Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH ARTICLE

Response mechanism of denitrifying anaerobic methane oxidation microorganisms to ammonia

Juqing Lou https://orcid.org/0000-0001-9078-0319 A B , Jiaping Li A and Xilei Wang A
+ Author Affiliations
- Author Affiliations

A School of Environmental Science and Engineering, Zhejiang Gongshang University, Hangzhou 310012, China.

B Corresponding author. Email: ljq7393@163.com

Environmental Chemistry 17(1) 17-27 https://doi.org/10.1071/EN19127
Submitted: 9 February 2019  Accepted: 22 July 2019   Published: 20 August 2019

Environmental context. Denitrifying anaerobic methane oxidation (DAMO) is a new process in wastewater treatment with the potential to provide cheap and sustainable development. To better apply this technology to the large scale, we studied the response mechanism of DAMO microorganisms to ammonia, the main form of nitrogen in the nitrogenous wastewater. The results can provide a theoretical basis for the stable and efficient operation of DAMO processes.

Abstract. The dominant microorganisms in the denitrifying anaerobic methane oxidation (DAMO) process are primarily DAMO bacteria and DAMO archaea, which can simultaneously realise methane oxidation and denitrification. Ammonia is the primary form of nitrogen found in wastewater. This study focuses on a coexistence system that contains both DAMO bacteria and DAMO archaea (DAMO co-system). The short- and long-term effects of NH4+-N on the DAMO co-system were investigated at both the macro level (such as denitrification performance) and the micro level (such as microbial structure and community). Short-term experimental studies demonstrated that the safe concentration of ammonia for this system was 250 mg N L−1. When the ammonia concentration was 500 mg N L−1, the nitrogen removal efficiency was significantly inhibited. With an increase in concentration and an extension of time, the inhibitory effect of ammonia was enhanced. Long-term experimental studies showed that the nitrogen removal performance of DAMO was completely inhibited when the ammonia concentration reached 1000 mg N L−1 and that ammonia had a toxic accumulation effect on the DAMO co-system. The results of the pH experimental study demonstrated that free ammonia (FA) was the limiting factor in the alkaline condition, while ionised NH4+ was the limiting factor in neutral and acidic conditions. Scanning electron microscopy (SEM) demonstrated that the microbes in the DAMO co-system shrank after short-term exposure and that the microorganisms shrank in the shape of polygons. High-throughput sequencing analysis demonstrated that the community structure of the DAMO co-system changed substantially, and the species diversity and abundance decreased distinctly after long-term inhibition. A genus analysis indicated that the reduction in Nitrospirae may be an internal reason for the decrease in the denitrification performance of the DAMO co-system.

Additional keywords: co-existence system, microbial population structure, microbial structure, N-DAMO archaea, N-DAMO bacteria.


References

Allegue T, Arias A, Fernandez-Gonzalez N, Omil F, Garrido JM (2018). Enrichment of nitrite-dependent anaerobic methane oxidizing bacteria in a membrane bioreactor. Chemical Engineering Journal 347, 721–730.
Enrichment of nitrite-dependent anaerobic methane oxidizing bacteria in a membrane bioreactorCrossref | GoogleScholarGoogle Scholar |

Chen J, Gu JD (2017). Faunal Burrows Alter the Diversity, Abundance, and Structure of AOA, AOB, Anammox and n-Damo Communities in Coastal Mangrove Sediments. Microbial Ecology 74, 140–156.
Faunal Burrows Alter the Diversity, Abundance, and Structure of AOA, AOB, Anammox and n-Damo Communities in Coastal Mangrove SedimentsCrossref | GoogleScholarGoogle Scholar | 28130576PubMed |

Chen J, Jiang XW, Gu JD (2015a). Existence of novel phylotypes of nitrite dependent anaerobic methane oxidizing bacteria in surface and subsurface sediments of the South China Sea. Geomicrobiology Journal 32, 1–10.
Existence of novel phylotypes of nitrite dependent anaerobic methane oxidizing bacteria in surface and subsurface sediments of the South China SeaCrossref | GoogleScholarGoogle Scholar |

Chen J, Zhou ZC, Gu JD (2015b). Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genes. Applied Microbiology and Biotechnology 99, 1463–1473.
Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genesCrossref | GoogleScholarGoogle Scholar | 25219532PubMed |

Chronopoulou PM, Shelley F, Pritchard WJ, Maanoja ST, Trimmer M (2017). Origin and fate of methane in the Eastern Tropical North Pacific oxygen minimum zone. The ISME Journal 11, 1386–1399.
Origin and fate of methane in the Eastern Tropical North Pacific oxygen minimum zoneCrossref | GoogleScholarGoogle Scholar | 28244978PubMed |

Chu ZR, Wang K, Li XK, Zhu MT, Yang L, Zhang J (2015). Microbial characterization of aggregates within a one-stage nitritation-anammox system using high-throughput amplicon sequencing. Chemical Engineering Journal 262, 41–48.
Microbial characterization of aggregates within a one-stage nitritation-anammox system using high-throughput amplicon sequencingCrossref | GoogleScholarGoogle Scholar |

Costa RB, Okada DY, Delforno TP, Foresti E (2019). Methane-oxidizing archaea, aerobic methanotrophs and nitrifiers coexist with methane as the sole carbon source. International Biodeterioration & Biodegradation 138, 57–62.
Methane-oxidizing archaea, aerobic methanotrophs and nitrifiers coexist with methane as the sole carbon sourceCrossref | GoogleScholarGoogle Scholar |

Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999). The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set. Systematic and Applied Microbiology 22, 434–444.
The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe SetCrossref | GoogleScholarGoogle Scholar | 10553296PubMed |

Duan HR, Ye L, Lu XY, Yuan ZG (2019). Overcoming nitrite oxidizing bacteria adaptation through alternating sludge treatment with free nitrous acid and free ammonia. Environmental Science & Technology 53, 1937–1946.
Overcoming nitrite oxidizing bacteria adaptation through alternating sludge treatment with free nitrous acid and free ammoniaCrossref | GoogleScholarGoogle Scholar |

Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJM, Jetten MSM, Strous M (2008). Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environmental Microbiology 10, 3164–3173.
Denitrifying bacteria anaerobically oxidize methane in the absence of ArchaeaCrossref | GoogleScholarGoogle Scholar | 18721142PubMed |

Fernandes TV, Keesman KJ, Zeeman G, van Lier JB (2012). Effect of ammonia on the anaerobic hydrolysis of cellulose and tributyrin. Biomass and Bioenergy 47, 316–323.
Effect of ammonia on the anaerobic hydrolysis of cellulose and tributyrinCrossref | GoogleScholarGoogle Scholar |

Fu L, Ding J, Lu YZ, Ding ZW, Zeng RJ (2017). Nitrogen source effects on the denitrifying anaerobic methane oxidation culture and anaerobic ammonium oxidation bacteria enrichment process. Applied Microbiology and Biotechnology 101, 3895–3906.
Nitrogen source effects on the denitrifying anaerobic methane oxidation culture and anaerobic ammonium oxidation bacteria enrichment processCrossref | GoogleScholarGoogle Scholar | 28168315PubMed |

Fu L, Zhang F, Bai YN, Lu YZ, Ding J, Zhou DD (2019). Mass transfer affects reactor performance, microbial morphology, and community succession in the methane-dependent denitrification and anaerobic ammonium oxidation co-culture. The Science of the Total Environment 651, 291–297.
Mass transfer affects reactor performance, microbial morphology, and community succession in the methane-dependent denitrification and anaerobic ammonium oxidation co-cultureCrossref | GoogleScholarGoogle Scholar | 30236845PubMed |

Fukunaga Y, Kurahashi M, Sakiyama Y, Ohuchi M, Yokota A, Harayama S (2009). Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum Planctomycetes. The Journal of General and Applied Microbiology 55, 267–275.
Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum PlanctomycetesCrossref | GoogleScholarGoogle Scholar | 19700920PubMed |

Gusmão VR, Chinalia FA, Sakamoto IK, Varesche MBA (2007). Performance of a reactor containing denitrifying immobilized biomass in removing ethanol and aromatic hydrocarbons (BTEX) in a short operating period. Journal of Hazardous Materials 139, 301–309.
Performance of a reactor containing denitrifying immobilized biomass in removing ethanol and aromatic hydrocarbons (BTEX) in a short operating periodCrossref | GoogleScholarGoogle Scholar | 16872740PubMed |

He ZF, Geng S, Shen LD, Lou LP, Zheng P, Xu XH, Hu BL (2015). The short- and long-term effects of environmental conditions on anaerobic methane oxidation coupled to nitrite reduction. Water Research 68, 554–562.
The short- and long-term effects of environmental conditions on anaerobic methane oxidation coupled to nitrite reductionCrossref | GoogleScholarGoogle Scholar |

Hu SH (2012). Enrichment and understanding of denitrifying anaerobic methane oxidation (DAMO) organism. PhD thesis, The University of Queensland.

Lee J, Koo T, Yulisa A, Hwang S (2019). Magnetite as an enhancer in methanogenic degradation of volatile fatty acids under ammonia-stressed condition. Journal of Environmental Management 241, 418–426.
Magnetite as an enhancer in methanogenic degradation of volatile fatty acids under ammonia-stressed conditionCrossref | GoogleScholarGoogle Scholar | 31035235PubMed |

Li J, Qi PQ, Qiang ZM, Dong HY, Gao DW, Wang D (2018). Is anammox a promising treatment process for nitrogen removal from nitrogen-rich saline wastewater?. Bioresource Technology 270, 722–731.
Is anammox a promising treatment process for nitrogen removal from nitrogen-rich saline wastewater?Crossref | GoogleScholarGoogle Scholar | 30193879PubMed |

Long Y, Liu C, Lin H, Li N, Guo Q, Xie S (2017). Vertical and horizontal distribution of sediment nitrite-dependent methane-oxidizing organisms in a mesotrophic freshwater reservoir. Canadian Journal of Microbiology 63, 525–534.
Vertical and horizontal distribution of sediment nitrite-dependent methane-oxidizing organisms in a mesotrophic freshwater reservoirCrossref | GoogleScholarGoogle Scholar | 28177782PubMed |

Lou JQ, Li JP, Wang XL (2018a). Effect mechanism of ammonia on denitrifying anaerobic methane oxidation bacteria. Acta Scientiae Circumstantiae 08, 3036–3044. [in Chinese]

Lou JQ, Wang XL, Li JP, Han JY (2018b). The short- and long-term effects of nitrite on denitrifying anaerobic methane oxidation (DAMO) organisms. Environmental Science and Pollution Research International 5, 4777–4790.

Lu HJ, Chandran K, Stensel D (2014). Microbial ecology of denitrification in biological wastewater treatment. Water Research 64, 237–254.
Microbial ecology of denitrification in biological wastewater treatmentCrossref | GoogleScholarGoogle Scholar |

Lu YZ, Fu L, Li N, Ding J, Bai YN, Samaras P, Raymond JXZ (2018). The content of trace element iron is a key factor for competition between anaerobic ammonium oxidation and methane-dependent denitrification processes. Chemosphere 198, 370–376.
The content of trace element iron is a key factor for competition between anaerobic ammonium oxidation and methane-dependent denitrification processesCrossref | GoogleScholarGoogle Scholar | 29421752PubMed |

Lu PL, Liu T, Ni BJ, Guo JH, Yuan ZG, Hu SH (2019). Growth kinetics of Candidatus ‘Methanoperedens nitroreducens’ enriched in a laboratory reactor. Science of the Total Environment 659, 442–450.
Growth kinetics of Candidatus ‘Methanoperedens nitroreducens’ enriched in a laboratory reactorCrossref | GoogleScholarGoogle Scholar |

Luo JH, Chen H, Yuan ZG, Guo JH (2018). Methane-supported nitrate removal from groundwater in a membrane biofilm reactor. Water Research 132, 71–78.
Methane-supported nitrate removal from groundwater in a membrane biofilm reactorCrossref | GoogleScholarGoogle Scholar | 29306701PubMed |

Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV, Ravin NV, Bonch-Osmolovskaya EA, Kublanov IV (2013). Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environmental Microbiology 15, 1759–1771.
Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum IgnavibacteriaeCrossref | GoogleScholarGoogle Scholar | 23297868PubMed |

Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damsté JSS, Op den Camp HJM, Jetten MSM, Strous M (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440, 918–921.
A microbial consortium couples anaerobic methane oxidation to denitrificationCrossref | GoogleScholarGoogle Scholar | 16612380PubMed |

Reed DC, Harrison JA (2016). Linking nutrient loading and oxygen in the coastal ocean: A new global scale model. Global Biogeochemical Cycles 30, 447–459.
Linking nutrient loading and oxygen in the coastal ocean: A new global scale modelCrossref | GoogleScholarGoogle Scholar |

Roy C, Bakshi U, Rameez MJ, Mandala SS, Haldar PK, Pyne P, Ghosh W (2019). Phylogenomics of an uncultivated, aerobic and thermophilic, photoheterotrophic member of Chlorobia sheds light into the evolution of the phylum Chlorobi. Computational Biology and Chemistry 80, 206–216.
Phylogenomics of an uncultivated, aerobic and thermophilic, photoheterotrophic member of Chlorobia sheds light into the evolution of the phylum ChlorobiCrossref | GoogleScholarGoogle Scholar | 30981103PubMed |

Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ (2016). Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351, 703–707.
Artificial electron acceptors decouple archaeal methane oxidation from sulfate reductionCrossref | GoogleScholarGoogle Scholar | 26912857PubMed |

Shen LD, Ouyang L, Zhu YZ, Trimmer M (2019). Active pathways of anaerobic methane oxidation across contrasting riverbeds. The ISME Journal 13, 752–766.
Active pathways of anaerobic methane oxidation across contrasting riverbedsCrossref | GoogleScholarGoogle Scholar | 30375505PubMed |

Siniscalchi LAB, Leite LR, Oliveira G, Chernicharo CAL, de Araújo JC (2017). Illumina sequencing-based analysis of a microbial community enriched under anaerobic methane oxidation condition coupled to denitrification revealed coexistence of aerobic and anaerobic methanotrophs. Environmental Science and Pollution Research 24, 16751–16764.
Illumina sequencing-based analysis of a microbial community enriched under anaerobic methane oxidation condition coupled to denitrification revealed coexistence of aerobic and anaerobic methanotrophsCrossref | GoogleScholarGoogle Scholar | 28567677PubMed |

Sun SP, Nàcher CPN, Merkey B, Zhou Q, Xia SQ, Yang DH, Sun JH, Smets BF (2010). Effective Biological Nitrogen Removal Treatment Processes for Domestic Wastewaters with Low C/N Ratios: A Review. Environmental Engineering Science 27, 111–126.
Effective Biological Nitrogen Removal Treatment Processes for Domestic Wastewaters with Low C/N Ratios: A ReviewCrossref | GoogleScholarGoogle Scholar |

Tian HL, Mancini E, Treu L, Angelidaki I, Fotidis IA (2019). Bioaugmentation strategy for overcoming ammonia inhibition during biomethanation of a protein-rich substrate. Chemosphere 231, 415–422.
Bioaugmentation strategy for overcoming ammonia inhibition during biomethanation of a protein-rich substrateCrossref | GoogleScholarGoogle Scholar |

Wang Y, Zhu GB, Harhangi HR, Zhu BL, Jetten MSM, Yin CQ, Op den Camp HJM (2012). Co-occurrence and distribution of nitrite-dependent an-aerobic ammonium and methane oxidizing bacteria in a paddy soil. FEMS Microbiology Letters 336, 79–88.
Co-occurrence and distribution of nitrite-dependent an-aerobic ammonium and methane oxidizing bacteria in a paddy soilCrossref | GoogleScholarGoogle Scholar | 22889245PubMed |

Wang TZ, Li YK, Liang MC, Yang PL, Bai ZH (2014). Biofilms on the surface of gravels and aquatic plants in rivers and lakes with reusing reclaimed water. Environmental Earth Sciences 72, 743–755.
Biofilms on the surface of gravels and aquatic plants in rivers and lakes with reusing reclaimed waterCrossref | GoogleScholarGoogle Scholar |

Wang DB, Wang YL, Liu YW, Ngo HN, Lian Y, Zhao JW, Chen F, Yang Q, Zeng GM, Li XM (2017a). Is denitrifying anaerobic methane oxidation-centered technologies a solution for the sustainable operation of wastewater treatment plants?. Bioresource Technology 234, 456–465.
Is denitrifying anaerobic methane oxidation-centered technologies a solution for the sustainable operation of wastewater treatment plants?Crossref | GoogleScholarGoogle Scholar |

Wang DB, Fu QZ, Xu QX, Liu YW, Ngo HN, Yang Q, Zeng GM, Li XM, Ni BJ (2017b). Free nitrous acid-based nitrifying sludge treatment in a two-sludge system enhances nutrient removal from low-carbon wastewater. Bioresource Technology 244, 920–928.
Free nitrous acid-based nitrifying sludge treatment in a two-sludge system enhances nutrient removal from low-carbon wastewaterCrossref | GoogleScholarGoogle Scholar |

Wang YL, Wang DB, Yang Q, Zeng GM, Li XM (2017c). Wastewater Opportunities for Denitrifying Anaerobic Methane Oxidation. Trends in Biotechnology 35, 799–802.
Wastewater Opportunities for Denitrifying Anaerobic Methane OxidationCrossref | GoogleScholarGoogle Scholar |

Wang DB, Duan YY, Yang Q, Liu YW, Ni BJ, Wang QL, Zeng GM, Li XM, Yuan ZG (2018a). Free ammonia enhances dark fermentative hydrogen production from waste activated sludge. Water Research 133, 272–281.
Free ammonia enhances dark fermentative hydrogen production from waste activated sludgeCrossref | GoogleScholarGoogle Scholar |

Wang R, Li XF, Hou LJ, Liu M, Zheng YL, Yin GY, Yang Y (2018b). Nitrogen fixation in surface sediments of the East China Sea: Occurrence and environmental implications. Marine Pollution Bulletin 137, 542–548.
Nitrogen fixation in surface sediments of the East China Sea: Occurrence and environmental implicationsCrossref | GoogleScholarGoogle Scholar | 30503466PubMed |

Wei FS (2002). ‘The state environmental protection administration: water and wastewater monitoring and analysis method, 4th edn.’ (China Environmental Science Press: Beijing) (in Chinese)

Wei D, Ngo HH, Guo WS, Xu WY, Du B, Wei Q (2018). Partial nitrification granular sludge reactor as a pretreatment for anaerobic ammonium oxidation (Anammox): Achievement, performance and microbial community. Bioresource Technology 269, 25–31.
Partial nitrification granular sludge reactor as a pretreatment for anaerobic ammonium oxidation (Anammox): Achievement, performance and microbial communityCrossref | GoogleScholarGoogle Scholar | 30149251PubMed |

Wu Q, Chang JL, Yan XX, Ailijiang N, Fan QX, Wang SH, Liang P, Zhang XY, Huang X (2016). Electrical stimulation enhanced denitrification of nitrite-dependent anaerobic methane-oxidizing bacteria. Biochemical Engineering Journal 106, 125–128.
Electrical stimulation enhanced denitrification of nitrite-dependent anaerobic methane-oxidizing bacteriaCrossref | GoogleScholarGoogle Scholar |

Xie GJ, Liu T, Cai C, Hu SH, Yuan ZG (2018). Achieving high-level nitrogen removal in mainstream by coupling anammox with denitrifying anaerobic methane oxidation in a membrane biofilm reactor. Water Research 131, 196–204.
Achieving high-level nitrogen removal in mainstream by coupling anammox with denitrifying anaerobic methane oxidation in a membrane biofilm reactorCrossref | GoogleScholarGoogle Scholar | 29289920PubMed |

Xing W, Li JL, Li P, Wang C, Cao YN, Li DS, Yang YF, Zhou JZ, Zuo JN (2018). Effects of residual organics in municipal wastewater on hydrogenotrophic denitrifying microbial communities. Journal of Environmental Sciences 65, 262–270.
Effects of residual organics in municipal wastewater on hydrogenotrophic denitrifying microbial communitiesCrossref | GoogleScholarGoogle Scholar |

Yan WW, Lua D, Liu JB, Zhou Y (2019). The interactive effiects of ammonia and carbon nanotube on anaerobic digestion. Chemical Engineering Journal 372, 332–340.
The interactive effiects of ammonia and carbon nanotube on anaerobic digestionCrossref | GoogleScholarGoogle Scholar |

Yang DY (2015). ‘Enrichment and characteristic research of denitrifying anaerobic methane oxidaton microorganisms.’ (Zhejiang Gongshang University: Hangzhou) (in Chinese)

Yang GJ, Xu QX, Wang DB, Tang L, Xia JF, Wang QL, Zeng GM, Yang Q, Li XM (2018a). Free ammonia-based sludge treatment reduces sludge production in the wastewater treatment process. Chemosphere 205, 484–492.
Free ammonia-based sludge treatment reduces sludge production in the wastewater treatment processCrossref | GoogleScholarGoogle Scholar |

Yang ZY, Wang W, He YF, Zhang RH, Liu GQ (2018b). Effect of ammonia on methane production, methanogenesis pathway, microbial community and reactor performance under mesophilic and thermophilic conditions. Renewable Energy 125, 915–925.
Effect of ammonia on methane production, methanogenesis pathway, microbial community and reactor performance under mesophilic and thermophilic conditionsCrossref | GoogleScholarGoogle Scholar |

Yu H, Kashima H, Regan JM, Hussain A, Elbeshbishy E, Lee H (2017a). Kinetic study on anaerobic oxidation of methane coupled to denitrification. Enzyme and Microbial Technology 104, 47–55.
Kinetic study on anaerobic oxidation of methane coupled to denitrificationCrossref | GoogleScholarGoogle Scholar | 28648180PubMed |

Yu H, Cui XF, Zhang RL (2017b). Experiment on degradation of coal adsorbed methane by anaerobic microorganism under simulated solid coal occurrence environment. Safety in Coal Mines 48, 1–4.

Yu GL, Peng HY, Fu YJ, Yan XJ, Du CY, Chen H (2019). Enhanced nitrogen removal of low C/N wastewater in constructed wetlands with co-immobilizing solid carbon source and denitrifying bacteria. Bioresource Technology 280, 337–344.
Enhanced nitrogen removal of low C/N wastewater in constructed wetlands with co-immobilizing solid carbon source and denitrifying bacteriaCrossref | GoogleScholarGoogle Scholar |

Zhang ZZ, Xu JJ, Shi ZJ, Cheng YF, Ji ZQ, Deng R, Jin RC (2017). Combined impacts of nanoparticles on anammox granules and the roles of EDTA and (S2-) in attenuation. Journal of Hazardous Materials 334, 49–58.
Combined impacts of nanoparticles on anammox granules and the roles of EDTA and (S2-) in attenuationCrossref | GoogleScholarGoogle Scholar | 28399429PubMed |

Zhang ZZ, Cheng YF, Xu LZJ, Bai YH, Jin RC (2018). Anammox granules show strong resistance to engineered silver nanoparticles during long-term exposure. Bioresource Technology 259, 10–17.
Anammox granules show strong resistance to engineered silver nanoparticles during long-term exposureCrossref | GoogleScholarGoogle Scholar | 29536867PubMed |

Zumft WG (1997). Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews 61, 533–616.