–241

    Article  Google Scholar 

  • 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 203:559–573

    Article  Google Scholar 

  • Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202

    Article  Google Scholar 

  • Conrad R (2005) Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal. Org Geochem 36:739–752

    Article  Google Scholar 

  • 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 15:116–123

    Article  Google Scholar 

  • 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 48:7536–7543

    Article  Google Scholar 

  • Cuetos MJ, Martinez EJ, Moreno R et al (2017) Enhancing anaerobic digestion of poultry blood using activated carbon. J Adv Res 8:297–307

    Article  Google Scholar 

  • 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. https://doi.org/10.2166/wpt.2011.033

  • 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 39:303–308

    Article  Google Scholar 

  • 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 87:1641–1647

    Article  Google Scholar 

  • De Vrieze J, Hennebel T, Boon N et al (2012) Methanosarcina: the rediscovered methanogen for heavy duty biomethanation. Bioresour Technol 112:1–9

    Article  Google Scholar 

  • Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Bio-Technol 7:173–190

    Article  Google Scholar 

  • Dosta J, Fernández I, Vázquez-Padín JR et al (2008) Short- and long-term effects of temperature on the Anammox process. J Hazard Mat 154:688–693

    Article  Google Scholar 

  • Dytczak MA, Londry KL, Oleszkiewicz JA (2008) Nitrifying genera in activated sludge may influence nitrification rates. Water Environ Res 80:388–396

    Article  Google Scholar 

  • 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 2011

    Google Scholar 

  • 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 15:369–410

    Article  Google Scholar 

  • 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 36:212–218

    Article  Google Scholar 

  • Flemming H-C, Wingender J, Szewzyk U et al (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575

    Article  Google Scholar 

  • Fotidis IA, Karakashev D, Kotsopoulos TA et al (2013) Effect of ammonium and acetate on methanogenic pathway and methanogenic community composition. FEMS Microbiol Ecol 83:38–48

    Article  Google Scholar 

  • 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 11:2087–2094

    Article  Google Scholar 

  • Furukawa K, Inatomi Y, Qiao S et al (2009) Innovative treatment system for digester liquor using anammox process. Bioresour Technol 100:5437–5443

    Article  Google Scholar 

  • 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 99:295–306

    Article  Google Scholar 

  • 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 163:92–99

    Article  Google Scholar 

  • 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 198:372–379

    Article  Google Scholar 

  • Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18:1049–1056

    Article  Google Scholar 

  • Geets J, Boon N, Verstraete W (2006) Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen fluctuations. FEMS Microbiol Ecol 58:1–13

    Article  Google Scholar 

  • 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 49:4705–4714

    Article  Google Scholar 

  • 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 102:362–373

    Article  Google Scholar 

  • Giustinianovich EA, Campos J-L, Roeckel MD (2016) The presence of organic matter during autotrophic nitrogen removal: Problem or opportunity? Sep Purif Technol 166:102–108

    Article  Google Scholar 

  • 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 7:257–264

    Article  Google Scholar 

  • Hansen KH, Angelidaki I, Ahring BK (1998) Anaerobic digestion of swine manure: Inhibition by ammonia. Water Res 32:5–12

    Article  Google Scholar 

  • Hansen KH, Angelidaki I, Ahring BK (1999) Improving thermophilic anaerobic digestion of swine manure. Water Res 33:1805–1810

    Article  Google Scholar 

  • 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 45:508–513

    Article  Google Scholar 

  • 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 69:90–99

    Article  Google Scholar 

  • Hattori S (2008) Syntrophic acetate-oxidizing microbes in methanogenic environments. Microbes Environ 23:118–127

    Article  Google Scholar 

  • 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 50:1601–1609

    Article  Google Scholar 

  • 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 2010

    Google Scholar 

  • Henze M, Harremoës P, Jansen JlC et al (1995) Wastewater treatment: biological and chemical processes. Springer, Berlin

    Google Scholar 

  • 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 79:6491–6500

    Article  Google Scholar 

  • 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. https://doi.org/10.1099/mgen.0.000072

  • 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 253:402–407

    Article  Google Scholar 

  • Hunik JH, Hamelers HVM, Koster IW (1990) Growth-rate inhibition of acetoclastic methanogens by ammonia and pH in poultry manure digestion. Biol Wastes 32:285–297

    Article  Google Scholar 

  • Jaroszynski LW, Oleszkiewicz JA (2011) Autotrophic ammonium removal from reject water: partial nitrification and anammox in one-reactor versus two-reactor systems. Environ Technol 32:289–294

    Article  Google Scholar 

  • 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 88:181–198

    Article  Google Scholar 

  • 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 4:1035–1046

    Article  Google Scholar 

  • 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 14:615–648

    Article  Google Scholar 

  • Jin R-C, Yang G-F, Yu J-J et al (2012) The inhibition of the Anammox process: a review. Chem Eng J 197:67–79

    Article  Google Scholar 

  • Kampschreur MJ, Temmink H, Kleerebezem R et al (2009) Nitrous oxide emission during wastewater treatment. Water Res 43:4093–4103

    Article  Google Scholar 

  • 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. https://doi.org/10.3389/fmicb.2014.00575

    Article  Google Scholar 

  • Kayhanian M (1994) Performance of a high-solids anaerobic digestion process under various ammonia concentrations. J Chem Technol Biotechnol 59:349–352

    Article  Google Scholar 

  • Koster IW, Lettinga G (1984) The influence of ammonium-nitrogen on the specific activity of pelletized methanogenic sludge. Agric Wastes 9:205–216

    Article  Google Scholar 

  • Kothari R, Pandey AK, Kumar S et al (2014) Different aspects of dry anaerobic digestion for bio-energy: an overview. Renew Sustain Energy Rev 39:174–195

    Article  Google Scholar 

  • 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 241:466–472

    Article  Google Scholar 

  • Kumar M, Lin J-G (2010) Co-existence of anammox and denitrification for simultaneous nitrogen and carbon removal—strategies and issues. J Hazard Mat 178:1–9

    Article  Google Scholar 

  • Labatut RA, Angenent LT, Scott NR (2014) Conventional mesophilic vs. thermophilic anaerobic digestion: a trade-off between performance and stability? Water Res 53:249–258

    Article  Google Scholar 

  • Lackner S, Gilbert EM, Vlaeminck SE et al (2014) Full-scale partial nitritation/anammox experiences—an application survey. Water Res 55:292–303

    Article  Google Scholar 

  • Lalov IG, Krysteva MA, Phelouzat J-L (2001) Improvement of biogas production from vinasse via covalently immobilized methanogens. Bioresour Technol 79:83–85

    Article  Google Scholar 

  • 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 103–120

    Google Scholar 

  • 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 55:215–222

    Article  Google Scholar 

  • 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 70:1–8

    Article  Google Scholar 

  • 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 234:303–309

    Article  Google Scholar 

  • 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 265:498–505

    Article  Google Scholar 

  • 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. https://doi.org/10.3389/fmicb.2016.01431

  • 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 97:10575–10583

    Article  Google Scholar 

  • Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann NY Acad Sci 1125:171–189

    Article  Google Scholar 

  • 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 17:648–655

    Article  Google Scholar 

  • Lotti T, van der Star WRL, Kleerebezem R et al (2012) The effect of nitrite inhibition on the anammox process. Water Res 46:2559–2569

    Article  Google Scholar 

  • Lotti T, Kleerebezem R, Lubello C et al (2014) Physiological and kinetic characterization of a suspended cell anammox culture. Water Res 60:1–14

    Article  Google Scholar 

  • 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 73:662–668

    Article  Google Scholar 

  • 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 47:2297–2306

    Article  Google Scholar 

  • 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 167:251–259

    Article  Google Scholar 

  • Madsen M, Holm-Nielsen JB, Esbensen KH (2011) Monitoring of anaerobic digestion processes: A review perspective. Renew Sustain Energy Rev 15:3141–3155

    Article  Google Scholar 

  • 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 28:255–265

    Article  Google Scholar 

  • Magrí A, Sole-Mauri F, Colprim J et al (2007b) Evaluation of the SHARON process (partial nitritation in a chemostat) using simulation. Afinidad 64:378–383

    Google Scholar 

  • Magrí A, Vanotti MB, Szögi AA (2012a) Anammox sludge immobilized in polyvinyl alcohol (PVA) cryogel carriers. Bioresour Technol 114:231–240

    Article  Google Scholar 

  • 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 41:1989–2000

    Article  Google Scholar 

  • 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 131:170–184

    Article  Google Scholar 

  • 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 14:1739–1756

    Article  Google Scholar 

  • Makádi M, Tomócsik A, Orosz V (2012) Digestate: a new nutrient source—review. In: Kumar S (ed) Biogas. InTech, Rijeka, pp 295–310

    Google Scholar 

  • 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 596–597:106–123

    Article  Google Scholar 

  • 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 36:412–427

    Article  Google Scholar 

  • 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 72:3273–3276

    Article  Google Scholar 

  • McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632

    Article  Google Scholar 

  • Morris BEL, Henneberger R, Huber H et al (2013) Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37:384–406

    Article  Google Scholar 

  • 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 10:2405–2418

    Article  Google Scholar 

  • 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 40:3109–3118

    Article  Google Scholar 

  • Müller V (2003) Energy conservation in acetogenic bacteria. Appl Environ Microbiol 69:6345–6353

    Article  Google Scholar 

  • Müller B, Sun L, Schnürer A (2013) First insights into the syntrophic acetate-oxidizing bacteria—a genetic study. MicrobiologyOpen 2:35–53

    Article  Google Scholar 

  • 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 31:1236–1242

    Article  Google Scholar 

  • 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 118:210–218

    Article  Google Scholar 

  • 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 110:701–705

    Article  Google Scholar 

  • 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 43:114–122

    Article  Google Scholar 

  • Nkoa R (2014) Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agron Sustain Dev 34:473–492

    Article  Google Scholar 

  • Nobu MK, Narihiro T, Rinke C et al (2015) Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J 9:1710–1722

    Article  Google Scholar 

  • 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 668:74–79

    Article  Google Scholar 

  • Pereira AD, Cabezas A, Etchebehere C et al (2017) Microbial communities in anammox reactors: a review. Environ Technol Rev 6:74–93

    Article  Google Scholar 

  • 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 75:1281–1293

    Article  Google Scholar 

  • 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 235:229–239

    Article  Google Scholar 

  • 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 197:161–170

    Article  Google Scholar 

  • 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 36:1981–1986

    Article  Google Scholar 

  • Pynaert K, Smets BF, Beheydt D et al (2004) Start-up of autotrophic nitrogen removal reactors via sequential biocatalyst addition. Environ Sci Technol 38:1228–1235

    Article  Google Scholar 

  • 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 23:157–164

    Article  Google Scholar 

  • 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. https://doi.org/10.1186/1475-2859-4-24

    Article  Google Scholar 

  • Ragsdale SW (2008) Enzymology of the Wood-Ljungdahl pathway of acetogenesis. Ann NY Acad Sci 1125:129–136

    Article  Google Scholar 

  • Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898

    Article  Google Scholar 

  • Rajagopal R, Massé DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour Technol 143:632–641

    Article  Google Scholar 

  • 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 103:116–122

    Article  Google Scholar 

  • Regueiro L, Carballa M, Lema JM (2016) Microbiome response to controlled shifts in ammonium and LCFA levels in co-digestion systems. J Biotechnol 220:35–44

    Article  Google Scholar 

  • 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 270:542–548

    Article  Google Scholar 

  • Romero-Güiza MS, Vila J, Mata-Alvarez J et al (2016) The role of additives on anaerobic digestion: a review. Renew Sustain Energy Rev 58:1486–1499

    Article  Google Scholar 

  • 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. https://doi.org/10.1039/c3ee42189a

    Article  Google Scholar 

  • Rudnitskaya A, Legin A (2008) Sensor systems, electronic tongues and electronic noses, for the monitoring of biotechnological processes. J Ind Microbiol Biotechnol 35:443–451

    Article  Google Scholar 

  • 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 250:513–522

    Article  Google Scholar 

  • 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 649:760–769

    Article  Google Scholar 

  • 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 228:935–943

    Article  Google Scholar 

  • 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 176:98–105

    Article  Google Scholar 

  • 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 71:785–791

    Article  Google Scholar 

  • Schink B, Montag D, Keller A et al (2017) Hydrogen or formate: Alternative key players in methanogenic degradation. Environ Microbiol Rep 9:189–202

    Article  Google Scholar 

  • Schnürer A, Houwen FP, Svensson BH (1994) Mesophilic syntrophic acetate oxidation during methane formation by a triculture at high ammonium concentration. Arch Microbiol 162:70–74

    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 Microb Ecol 29:249–261

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Seuntjens D, Carvajal-Arroyo JM, Ruopp M et al (2018) High-resolution mapping and modeling of anammox recovery from recurrent oxygen exposure. Water Res 144:522–531

    Article  Google Scholar 

  • Siles JA, Brekelmans J, Martín MA et al (2010) Impact of ammonia and sulphate concentration on thermophilic anaerobic digestion. Bioresour Technol 101:9040–9048

    Article  Google Scholar 

  • Silva AJ, Hirasawa JS, Varesche MB et al (2006) Evaluation of support materials for the immobilization of sulfate-reducing bacteria and methanogenic archaea. Anaerobe 12:93–98

    Article  Google Scholar 

  • Stams AJM (1994) Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie Van Leeuwenhoek 66:271–294

    Article  Google Scholar 

  • St-Pierre B, Wright A-DG (2014) Comparative metagenomic analysis of bacterial populations in three full-scale mesophilic anaerobic manure digesters. Appl Microbiol Biotechnol 98:2709–2717

    Article  Google Scholar 

  • 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 63:2446–2448

    Google Scholar 

  • 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 50:589–596

    Article  Google Scholar 

  • Sun L, Müller B, Westerholm M et al (2014) Syntrophic acetate oxidation in industrial CSTR biogas digesters. J Biotechnol 171:39–44

    Article  Google Scholar 

  • 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 218:1215–1223

    Article  Google Scholar 

  • Sung S, Liu T (2003) Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere 53:43–52

    Article  Google Scholar 

  • Tang C-J, Zheng P, Wang C-H et al (2011) Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res 45:135–144

    Article  Google Scholar 

  • 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 230:149–157

    Article  Google Scholar 

  • Udert KM, Fux C, Münster M et al (2003) Nitrification and autotrophic denitrification of source-separated urine. Water Sci Technol 48(1):119–130

    Article  Google Scholar 

  • 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 41:4149–4163

    Article  Google Scholar 

  • van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON®-Anammox® process for treatment of ammonium rich wastewater. Water Sci Technol 44(1):153–160

    Article  Google Scholar 

  • 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 162:1–20

    Article  Google Scholar 

  • van Niftrik L, Jetten MSM (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76:585–596

    Article  Google Scholar 

  • Vanwonterghem I, Evans PN, Parks DH et al (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1:16170. https://doi.org/10.1038/nmicrobiol.2016.170

    Article  Google Scholar 

  • 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 69:1151–1158

    Article  Google Scholar 

  • 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 43:5035–5041

    Article  Google Scholar 

  • Vlaeminck SE, De Clippeleir H, Verstraete W (2012) Microbial resource management of one-stage partial nitritation/anammox. Microb Biotechnol 5:433–448

    Article  Google Scholar 

  • 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 178:138–145

    Article  Google Scholar 

  • Wang H, Fotidis IA, Angelidaki I (2015) Ammonia effect on hydrogenotrophic methanogens and syntrophic acetate-oxidizing bacteria. FEMS Microbiol Ecol 91:fiv130. https://doi.org/10.1093/femsec/fiv130

    Article  Google Scholar 

  • 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 23:7615–7626

    Article  Google Scholar 

  • Wang H, Zhang Y, Angelidaki I (2016b) Ammonia inhibition on hydrogen enriched anaerobic digestion of manure under mesophilic and thermophilic conditions. Water Res 105:314–319

    Article  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

    Google Scholar 

  • Westerholm M, Dolfing J, Sherry A et al (2011) Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes. Environ Microbiol Rep 3:500–505

    Article  Google Scholar 

  • 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 78:7619–7625

    Article  Google Scholar 

  • Westerholm M, Moestedt J, Schnürer A (2016) Biogas production through syntrophic acetate oxidation and deliberate operating strategies for improved digester performance. Appl Energy 179:124–135

    Article  Google Scholar 

  • Wett B (2006) Solved upscaling problems for implementing deammonification of rejection water. Water Sci Technol 53(12):121–128

    Article  Google Scholar 

  • 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 99:6419–6425

    Article  Google Scholar 

  • 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 234:439–447

    Article  Google Scholar 

  • 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 108:2544–2552

    Article  Google Scholar 

  • Yenigün O, Demirel B (2013) Ammonia inhibition in anaerobic digestion: a review. Process Biochem 48:901–911

    Article  Google Scholar 

  • 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 102:3761–3767

    Article  Google Scholar 

  • 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 114:84–89

    Article  Google Scholar 

  • Zhang C, Su H, Tan T (2013) Batch and semi-continuous anaerobic digestion of food waste in a dual solid-liquid system. Bioresour Technol 145:10–16

    Article  Google Scholar 

  • 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. https://doi.org/10.1038/srep05268

    Article  Google Scholar 

  • Zhang L, Narita Y, Gao L et al (2017) Maximum specific growth rate of anammox bacteria revisited. Water Res 116:296–303

    Article  Google Scholar 

  • 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 191:140–145

    Article  Google Scholar 

  • 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 209:148–156

    Article  Google Scholar 

  • 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 52:11285–11296

    Article  Google Scholar 

  • Zhuang L, Tang J, Wang Y et al (2015) Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. J Hazard Mater 293:37–45

    Article  Google Scholar 

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Acknowledgements

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.

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Authors and Affiliations

  1. LEQUIA, Institute of the Environment, University of Girona, Campus Montilivi, Carrer Maria Aurèlia Capmany 69, 17003, Girona, Catalonia, Spain

    Albert Magrí

  2. Department of Agri-Food Engineering and Biotechnology (DEAB), Universitat Politècnica de Catalunya (UPC) BarcelonaTech, Campus Baix Llobregat, Edifici D4, Carrer Esteve Terradas 8, 08860, Castelldefels (Barcelona), Catalonia, Spain

    Albert Magrí

  3. Integral Management of Organic Waste (GIRO), Institute of Agrifood Research and Technology (IRTA), Torre Marimon, 08140, Caldes de Montbui (Barcelona), Catalonia, Spain

    Belén Fernández, Francesc X. Prenafeta-Boldú & Josep Ruiz-Sánchez

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  1. Universidade Federal da Fronteira Sul (UFFS)—Campus Erechim, Erechim, Rio Grande do Sul, Brazil

    Helen Treichel

  2. Universidade Federal de Santa Catarina, Florianópolis, Brazil

    Gislaine Fongaro

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Magrí, A., Fernández, B., Prenafeta-Boldú, F.X., Ruiz-Sánchez, J. (2019). Coupling Syntrophic Acetate Oxidation and Anaerobic Ammonium Oxidation When Treating Nitrogen-Rich Organic Wastes for Energy Recovery and Nitrogen Removal: Overview and Prospects. In: Treichel, H., Fongaro, G. (eds) Improving Biogas Production. Biofuel and Biorefinery Technologies, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-10516-7_6

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