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Removal of nitrogen from wastewaters by anaerobic ammonium oxidation (ANAMMOX) using granules in upflow reactors

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Abstract

Nitrogen pollution of waters has sometimes caused severe eutrophication, leading to the death of fishes and most aquatic life. There is therefore a need for efficient and cost-effective methods to remove nitrogen from ammonium-rich wastewaters. Anaerobic ammonium oxidation (ANAMMOX) is a promising process to remove nitrogen because this process directly oxidizes ammonium (NH4 +) to dinitrogen gas (N2) under anoxic condition. Nonetheless, a challenge of this process is that chemolithoautotrophic Anammox bacteria grow slowly at the beginning, thus resulting in low Anammox biomass and instability of reactors. Such issues can be overcome by granulation of the Anammox sludge. Here, we review the characteristics of the Anammox bacteria, and the formation, structure and flotation of Anammox granules under high hydraulic loadings. We also evaluate the performances of full-scale granular Anammox processes. The major points are: 1) Anammox bacteria secrete a large amount of extracellular polymeric substances (EPS), up to 415 mg g−1 of volatile suspended solids (VSS), containing many hydrophobic functional groups that facilitate biomass granulation. 2) Granulation enhances the sludge settling property and retention time, which contributes to the extremely high nitrogen removal rate of 77 kg m−3 d−1 of Anammox upflow reactors. 3) Flotation of Anammox granules frequently occurs under nitrogen removal rate higher than 10 kg m−3 d−1, which is mainly due to the overproduction of EPS under high hydraulic conditions.

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References

  • Adav SS, Lee DJ, Tay JH (2008) Extracellular polymeric substances and structural stability of aerobic granule. Water Res 42:1644–1650. doi:10.1016/j.watres.2007.10.013

    Article  CAS  Google Scholar 

  • Ali M, Chai LY, Tang CJ, Zheng P, Min XB, Yang ZH, Xiong L, Song YX (2013) The increasing interest of anammox research in China: bacteria, process development, and application. BioMed Res Int, article ID: 134914

  • Ali M, Chai LY, Min XB, Tang CJ, Afrin S, Liao Q, Wang HY, Peng C, Song YX, Zheng P (2016a) Performance and characteristics of a nitritation air-lift reactor under long-term HRT shortening. Int Biodeterior Biodegr 111:45–53. doi:10.1016/j.watres.2007.10.013

    Article  CAS  Google Scholar 

  • Ali M, Chai LY, Wang HY, Tang CJ, Min XB, Yan X, Peng C, Song YX, Zheng P (2016b) Enhanced short-cut nitrification in an airlift reactor by CaCO3 attachment on biomass under high bicarbonate condition. Biodegradation 27:131–144. doi:10.1007/s10532-016-9761-x

    Article  CAS  Google Scholar 

  • Amine-Khodja A, Richard C, Lavédrine B, Guyot G, Trubetskaya O, Trubetskoj O (2006) Water-soluble fractions of composts for the photodegradation of organic pollutants in solar light. Environ Chem Lett 4:249. doi:10.1007/s10311-006-0074-x

    Article  CAS  Google Scholar 

  • Arrojo B, Mosquera-Corral A, Campos JL, Méndez R (2006) Effects of mechanical stress on Anammox granules in a sequencing batch reactor (SBR). J Biotechnol 123:453–463. doi:10.1016/j.jbiotec.2005.12.023

    Article  CAS  Google Scholar 

  • Brandsma J, Van de Vossenberg J, Risgaard-Petersen N, Schmid MC, Engström P, Eurenius K, Hulth S, Jaeschke A, Abbas B, Hopmans EC, Strous M, Schouten S, Jetten MSM, Sinninghe Damsté JS (2011) A multi-proxy study of anaerobic ammonium oxidation in marine sediments of the Gullmar Fjord, Sweden. Environ Microbiol Rep 3:360–366. doi:10.1111/j.1758-2229.2010.00233.x

    Article  CAS  Google Scholar 

  • Cai M, Zhu Y, Wei Z, Hu JQ, Pan SD, Xiao R, Dong CY, Jin MC (2016) Rapid decolorization of dye Orange G by microwave enhanced Fenton-like reaction with delafossite-type CuFeO2: a kinetic and mechanistic study. Sci Total Environ. doi:10.1016/j.scitotenv.2016.12.047

    Google Scholar 

  • Carneiro J, Cardenas LM, Hatch DJ, Trindade H, Scholefield D, Clegg CD, Hobbs P (2010) Effect of the nitrification inhibitor dicyandiamide on microbial communities and N2O from an arable soil fertilized with ammonium sulphate. Environ Chem Lett 8:237–246. doi:10.1007/s10311-009-0212-3

    Article  CAS  Google Scholar 

  • Chai LY, Min XB, Tang N, Wang YY (2009) Mechanism and kinetics of Zn(II) removal from wastewater by immobilized beads of SRB sludge. Int J Environ Pollut 37:20–33

    Article  CAS  Google Scholar 

  • Chai L, Wang Q, Li Q, Yang Z, Wang Y (2010) Enhanced removal of Hg(II) from acidic aqueous solution using thiol-functionalized biomass. Water Sci Technol 62:2157–2166. doi:10.2166/wst.2010.385

    Article  CAS  Google Scholar 

  • Chai LY, Wang YY, Zhao N, Yang W, You XY (2013) Sulfate-doped Fe3O4/Al2O3 nanoparticles as a novel adsorbent for fluoride removal from drinking water. Water Res 47:4040–4049. doi:10.1016/j.watres.2013.02.057

    Article  CAS  Google Scholar 

  • Chai LY, Yan X, Li QZ, Yang BT, Wang QW (2014) A comparative study of abiological granular sludge (ABGS) formation in different processes for zinc removal from wastewater. Environ Sci Pollut Res 21:12436–12444. doi:10.1007/s11356-014-3184-1

    Article  CAS  Google Scholar 

  • Chai LY, Ali M, Min XB, Song YX, Tang CJ, Wang HY, Yu C (2015) Partial nitrification in an air-lift reactor with long-term feeding of increasing ammonium concentrations. Bioresour Technol 185:134–142. doi:10.1016/j.biortech.2015.02.091

    Article  CAS  Google Scholar 

  • Chen MY, Lee DJ, Tay JH, Show KY (2007) Staining of extracellular polymeric substances and cells in bioaggregates. Appl Microbiol Biotechnol 75:467–474. doi:10.1007/s00253-006-0816-5

    Article  CAS  Google Scholar 

  • Chen JW, Ji QX, Zheng P, Chen TT, Wang CH, Mahmood Q (2010) Floatation and control of granular sludge in a high-rate anammox reactor. Water Res 44:3321–3328. doi:10.1016/j.watres.2010.03.016

    Article  CAS  Google Scholar 

  • Chen H, Ma C, Yang GF, Wang HZ, Yu ZM, Jin RC (2014) Floatation of flocculent and granular sludge in a high-loaded anammox reactor. Bioresour Technol 169:409–415. doi:10.1016/j.biortech.2014.06.063

    Article  CAS  Google Scholar 

  • Chen D, Szostak P, Wei Z, Xiao R (2016a) Reduction of orthophosphates loss in agricultural soil by nano calcium sulfate. Sci Total Environ 539:381–387. doi:10.1016/j.scitotenv.2015.09.028

    Article  CAS  Google Scholar 

  • Chen QQ, Sun FQ, Guo Q, Shen YY, Zhu WQ, Jin RC (2016b) Process stability in an anammox UASB reactor with individual and combined thiocyanate and hydraulic shocks. Sep Purif Technol 173:165–173. doi:10.1016/j.seppur.2016.09.005

    Article  CAS  Google Scholar 

  • Cirpus IEY, De Been M, Op den Camp HJM, Strous M, Le Paslier D, Kuenen GJ, Jetten SM (2005) A new soluble 10 kDa monoheme cytochrome c-552 from the anammox bacterium Candidatus “Kuenenia stuttgartiensis”. FEMS Microbiol Lett 252:273–278. doi:10.1016/j.femsle.2005.09.007

    Article  CAS  Google Scholar 

  • Cirpus IE, Geerts W, Hermans JH, Opden Camp HJ, Strous M, Kuenen JG, Jetten MS (2006) Challenging protein purification from anammox bacteria. Int J Biol Macromol 39:88–94. doi:10.1016/j.ijbiomac.2006.02.018

    Article  CAS  Google Scholar 

  • Dai HJ, Huang ZJ, Deng QH, Li Y, Xiao T, Ning XP, Lu Y, Yuan H (2015) The effects of lead exposure on serum uric acid and Hyperuricemia in Chinese adults: a cross-sectional study. Int J Environ Res Public Health 12:9672–9682. doi:10.3390/ijerph120809672

    Article  CAS  Google Scholar 

  • Dalsgaard T, Thamdrup B (2002) Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl Environ Microbiol 68:3802–3808. doi:10.1128/AEM.68.8.3802-3808.2002

    Article  CAS  Google Scholar 

  • Dang HY, Chen RP, Wang L, Guo LZ, Chen PP, Tang ZW, Tian F, Li SZ, Klotz Martin G (2010) Environmental factors shape sediment Anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol 76:7036–7047. doi:10.1128/AEM.01264-10

    Article  CAS  Google Scholar 

  • Dang HY, Zhou HX, Zhang ZN, Yu ZS, Hua E, Liu XS, Jiao NZ (2013) Molecular detection of Candidatus Scalindua pacifica and environmental responses of Sediment Anammox bacterial community in the Bohai Sea, China. PLoS One 8:e61330. doi:10.1371/journal.pone.0061330

    Article  CAS  Google Scholar 

  • Deng J, Gu YF, Zhang J, Xue K, Qin YJ, Yuan MT, Yi HQ, He ZL, Wu LY, Schuur EAG, Tiedje JM, Zhou JZ (2015) Shifts of tundra bacterial and Archaeal communities along a permafrost thaw gradient in Alaska. Mol Ecol 24:222–234. doi:10.1111/mec.13015

    Article  CAS  Google Scholar 

  • Di Iaconi C, Ramadori R, Lopez A, Passino R (2006) Influence of hydrodynamic shear force on properties of granular biomass in a sequencing batch biofilter reactor. J Biochem Eng 30:152–157. doi:10.1016/j.bej.2006.03.002

    Article  CAS  Google Scholar 

  • Franco A, Roca E, Lema JM (2006) Granulation in high-load denitrifying upflow sludge bed pulsed reactors. Water Res 40:871–880. doi:10.1016/j.watres.2005.11.044

    Article  CAS  Google Scholar 

  • Fuerst JA (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59:299–328. doi:10.1146/annurev.micro.59.030804.121258

    Article  CAS  Google Scholar 

  • Gonzalez-Gil G, Sougrat R, Behzad AR, Lens PNL, Saikaly PE (2015) Microbial community composition and ultrastructure of granules from a full-scale Anammox reactor. Microb Ecol 70:118–131. doi:10.1007/s00248-014-0546-7

    Article  CAS  Google Scholar 

  • Hong YG, Li M, Cao HL, Gu JD (2011) Residence of habitat-specific Anammox bacteria in the deep-sea subsurface sediments of the South China Sea: analyses of marker gene abundance with physical chemical parameters. Microb Ecol 62:36–47. doi:10.1007/s00248-011-9849-0

    Article  Google Scholar 

  • Hori K, Matsumoto S (2010) Bacterial adhesion: from mechanism to control. Biochem Eng J 48(3):424–434. doi:10.1016/j.bej.2009.11.014

    Article  CAS  Google Scholar 

  • Hou XL, Liu ST, Zhang ZT (2015) Role of extracellular polymeric substance in determining the high aggregation ability of anammox sludge. Water Res 75:51–62. doi:10.1016/j.watres.2015.02.031

    Article  CAS  Google Scholar 

  • Hu BL, Zheng P, Tang CJ, Chen JW (2010) Identification and quantification of anammox bacteria in eight nitrogen removal reactors. Water Res 44:5014–5020. doi:10.1016/j.watres.2010.07.021

    Article  CAS  Google Scholar 

  • Hulshoff Pol LW, de Castro Lopes SI, Lettinga G, Lens PN (2004) Anaerobic sludge granulation. Water Res 38:1376–1389. doi:10.1016/j.watres.2003.12.002

    Article  CAS  Google Scholar 

  • Ismail SB, de La Parra CJ, Temmink H, van Lier JB (2010) Extracellular polymeric substances (EPS) in upflow anaerobic sludge blanket (UASB) reactors operated under high salinity conditions. Water Res 44:1909–1917. doi:10.1016/j.watres.2009.11.039

    Article  CAS  Google Scholar 

  • Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT, Op den Camp HJ (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 44:65–84. doi:10.1080/10409230902722783

    Article  CAS  Google Scholar 

  • Jiang K, Zhou KG, Yang YC, Du H (2013) A pilot-scale study of cryolite precipitation from high fluoride-containing wastewater in a reaction-separation integrated reactor. J Environ Sci 25:1331–1337. doi:10.1016/S1001-0742(12)60204-6

    Article  CAS  Google Scholar 

  • Jiang K, Zhou KG, Yang YC, Du H (2014) Growth kinetics of calcium fluoride at high super saturation in a fluidized bed reactor. Environ Technol 35:82–88. doi:10.1080/09593330.2013.811542

    Article  CAS  Google Scholar 

  • Jin RC, Zhang QQ, Liu JH, Yang BE, Wu K, Zheng P (2013) Performance and stability of the partial nitrification process for nitrogen removal from monosodium glutamate wastewater. Sep Purif Technol 103:195–202. doi:10.1016/j.seppur.2012.10.042

    Article  CAS  Google Scholar 

  • Kanakaraju D, Glass BD, Oelgemöller M (2014) Titanium dioxide photocatalysis for pharmaceutical wastewater treatment. Environ Chem Lett 12:27–47. doi:10.1007/s10311-013-0428-0

    Article  CAS  Google Scholar 

  • Kartal B, Rattray J, van Niftrik LA (2007) Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49. doi:10.1016/j.syapm.2006.03.004

    Article  CAS  Google Scholar 

  • Kartal B, van Niftrik L, Rattray J, de Vossenberg J, Schmid MC, Damste JS, Jetten MSM, Strous M (2008) Candidatus “Brocadia fulgida”: an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63:46–55. doi:10.1111/j.1574-6941.2007.00408.x

    Article  CAS  Google Scholar 

  • Kartal B, Kuenen JG, van Loosdrecht MCM (2010) Sewage treatment with Anammox. Science 328:702–703. doi:10.1126/science.1185941

    Article  CAS  Google Scholar 

  • Klotz MG, Schmid MC, Strous M, Op den Camp HJM, Jetten MSM, Hooper AB (2008) Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol 10:3150–3163. doi:10.1111/j.1462-2920.2008.01733.x

    Article  CAS  Google Scholar 

  • Kuenen JG, Jetten MSM (2001) Extraordinary anaerobic ammonium-oxidizing bacteria. ASM News 67:456–463

    Google Scholar 

  • Kuenen JG, Robertson LA (1994) Combined nitrification–denitrification processes. FEMS Microbiol Rev 15:109–117. doi:10.1111/j.1574-6976.1994.tb00129.x

    Article  CAS  Google Scholar 

  • Kuypers MM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG, Sinninghe Damsté JS, Strous M, Jetten MS (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608–611. doi:10.1038/nature01472

    Article  CAS  Google Scholar 

  • Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM (2014) Full-scale partial nitritation/anammox experiences: an application survey. Water Res 55:292–303. doi:10.1016/j.watres.2014.02.032

    Article  CAS  Google Scholar 

  • Li M, Gu JD (2016) The diversity and distribution of anammox bacteria in the marine aquaculture zones. Appl Microbiol Biotechnol 100:8943–8953. doi:10.1007/s00253-016-7690-6

    Article  CAS  Google Scholar 

  • Li H, Chen S, Mu BZ, Gu JD (2010) Molecular detection of anaerobic ammonium-oxidizing (Anammox) bacteria in high-temperature petroleum reservoirs. Microb Ecol 60:771–783. doi:10.1007/s00248-010-9733-3

    Article  CAS  Google Scholar 

  • Li XF, Barnes D, Chen J (2011) Performance of struvite precipitation during pretreatment of raw landfill leachate and its biological validation. Environ Chem Lett 9:71–75. doi:10.1007/s10311-009-0248-4

    Article  CAS  Google Scholar 

  • Li MM, Zhu JY, Gan M, Wang QF, Shi QJ, Chai LY (2014) Characteristics of chromium coprecipitation mediated by acidithiobacillus ferrooxidans DC. Water Air Soil Pollut 225:2071. doi:10.1007/s11270-014-2071-1

    Article  CAS  Google Scholar 

  • Li PJ, Xia JL, Yang S, Nie ZY, Su DL, Gao QR, Zhang C, Ma YL (2015) Optimizing production of pectinase from orange peel by penicilliumoxalicum PJ02 using response surface methodology. Waste Biomass Valoriz 6:13–22. doi:10.1007/s12649-014-9317-4

    Article  CAS  Google Scholar 

  • Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175:413–429. doi:10.1007/s002030100280

    Article  CAS  Google Scholar 

  • Liu Y, Tay JH (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res 36:1653–1665. doi:10.1016/S0043-1354(01)00379-7

    Article  CAS  Google Scholar 

  • Liu YQ, Liu Y, Tay JH (2004) The effects of extracellular polymeric substances on the formation and stability of biogranules. Appl Microbiol Biotechnol 65:143–148. doi:10.1007/s00253-004-1657-8

    Article  CAS  Google Scholar 

  • Liu ST, Yang FL, Gong Z, Meng FG, Chen HH, Xue Y, Furukawa K (2008) Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresour Technol 99:6817–6825. doi:10.1016/j.biortech.2008.01.054

    Article  CAS  Google Scholar 

  • Liu XW, Sheng GP, Yu HQ (2009) Physicochemical characteristics of microbial granules. Biotechnol Adv 27:1061–1070. doi:10.1016/j.biotechadv.2009.05.020

    Article  CAS  Google Scholar 

  • Lu HF, Zheng P, Ji QX, Zhang HT, Ji JY, Wang L, Ding S, Chen TT, Zhang JQ, Tang CJ, Chen JW (2012) The structure, density and settlability of anammox granular sludge in high-rate reactors. Bioresour Technol 123:312–317. doi:10.1016/j.biortech.2012.07.003

    Article  CAS  Google Scholar 

  • Lu HF, Ji QX, Ding S, Zheng P (2013) The morphological and settling properties of ANAMMOX granular sludge in high-rate reactors. Bioresour Technol 143:592–597. doi:10.1016/j.biortech.2013.06.046

    Article  CAS  Google Scholar 

  • Ma YG, Hira D, Li ZG, Chen C, Furukawa K (2011) Nitrogen removal performance of a hybrid anammox reactor. Bioresour Technol 102:6650–6656. doi:10.1016/j.biortech.2011.03.081

    Article  CAS  Google Scholar 

  • Ma B, Wang SY, Cao SB, Miao Y, Jia F, Du R, Peng YZ (2016) Biological nitrogen removal from sewage via anammox. Bioresour Technol 200:981–990. doi:10.1016/j.biortech.2015.10.074

    Article  CAS  Google Scholar 

  • Maciej D (2000) Activities in nonpoint pollution control in rural areas of Poland. Ecol Eng 14:429––434. doi:10.1016/S0925-8574(99)00066-X

    Article  Google Scholar 

  • Martínez F, Lema J, Mendez R, Cuervo-Lopez F, Gomez J (2004) Role of exopolymeric protein on the settleability of nitrifying sludges. Bioresour Technol 94:43–48

    Article  CAS  Google Scholar 

  • Mizuto K, Okabe S (2014) Ecophysiology of anammox bacterium ‘Candidatus Scalindua japonica’. Master Thesis

  • Mu Y, Yu HQ (2006) Biological hydrogen production in a UASB reactor with granules. I: physicochemical characteristics of hydrogen-producing granules. Biotechnol Bioeng 94:980–987

    Article  CAS  Google Scholar 

  • Ni BJ, Chen YP, Liu SY, Fang F, Xie WM, Yu HQ (2009) Modeling a granule-based anaerobic ammonium oxidizing (ANAMMOX) process. Biotechnol Bioeng 103:490–499. doi:10.1002/bit.22279

    Article  CAS  Google Scholar 

  • Ni BJ, Hu BL, Fang F, Xie WM, Kartal B, Liu XW, Sheng GP, Jetten M, Zheng P, Yu HQ (2010) Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol 76:2652––2656. doi:10.1128/AEM.02271-09

    Article  CAS  Google Scholar 

  • Ni SQ, Sun N, Yang HL, Zhang J, Ngo HH (2015) Distribution of extracellular polymeric substances in anammox granules and their important roles during anammox granulation. Biochem Eng J 101:126–133. doi:10.1016/j.bej.2015.05.014

    Article  CAS  Google Scholar 

  • Peng C, Chai LY, Tang CJ, Min XB, Ali M, Song YX, Qi WM (2017a) Feasibility and enhancement of copper and ammonia removal from wastewater using struvite formation: a comparative research. J Chem Technol Biotechnol 92:325–333. doi:10.1002/jctb.5009

    Article  CAS  Google Scholar 

  • Peng C, Chai LY, Tang CJ, Min XB, Duan CS, Yu C (2017b) Study on the mechanism of copper–ammonia complex decomposition in struvite formation process and enhanced ammonia and copper removal. J Environ Sci. doi:10.1016/j.jes.2016.06.020

    Google Scholar 

  • Qiao S, Yamamoto T, Misaka M (2010) High-rate nitrogen removal from livestock manure digester liquor by combined partial nitritation-anammox process. Biodegradation 21:11–20. doi:10.1007/s10532-009-9277-8

    Article  Google Scholar 

  • Quan ZX, Rhee SK, Zuo JE, Bae JW, Park JR, Lee ST, Park JH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130–3139. doi:10.1111/j.1462-2920.2008.01642.x

    Article  CAS  Google Scholar 

  • Schalk J, De VS, Kuenen JG, Jetten MS (2000) Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39:5405–5412. doi:10.1021/bi992721k

    Article  CAS  Google Scholar 

  • Schluter J, Nadell Carey D, Bassler BL, Foster KR (2015) Adhesion as a weapon in microbial competition. ISME J 9:139–149. doi:10.1038/ismej.2014.174

    Article  CAS  Google Scholar 

  • Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93–106. doi:10.1016/S0723-2020(00)80050-8

    Article  CAS  Google Scholar 

  • Schmid M, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damsté JS, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp. Nov., Candidatus “Scalindua wagneri”, sp. Nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538. doi:10.1078/072320203770865837

    Article  CAS  Google Scholar 

  • Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM, Pommerening RA, op den Camp HJM, Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10:3140–3149. doi:10.1111/j.1462-2920.2008.01732.x

    Article  CAS  Google Scholar 

  • Shen LD, Hu AH, Jin RC, Cheng DQ, Zheng P, Xu XY, Hu BL (2012) Enrichment of anammox bacteria from three sludge sources for the startup of monosodium glutamate industrial wastewater treatment system. J Hazard Mater 199–200:193–199. doi:10.1016/j.jhazmat.2011.10.081

    Article  CAS  Google Scholar 

  • Shimamura M, Nishiyama T, Shigetomo H (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium- oxidizing enrichment culture. Appl Environ Microbiol 73:1065–1072. doi:10.1128/AEM.01978-06

    Article  CAS  Google Scholar 

  • Shimamura M, Nishiyama T, Shinya K, Kawahara Y, Furukawa K, Fujii T (2008) Another multiheme protein, hydroxylamine oxidoreductase abundantly produced in an anammox bacterium besides the hydrazine-oxidizing enzyme. J Biosci Bioeng 105:243–248. doi:10.1263/jbb.105.432

    Article  CAS  Google Scholar 

  • Sinninghe Damste JS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, Van Duin ACT, Van Niftrik LA, Jetten MSM (2002) Linearly concatenated cyclobutane lipids form adense bacterial membrane. Nature 419:708–712. doi:10.1038/nature01128

    Article  CAS  Google Scholar 

  • Song YX, Liao Q, Chai LY, Yu C, Duan CS, Peng C, Tang CJ (2017) Physicochemical and microbial properties of settled and floated anammox granules in upflow reactor. Biochem Eng J. Accepted

  • Speth DR, Guerrero-Cruz S, Dutilh BE, Jetten MSM (2016) Genome-based microbial ecology of anammox granules in a full-scale wastewater treatment system. Nature Comm 7:11172. doi:10.1038/ncomms11172

    Article  CAS  Google Scholar 

  • Strous M, Van Gerven E, Kuenen JG, Jetten M (1997) Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (Anammox) sludge. App Environ Microbiol 63:2446–2448.

    CAS  Google Scholar 

  • Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (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. doi:10.1007/s002530051340

    Article  CAS  Google Scholar 

  • Strous M, Pelletier E, Mangenot S et al (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794. doi:10.1038/nature04647

    Article  Google Scholar 

  • Sultan M (2016) Polyurethane for removal of organic dyes from textile wastewater. Environ Chem Lett. doi:10.1007/s10311-016-0597-8

    Google Scholar 

  • Tang CJ, Zheng P, Zhang L (2008) Seeding sludge and start-up strategy for Anammox bioreactor. China Water Wastewater 24:15–20 (in Chinese)

    CAS  Google Scholar 

  • Tang CJ, Zheng P, Mohmmod Q, Chen JW (2009a) Start-up and inhibition analysis of the Anammox process seeded with anaerobic granular sludge. J Ind Microbiol Biotechnol 36:1093–1100. doi:10.1007/s10295-009-0593-0

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Qaisar M (2009b) The shear force amendments on the slugging behavior of upflow Anammox granular sludge bed reactor. Sep Purif Technol 69:262–268. doi:10.1016/j.seppur.2009.07.029

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Hu BL, Chen JW, Wang CH (2010a) Influence of substrates on nitrogen removal performance and microbiology of anaerobic ammonium oxidation by operating two UASB reactors fed with different substrate levels. J Hazard Mater 181:19–26. doi:10.1016/j.jhazmat.2010.04.015

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Wang CH, Mohmmod Q (2010b) Suppression of anaerobic ammonium-oxidizers under high organic content in high-rate Anammox UASB reactor. Bioresour Technol 101:1762–1768. doi:10.1016/j.biortech.2009.10.032

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Zhang L, Chen JW, Mohmmod Q, Chen XG, Hu BL, Wang CH, Yu Y (2010c) Enrichment features of anammox consortia from methanogenic granules loaded with high organic and methanol content. Chemosphere 79:613–619. doi:10.1016/j.chemosphere.2010.02.045

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Chen TT, Qaisar M, Zhang JQ, Ding S, Chen XG, Chen JW, Wu DT (2011a) Enhanced nitrogen removal from pharmaceutical wastewater using SBA-ANAMMOX process. Water Res 45:201–210. doi:10.1016/j.watres.2010.08.036

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Wang CH, Mohmmod Q, Zhang JQ, Chen XG, Zhang L, Chen JW (2011b) Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res 45:135–144. doi:10.1016/j.watres.2010.08.018

    Article  CAS  Google Scholar 

  • Tang CJ, He R, Zheng P, Chai LY, Min XB (2013a) Mathematical modeling of high-rate Anammox UASB reactor based on granular packing patterns. J Hazard Mater 250–251:1–8. doi:10.1016/j.jhazmat.2013.01.058

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Chai LY, Min XB (2013b) Characterization and quantification of anammox start-up in UASB reactors seeded with conventional activated sludge. Int Biodeterior Biodegr 82:141–148. doi:10.1016/j.ibiod.2013.02.014

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Chai LY, Min XB (2013c) Thermodynamic and kinetic investigation of anaerobic bioprocesses on ANAMMOX under high organic conditions. Chem Eng J 230:149–157. doi:10.1016/j.cej.2013.06.047

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Ding S, Lu HF (2014) Enhanced nitrogen removal from ammonium-rich wastewater containing high organic contents by coupling with novel high-rate ANAMMOX granules addition. Chem Eng J 240:454–461. doi:10.1016/j.cej.2013.11.052

    Article  CAS  Google Scholar 

  • Tappin AD, Loughnane JP, McCarthy AJ, Fitzsimons MF (2016) Unexpected removal of the most neutral cationic pharmaceutical in river waters. Environ Chem Lett 14:455. doi:10.1007/s10311-016-0582-2

    Article  CAS  Google Scholar 

  • Trigo C, Campos JL, Garrido JM, Mendez R (2006) Start-up of the Anammox process in a membrane bioreactor. J Biotechnol 126:475–487. doi:10.1016/j.jbiotec.2006.05.008

    Article  CAS  Google Scholar 

  • Trubetskaya OE, Richard C, Trubetskoj OA (2016) High amounts of free aromatic amino acids in the protein-like fluorescence of water-dissolved organic matter. Environ Chem Lett 14:495–500. doi:10.1007/s10311-016-0556-4

    Article  CAS  Google Scholar 

  • Tsuneda S, Nagano T, Hoshino T (2003) Characterization of nitrifying granules produced in an aerobic upflow fluidized bed reactor. Water Res 37:4965–4973. doi:10.1016/j.watres.2003.08.017

    Article  CAS  Google Scholar 

  • Tsushima I, Ogasawara Y, Kindaichi T, Okabe S (2007) Development of high-rate anaerobic ammonium-oxidizing (Anammox) biofilm reactors. Water Res 41:1623–1634. doi:10.1016/j.watres.2007.01.050

    Article  CAS  Google Scholar 

  • Van De Vossenberg J, Woebken D, Maalcke WJ, Wessels HJ, Dutilh BE, Kartal B, Janssen-Megens EM, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, Van Der Biezen E, Pluk W, Francoijs KJ, Russ L, Lam P, Malfatti SA, Tringe SG, Haaijer SC, Op den Camp HJ, Stunnenberg HG, Amann R, Kuypers MM, Jetten MS (2013) The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol 15:1275–1289. doi:10.1111/j.1462-2920.2012.02774.x

    Article  CAS  Google Scholar 

  • Van der Star WRL, Abma WR, Bolmmers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, van Loosdrecht MCM (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41:4149–4163. doi:10.1016/j.watres.2009.09.051

    Article  CAS  Google Scholar 

  • Van Loosdrecht MCM, Jetten M (1998) Microbiological conversions in nitrogen removal. Water Sci Technol 38:1–7. doi:10.1016/S0273-1223(98)00383-7

    Article  Google Scholar 

  • Van Niftrik L, Van Helden M, Kirchen S, van Donselaar EG, Harhangi HR, Webb RI, Fuerst JA, Op den Camp HJ, Jetten MS, Strous M (2010) Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium ‘Candidatus Kuenenia stuttgartiensis’. Molecul Microbiol 77:701–715. doi:10.1111/j.1365-2958.2010.07242.x

    Article  CAS  Google Scholar 

  • Vazquez-Padin J, Mosquera-Corral A, Campos JL, Mendez R, Revsbech NP (2010) Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Res 44:4359–4370. doi:10.1016/j.watres.2010.05.041

    Article  CAS  Google Scholar 

  • Vlaeminck S, Terada A, Smets BF, De Clippeleir H, Schaubroeck T, Bolca S, Demeestere L, Mast J, Boon N, Carballa M, Verstraete W (2010) Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and Anammox. Appl Environ Microbiol 76:900–909. doi:10.1128/AEM.02337-09

    Article  CAS  Google Scholar 

  • Wang C, Lee P, Kumar M, Huang YT, Sung S, Lin JG (2010a) Simultaneous partial nitrification, anaerobic ammonium oxidation and dentrification (SNAD) in a full-scale landfill leachate treatment plant. J Hazard Mater 175:622–628. doi:10.1016/j.jhazmat.2009.10.052

    Article  CAS  Google Scholar 

  • Wang ZX, Chai LY, Yang ZH, Wang YY, Wang HY (2010b) Identifying sources and assessing potential risk of heavy metals in soils from direct exposure to children in a mine-impacted city, Changsha, China. J Environ Qual 39:1616–1623. doi:10.2134/jeq2010.0007

    Article  CAS  Google Scholar 

  • Wang QW, Qin WQ, Chai LY, Li QZ (2014) Understanding the formation of colloidal mercury in acidic wastewater with high concentration of chloride ions by electrocapillary curves. Environ Sci Pollut Res 21:3866–3872. doi:10.1007/s11356-013-2379-1

    Article  CAS  Google Scholar 

  • Wang SL, Hong YG, Wu JP, Xu XR, Bin LY, Pan YP, Guan FJ, Wen JL (2015a) Comparative analysis of two 16S rRNA gene-based PCR primer sets provides insight into the diversity distribution patterns of anammox bacteria in different environments. Appl Microbiol Biotechnol 99:8163–8176. doi:10.1007/s00253-015-6814-8

    Article  CAS  Google Scholar 

  • Wang T, Zhang LY, Li CF, Yang WC, Song TT, Tang CJ, Meng Y, Dai S, Wang HY, Chai LY, Luo J (2015b) Synthesis of core-shell magnetic Fe3O4@poly(m-Phenylenediamine) particles for chromium reduction and adsorption. Environ Sci Technol 49(9):5654–5662. doi:10.1021/es5061275

    Article  CAS  Google Scholar 

  • Wang SH, Guo JB, Lian J, Ngo HH, Guo WS, Liu YM, Song YY (2016) Rapid start-up of the anammox process by denitrifying granular sludge and the mechanism of the anammox electron transport chain. Biochem Eng J 115:101–107. doi:10.1016/j.bej.2016.09.001

    Article  CAS  Google Scholar 

  • Wei Z, Spinney R, Ke R, Yang Z, Xiao R (2016) Effect of pH on the sonochemical degradation of organic pollutants. Environ Chem Lett 14(2):163–182. doi:10.1007/s10311-016-0557-3

    Article  CAS  Google Scholar 

  • Wett B (2006) Solved upscaling problems for implementing deammonification of rejection water. Water Sci Technol 53:121–128. doi:10.2166/wst.2006.413

    Article  CAS  Google Scholar 

  • Wiszniowski J, Robert D, Surmacz-Gorska J, Miksch K, Weber JV (2006) Landfill leachate treatment methods: a review. Environ Chem Lett 4:51–61. doi:10.1007/s10311-005-0016-z

    Article  CAS  Google Scholar 

  • Woebken D, Lam P, Kuypers MM, Naqvi SW, Kartal B, Strous M, Jetten MS, Fuchs BM, Amann R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10:3106–3119. doi:10.1111/j.1462-2920.2008.01640.x

    Article  CAS  Google Scholar 

  • Wu J, Zhou HM, Li HZ, Zhang PC, Jiang J (2009) Impacts of hydrodynamic shear force on nucleation of flocculent sludge in anaerobic reactor. Water Res 43:3029–3036

    Article  CAS  Google Scholar 

  • Wu Z, Hua Z, Yuan XZ, Wang H, Wang LL, Chen XH, Zeng GM, Wu W (2014) Adsorptive removal of methylene blue by rhamnolipid-functionalized graphene oxide from wastewater. Water Res 67:330–344. doi:10.1016/j.watres.2014.09.026

    Article  CAS  Google Scholar 

  • Wu YD, Zhou KG, Dong SY, Yu W, Zhang HQ (2015) Recovery of gallic acid from gallic acid processing wastewater. Environ Technol 36:661–666. doi:10.1080/09593330.2014.957246

    Article  CAS  Google Scholar 

  • Xiang KS, Liu H, Yang BT, Zhang C, Yang S, Liu ZL, Liu C, Xie XF, Chai LY, Min XB (2016) Selenium catalyzed Fe(III)-EDTA reduction by Na2SO3: a reaction-controlled phase transfer catalysis. Environ Sci Pollut Res 8:8113–8119. doi:10.1007/s11356-016-6267-3

    Article  CAS  Google Scholar 

  • Xiao R, Wei Z, Chen D, Weavers LK (2014) Kinetics and mechanism of sonochemical degradation of pharmaceuticals in municipal wastewater. Environ Sci Technol 48:9675–9683. doi:10.1021/es5016197

    Article  CAS  Google Scholar 

  • Xiao R, Arnot JR, MacLeod M (2015a) Towards an improved understanding of processes controlling absorption efficiency and biomagnification of organic chemicals by fish. Chemosphere 138:89–95. doi:10.1016/j.chemosphere.2015.05.053

    Article  CAS  Google Scholar 

  • Xiao R, Ye T, Wei Z, Luo S, Yang Z, Spinney R (2015b) Quantitative structure-activity relationship (QSAR) for the oxidation of trace organic contaminants by sulfate radical. Environ Sci Technol 49:13394–13402. doi:10.1021/acs.est.5b03078

    Article  CAS  Google Scholar 

  • Xiao R, Zammit I, Wei Z, MacLeod M, Spinney R (2015c) Kinetics and mechanism of the oxidation of cyclosiloxanes by hydroxyl radical in the gas phase: an experimental and theoretical study. Environ Sci Technol 49:13322–13330. doi:10.1021/acs.est.5b03744

    Article  CAS  Google Scholar 

  • Xie WM, Ni BJ, Seviour T, Yu HQ (2013) Evaluating the impact of operational parameters on the formation of soluble microbial products (SMP) by activated sludge. Water Res 47:1073–1079. doi:10.1016/j.watres.2012.11.022

    Article  CAS  Google Scholar 

  • Xing BS, Guo Q, Yang GF, Zhang ZZ, Li P, Guo LX, Jin RC (2015) The properties of anaerobic ammonium oxidation (anammox) granules: roles of ambient temperature, salinity and calcium concentration. Sep Purif Technol 147:311–318. doi:10.1016/j.seppur.2015.04.035

    Article  CAS  Google Scholar 

  • Xiong L, Wang YY, Tang CJ, Chai LY, Xu KQ, Song YX, Ali M, Zheng P (2013) Start-up characteristics of a granule-based Anammox UASB reactor seeded with anaerobic granular sludge. BioMed Res Int. doi:10.1155/2013/396487

    Google Scholar 

  • Xue S, Ma Y, Zhou X, Liu F (2011) Screening and biological characteristics of a manganese tolerant microorganism. Environ Eng Manag J 10:881–885

    CAS  Google Scholar 

  • Yan X, Li QZ, Chai LY, Yang BT, Wang QW (2014) Formation of abiological granular sludge – A facile and bioinspired proposal for improving sludge settling performance during heavy metal wastewater treatment. Chemosphere 113:36–41. doi:10.1016/j.chemosphere.2014.04.038

    Article  CAS  Google Scholar 

  • Yan X, Chai L, Li Q, Ye L, Yang B, Wang Q (2017) Abiological Granular Sludge Formation Benefit for Heavy Metal Wastewater Treatment Using Sulfide Precipitation. CLEAN-Soil, Air, Water, doi:10.1002/clen.201500730

    Google Scholar 

  • Yang QX, Jia ZJ, Liu RY, Chen JJ (2007) Molecular diversity and anammox activity of novel planctomycete-like bacteria in the wastewater treatment system of a full-scale alcohol manufacturing plant. Process Biochem 42:180–187. doi:10.1016/j.procbio.2006.07.032

    Article  CAS  Google Scholar 

  • Yang J, Chai LY, Wang YY, He XW, Wang JL (2010) Transportation and distribution of chromium in the anaerobic sludge treating the chromium-containing wastewater. Int J Environ Pollut 38:256–266. doi:10.1504/IJEP.2009.027226

    Article  Google Scholar 

  • Yang Y, Liu H, Xiang XH (2013) Outline of occupational chromium poisoning in China. Bull Environ Contam Toxicol 90:742–749. doi:10.1007/s00128-013-0998-3

    Article  CAS  Google Scholar 

  • Yin L, Li X, Liu Y, Zhang D, Zhang S, Luo X (2012) Biodegradation of cypermethrin by rhodopseudomonas palustris GJ-22 isolated from activated sludge. Fresen Environ Bull 21:397–405

    CAS  Google Scholar 

  • Yu C, Song YX, Chai LY, Duan CS, Tang CJ, Ali M, Peng C (2016) Comparative evaluation of short-term stress of Cd(II), Hg(II), Pb(II), As(III) and Cr(VI) on anammox granules by batch test. J Biosci Bioeng 122:722–729. doi:10.1016/j.jbiosc.2016.06.008

    Article  CAS  Google Scholar 

  • Yuan SJ, Sun M, Sheng GP, Li Y, Li WW, Yao RS, Yu HQ (2010) Identification of key constituents and structure of the extracellular polymeric substances excreted by Bacillus megaterium TF10 for their flocculation capacity. Environ Sci Technol 145:1152–1157. doi:10.1021/es1030905

    Google Scholar 

  • Zhang Y, Xie JP, Liu MM, Tian Z, He ZL, Joy D, Nostrand Van, Ren LR, Zhou JZ, Yang M (2013) Microbial community functional structure in response to antibiotics in pharmaceutical wastewater treatment systems. Water Res 47:6298–6308. doi:10.1016/j.watres.2013.08.003

    Article  CAS  Google Scholar 

  • Zhang L, Zhang SJ, Peng YZ, Han XY, Gan YP (2015) Nitrogen removal performance and microbial distribution in pilot- and full-scale integrated fixed-biofilm activated sludge reactors based on nitritation-anammox process. Bioresour Technol 196:448–453. doi:10.1016/j.biortech.2015.07.090

    Article  CAS  Google Scholar 

  • Zhang ZZ, Xu JJ, Hu HY, Shi ZJ, Ji ZQ, Deng R, Shi ML, Jin RC (2016) Insight into the short- and long-term effects of inorganic phosphate on anammox granule property. Bioresour Technol 208:161–169. doi:10.1016/j.biortech.2016.02.097

    Article  CAS  Google Scholar 

  • Zheng YM, Yu HQ (2007) Determination of the pore size distribution and porosity of aerobic granules using size-exclusion chromatography. Water Res 41:39–46

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Acknowledgements

Financial support of this work by the National Natural Science Foundations of China (51674305, 51204213) is gratefully acknowledged.

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Tang, CJ., Duan, CS., Yu, C. et al. Removal of nitrogen from wastewaters by anaerobic ammonium oxidation (ANAMMOX) using granules in upflow reactors. Environ Chem Lett 15, 311–328 (2017). https://doi.org/10.1007/s10311-017-0607-5

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