Abstract
Biological denitrification process in mainstream wastewater treatment often needs dosing supplemental electrons, consequently adding a remarkable operating cost. Organic carbon compounds are nowadays the most intensively used electron sources in full-scale wastewater treatment, corresponding with the well-understood carbon-nitrogen biogeochemistry for heterotrophic denitrification process. In the twenty-first century, the low-carbon technology is on calling to reduce the carbon footprint and relieve climate changing threatens. Autotrophic denitrification is highly recommended for mainstream wastewater treatment. The reduced-sulphur compounds (such as sulphide, elemental sulphur, and thiosulphate) could be utilised as electron donors, to drive sulphur cycle reactions to reduce nitrate and nitrite to dinitrogen gas. Based on the literature review and our own research experiences, this paper presents our perspectives on sulphur-driven autotrophic denitrification. It particularly focuses on the functional enzymes, sulphur bioreactors, and influential operating factors. Overall, this paper provides new insights on sulphur-nitrogen biogeochemistry and application as a low-carbon technology for nitrogen removal during municipal wastewater treatment.




Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
An S, Tang K, Nemati M (2010) Simultaneous biodesulphurization and denitrification using an oil reservoir microbial culture: effects of sulphide loading rate and sulphide to nitrate loading ratio. Water Res 44:1531–1541. https://doi.org/10.1016/j.watres.2009.10.037
Bartacek J, Manconi I, Sansone G, Murgia R, Lens PN (2010) Divalent metal addition restores sulfide-inhibited N2O reduction in Pseudomonas aeruginosa. Nitric Oxide 23:101–105. https://doi.org/10.1016/j.niox.2010.04.005
Baspinar AB, Turker M, Hocalar A, Ozturk I (2011) Biogas desulphurization at technical scale by lithotrophic denitrification: integration of sulphide and nitrogen removal. Process Biochem 46:916–922. https://doi.org/10.1016/j.procbio.2011.01.001
Bayrakdar A, Tilahun E, Calli B (2016) Biogas desulfurization using autotrophic denitrification process. Appl Microbiol Biotechnol 100:939–948. https://doi.org/10.1007/s00253-015-7017-z
Beller HR, Chain PS, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP (2006a) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188:1473–1488. https://doi.org/10.1128/JB.188.4.1473-1488.2006
Beller HR, Letain TE, Chakicherla A, Kane SR, Legler TC, Coleman MA (2006b) Whole-genome transcriptional analysis of chemolithoautotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J Bacteriol 188:7005–7015. https://doi.org/10.1128/JB.00568-06
Braker G, Zhou J, Wu L, Devol AH, Tiedje JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Appl Environ Microbiol 66:2096–2104. https://doi.org/10.1128/AEM.66.5.2096-2104.2000
Brüser T, Selmer T, Dahl C (2000a) “ADP sulfurylase” from Thiobacillus denitrificans is an adenylylsulfate: phosphate adenylyltransferase and belongs to a new family of nucleotidyl transferases. J Biol Chem 275:1691–1698. https://doi.org/10.1074/jbc.275.3.1691
Brüser T, Lens PNL, Trüper HG (2000b) The biological sulfur cycle. In: PNL L, Hulshoff Pol L (eds) Environmental technologies to treat sulfur pollution principles and engineering. IWA Publishing, London, pp 47–86
Butland G, Spiro S, Watmough NJ, Richardson DJ (2001) Two conserved glutamates in the bacterial nitric oxide reductase are essential for activity but not assembly of the enzyme. J Bacteriol 183:189–199. https://doi.org/10.1128/JB.183.1.189-199.2001
Campos JL, Carvalho S, Portela R, Mosquera-Corral A, Méndez R (2008) Kinetics of denitrification using sulphur compounds: effects of S/N ratio, endogenous and exogenous compounds. Bioresour Technol 99:1293–1299. https://doi.org/10.1016/j.biortech.2007.02.007
Can-Dogan E, Turker M, Dagasan L, Arslan A (2010) Sulfide removal from industrial wastewaters by lithotrophic denitrification using nitrate as an electron acceptor. Water Sci Technol 62:2286–2293. https://doi.org/10.2166/wst.2010.545
Cardoso RB, Sierra-Alvarez R, Rowlette P, Flores ER, Gómez J, Field JA (2006) Sulfide oxidation under chemolithoautotrophic denitrifying conditions. Biotechnol Bioeng 95:1148–1157. https://doi.org/10.1002/bit.21084
Chung Y-C, Huang C, Tseng C-P (2001) Biological elimination of H2S and NH3 from wastegases by biofilter packed with immobilized heterotrophic bacteria. Chemosphere 43:1043–1050. https://doi.org/10.1016/S0045-6535(00)00211-3
Chung J, Amin K, Kim S, Yoon S, Kwon K, Bae W (2014) Autotrophic denitrification of nitrate and nitrite using thiosulfate as an electron donor. Water Res 58:169–178. https://doi.org/10.1016/j.watres.2014.03.071
Claus G, Kutzner HJ (1985) Physiology and kinetics of autotrophic denitrification by Thiobacillus denitrificans. Appl Microbiol Biotechnol 22:283–288. https://doi.org/10.1007/BF00252031
Cox HHJ, Deshusses MA (2002) Co-treatment of H2S and toluene in a biotrickling filter. Chem Eng J 87:101–110. https://doi.org/10.1016/S1385-8947(01)00222-4
Cui Y, Wu D, Mackey H, Chui H, Chen G (2018) Application of a moving-bed biofilm reactor for sulfur-oxidizing autotrophic denitrification. Water Sci Technol 77:1027–1034. https://doi.org/10.2166/wst.2017.617
Dahl C (1996) Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142:3363–3372. https://doi.org/10.1099/13500872-142-12-3363
Dahl C (2008) Inorganic Sulfur Compounds as Electron Donors in Purple Sulfur Bacteria. In: Hell R, Dahl C, Knaff D, Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms. Springer Netherlands, Dordrecht, pp 289–317
Dahl C, Friedrich CG (2008) Microbial sulfur metabolism. Springer-Verlag, Berlin Heidelberg
Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O, Brune DC (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187:1392–1404. https://doi.org/10.1128/JB.187.4.1392-1404.2005
Dam B, Mandal S, Ghosh W, Gupta SK, Roy P (2007) The S4-intermediate pathway for the oxidation of thiosulfate by the chemolithoautotroph Tetrathiobacter kashmirensis and inhibition of tetrathionate oxidation by sulfite. Res Microbiol 158:330–338. https://doi.org/10.1016/j.resmic.2006.12.013
Deng L, Chen H, Chen Z, Liu Y, Pu X, Song L (2009) Process of simultaneous hydrogen sulfide removal from biogas and nitrogen removal from swine wastewater. Bioresour Technol 100:5600–5608. https://doi.org/10.1016/j.biortech.2009.06.012
Di Capua F, Papirio S, Lens PN, Esposito G (2015) Chemolithotrophic denitrification in biofilm reactors. Chem Eng J 280:643–657. https://doi.org/10.1016/j.cej.2015.05.131
Di Capua F, Ahoranta SH, Papirio S, Lens PN, Esposito G (2016) Impacts of sulfur source and temperature on sulfur-driven denitrification by pure and mixed cultures of Thiobacillus. Process Biochem 51:1576–1584. https://doi.org/10.1016/j.procbio.2016.06.010
Di Capua F, Milone I, Lakaniemi AM, Lens PN, Esposito G (2017) High-rate autotrophic denitrification in a fluidized-bed reactor at psychrophilic temperatures. Chem Eng J 313:591–598. https://doi.org/10.1016/j.cej.2016.12.106
Dolejs P, Paclík L, Maca J, Pokorna D, Zabranska J, Bartacek J (2015) Effect of S/N ratio on sulfide removal by autotrophic denitrification. Appl Microbiol Biotechnol 99:2383–2392. https://doi.org/10.1007/s00253-014-6140-6
Driscoll CT, Bisogni JJ (1978) The use of sulfur and sulfide in packed bed reactors for autotrophic denitrification. J Water Pollut Control Fed 50:569–577
Einsle O, Messerschmidt A, Stach P, Bourenkov GP, Bartunik HD, Huber R, Kroneck PM (1999) Structure of cytochrome c nitrite reductase. Nature 400:476–480. https://doi.org/10.1038/22802
Fajardo C, Mora M, Fernández I, Mosquera-Corral A, Campos JL, Méndez R (2014) Cross effect of temperature, pH and free ammonia on autotrophic denitrification process with sulphide as electron donor. Chemosphere 97:10–15. https://doi.org/10.1016/j.chemosphere.2013.10.028
Fernández N, Sierra-Alvarez R, Field JA, Amils R, Sanz JL (2008) Microbial community dynamics in a chemolithotrophic denitrification reactor inoculated with methanogenic granular sludge. Chemosphere 70:462–474. https://doi.org/10.1016/j.chemosphere.2007.06.062
Fernández M, Ramírez M, Gómez JM, Cantero D (2014) Biogas biodesulfurization in an anoxic biotrickling filter packed with open-pore polyurethane foam. J Hazard Mater 264:529–535. https://doi.org/10.1016/j.jhazmat.2013.10.046
Fida TT, Chen C, Okpala G, Voordouw G (2016) Implications of limited thermophilicity of nitrite reduction for control of sulfide production in oil reservoirs. Appl Environ Microbiol 82:4190–4199. https://doi.org/10.1128/AEM.00599-16
Flere JM, Zhang TC (1998) Sulfur-based autotrophic denitrification pond systems for in-situ remediation of nitrate-contaminated surface water. Water Sci Technol 38:15–22. https://doi.org/10.1016/S0273-1223(98)00385-0
Flere JM, Zhang TC (1999) Nitrate removal with sulfur-limestone autotrophic denitrification processes. J Environ Eng 125:721–729. https://doi.org/10.1061/(ASCE)0733-9372(1999)125:8(721)
Francis CA, Beman JM, Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1:19
Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882. https://doi.org/10.1128/AEM.67.7.2873-2882.2001
Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259. https://doi.org/10.1016/j.mib.2005.04.005
Frigaard NU, Dahl C (2008) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54:103–200. https://doi.org/10.1016/S0065-2911(08)00002-7
Furumai H, Tagui H, Fujita K (1996) Effects of pH and alkalinity on sulfur-denitrification in a biological granular filter. Water Sci Technol 34:355–362. https://doi.org/10.1016/0273-1223(96)00544-6
Gadekar S, Nemati M, Hill GA (2006) Batch and continuous biooxidation of sulphide by Thiomicrospirasp. CVO: reaction kinetics and stoichiometry. Water Res 40:2436–2446. https://doi.org/10.1016/j.watres.2006.04.007
Gevertz D, Telang AJ, Voordouw G, Jenneman GE (2000) Isolation and characterization of strains CVO and FWKO B, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Appl Environ Microbiol 66:2491–2501. https://doi.org/10.1128/AEM.66.6.2491-2501.2000
Ghosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev 33:999–1043. https://doi.org/10.1111/j.1574-6976.2009.00187.x
González PJ, Correia C, Moura I, Brondino CD, Moura JJG (2006) Bacterial nitrate reductases: molecular and biological aspects of nitrate reduction. J Inorg Biochem 100:1015–1023. https://doi.org/10.1016/j.jinorgbio.2005.11.024
Gonzalez PJ, Rivas MG, Mota CS, Brondino CD, Moura I, Moura JJ (2013) Periplasmic nitrate reductases and formate dehydrogenases: biological control of the chemical properties of Mo and W for fine tuning of reactivity, substrate specificity and metabolic role. Coord Chem Rev 257:315–331. https://doi.org/10.1016/j.ccr.2012.05.020
González-Sánchez A, Revah S (2007) The effect of chemical oxidation on the biological sulfide oxidation by an alkaliphilic sulfoxidizing bacterial consortium. Enzym Microb Technol 40:292–298. https://doi.org/10.1016/j.enzmictec.2006.04.017
Grady CPL, Daigger GT, Lim HC (1999) Biological wastewater treatment, 2nd edn. Marcel Dekker, New York
Griesbeck C, Hauska G, Schütz M (2000) Biological sulfide oxidation: sulfide-quinone reductase (SQR), the primary reaction. Res Dev Microbiol 4:179–203
Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565. https://doi.org/10.1021/bi026032b
Gu JD, Qiu W, Koenig A, Fan Y (2004) Removal of high NO3 − concentrations in saline water through autotrophic denitrification by the bacterium Thiobacillus denitrificans strain MP. Water Sci Technol 49:105–112. https://doi.org/10.2166/wst.2004.0743
Hao T, Wei L, Lu H, Chui H, Mackey HR, van Loosdrecht MCM, Chen G (2013) Characterization of sulfate-reducing granular sludge in the SANI® process. Water Res 47:7042–7052. https://doi.org/10.1016/j.watres.2013.07.052
Hashimoto S, Furukawa K, Shioyama M (1987) Autotrophic denitrification using elemental sulfur. J Ferment Technol 65:683–692. https://doi.org/10.1016/0385-6380(87)90011-2
Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M (2000) Nitric oxide reductases in bacteria. Biochim Biophys Acta Bioenerg 1459:266–273. https://doi.org/10.1016/S0005-2728(00)00161-4
Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189. https://doi.org/10.1128/AEM.00231-06
Hino T, Matsumoto Y, Nagano S, Sugimoto H, Fukumori Y, Murata T, Iwata S, Shiro Y (2010) Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330:1666–1670. https://doi.org/10.1126/science.1195591
Jiang G, Sharma KR, Guisasola A, Keller J, Yuan Z (2009) Sulfur transformation in rising main sewers receiving nitrate dosage. Water Res 43:4430–4440. https://doi.org/10.1016/j.watres.2009.07.001
Jing C, Ping Z, Mahmood Q (2010) Influence of various nitrogenous electron acceptors on the anaerobic sulfide oxidation. Bioresour Technol 101:2931–2937. https://doi.org/10.1016/j.biortech.2009.11.047
Kampschreur MJ, Temmink H, Kleerebezem R, Jetten MSM, van Loosdrecht MCM (2009) Nitrous oxide emission during wastewater treatment. Water Res 43:4093–4103. https://doi.org/10.1016/j.watres.2009.03.001
Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the beta-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Microbiol 50:547–550. https://doi.org/10.1099/00207713-50-2-547
Kelly DP, Shergill JK, Lu WP, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71:95–107. https://doi.org/10.1023/A:1000135707181
Kim E-W, Bae J-H (2000) Alkalinity requirements and the possibility of simultaneous heterotrophic denitrification during sulfur-utilizing autotrophic denitrification. Water Sci Technol 42:233–238
Kim B-W, Chang H, Kyu Kim I, Suk Lee K (1992) Growth kinetics of the photosynthetic bacterium Chlorobium thiosulfatophilum in a fed-batch reactor. Biotechnol Bioeng 40:583–592. https://doi.org/10.1002/bit.260400505
Kimura K, Nakamura M, Watanabe Y (2002) Nitrate removal by a combination of elemental sulfur-based denitrification and membrane filtration. Water Res 36:1758–1766. https://doi.org/10.1016/S0043-1354(01)00376-1
Kleerebezem R, Mendez R (2002) Autotrophic denitrification for combined hydrogen sulfide removal from biogas and post-denitrification. Water Sci Technol 45:349–356. https://doi.org/10.2166/wst.2002.0368
Koenig A, Liu LH (2001) Kinetic model of autotrophic denitrification in sulphur packed-bed reactors. Water Res 35:1969–1978. https://doi.org/10.1016/S0043-1354(00)00483-8
Koenig A, Liu LH (2002) Use of limestone for pH control in autotrophic denitrification: continuous flow experiments in pilot-scale packed bed reactors. J Biotechnol 99:161–171. https://doi.org/10.1016/S0168-1656(02)00183-9
Koenig A, Liu L (2004) Autotrophic denitrification of high–salinity wastewater using elemental sulfur: batch tests. Water Environ Res 76:37–46
Kostrytsia A, Papirio S, Morrison L, Ijaz UZ, Collins G, Lens PN, Esposito G (2018) Biokinetics of microbial consortia using biogenic sulfur as a novel electron donor for sustainable denitrification. Bioresour Technol 270:359–367. https://doi.org/10.1016/j.biortech.2018.09.044
Lau GN, Sharma KR, Chen GH, van Loosdrecht MCM (2006) Integration of sulphate reduction, autotrophic denitrification and nitrification to achieve low-cost excess sludge minimisation for Hong Kong sewage. Water Sci Technol 53:227–235. https://doi.org/10.2166/wst.2006.101
Lin S, Mackey HR, Hao T, Guo G, van Loosdrecht MC, Chen G (2018) Biological sulfur oxidation in wastewater treatment: a review of emerging opportunities. Water Res 143:399–415. https://doi.org/10.1016/j.watres.2018.06.051
Liu LH, Koenig A (2002) Use of limestone for pH control in autotrophic denitrification: batch experiments. Process Biochem 37:885–893. https://doi.org/10.1016/S0168-1656(02)00183-9
Liu Y, Peng L, Ngo HH, Guo W, Wang D, Pan Y, Sun J, Ni B-J (2016) Evaluation of nitrous oxide emission from sulfide- and sulfur-based autotrophic denitrification processes. Environ Sci Technol 50:9407–9415. https://doi.org/10.1021/acs.est.6b02202
Lu H, Chandran K (2010) Factors promoting emissions of nitrous oxide and nitric oxide from denitrifying sequencing batch reactors operated with methanol and ethanol as electron donors. Biotechnol Bioeng 106:390–398. https://doi.org/10.1002/bit.22704
Lu H, Wu D, Tang DTW, Chen GH, Van Loosdrecht MCM, Ekama G (2011) Pilot scale evaluation of SANI® process for sludge minimization and greenhouse gas reduction in saline sewage treatment. Water Sci Technol 63:2149–2154. https://doi.org/10.2166/wst.2011.342
Lu H, Ekama GA, Wu D, Feng J, van Loosdrecht MCM, Chen G-H (2012a) SANI® process realizes sustainable saline sewage treatment: steady state model-based evaluation of the pilot-scale trial of the process. Water Res 46:475–490. https://doi.org/10.1016/j.watres.2011.11.031
Lu H, Wu D, Jiang F, Ekama GA, van Loosdrecht MCM, Chen G-H (2012b) The demonstration of a novel sulfur cycle-based wastewater treatment process: sulfate reduction, autotrophic denitrification, and nitrification integrated (SANI®) biological nitrogen removal process. Biotechnol Bioeng 109:2778–2789. https://doi.org/10.1002/bit.24540
Mahmood Q, Zheng P, Cai J, Wu D, Hu B, Li J (2007) Anoxic sulfide biooxidation using nitrite as electron acceptor. J Hazard Mater 147:249–256. https://doi.org/10.1016/j.jhazmat.2007.01.002
Mahmood Q, Zheng P, Hayat Y, Islam E, Wu D, Ren-Cun J (2008) Effect of pH on anoxic sulfide oxidizing reactor performance. Bioresour Technol 99:3291–3296. https://doi.org/10.1016/j.biortech.2007.07.006
Manconi I, Carucci A, Lens P (2007) Combined removal of sulfur compounds and nitrate by autotrophic denitrification in bioaugmented activated sludge system. Biotechnol Bioeng 98:551–560. https://doi.org/10.1002/bit.21383
Matsumoto Y, Tosha T, Pisliakov AV, Hino T, Sugimoto H, Nagano S, Sugita Y, Shiro Y (2012) Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus. Nat Struct Mol Biol 19:238–245. https://doi.org/10.1038/nsmb.2213
Moon HS, Ahn K-H, Lee S, Nam K, Kim JY (2004) Use of autotrophic sulfur-oxidizers to remove nitrate from bank filtrate in a permeable reactive barrier system. Environ Pollut 129:499–507. https://doi.org/10.1016/j.envpol.2003.11.004
Moon HS, Nam K, Kim JY (2006) Initial alkalinity requirement and effect of alkalinity sources in sulfur-based autotrophic denitrification barrier system. J Environ Eng 132:971–975. https://doi.org/10.1061/(ASCE)0733-9372(2006)132:9(971)
Moon HS, Shin DY, Nam K, Kim JY (2008) A long-term performance test on an autotrophic denitrification column for application as a permeable reactive barrier. Chemosphere 73:723–728. https://doi.org/10.1016/j.chemosphere.2008.06.065
Mora M, Guisasola A, Gamisans X, Gabriel D (2014) Examining thiosulfate-driven autotrophic denitrification through respirometry. Chemosphere 113:1–8. https://doi.org/10.1016/j.chemosphere.2014.03.083
Mora M, Fernández M, Gómez JM, Cantero D, Lafuente J, Gamisans X, Gabriel D (2015a) Kinetic and stoichiometric characterization of anoxic sulfide oxidation by SO-NR mixed cultures from anoxic biotrickling filters. Appl Microbiol Biotechnol 99:77–87. https://doi.org/10.1007/s00253-014-5688-5
Mora M, Dorado AD, Gamisans X, Gabriel D (2015b) Investigating the kinetics of autotrophic denitrification with thiosulfate: modeling the denitritation mechanisms and the effect of the acclimation of SO-NR cultures to nitrite. Chem Eng J 262:235–241. https://doi.org/10.1016/j.cej.2014.09.101
Moraes BDS, Souza TSO, Foresti E (2012) Effect of sulfide concentration on autotrophic denitrification from nitrate and nitrite in vertical fixed-bed reactors. Process Biochem 47:1395–1401. https://doi.org/10.1016/j.procbio.2012.05.008
Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181:6573–6584
Moura I, Moura JJ (2001) Structural aspects of denitrifying enzymes. Curr Opin Chem Biol 5:168–175. https://doi.org/10.1016/S1367-5931(00)00187-3
Müller FH, Bandeiras TM, Urich T, Teixeira M, Gomes CM, Kletzin A (2004) Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate: quinone oxidoreductase. Mol Microbiol 53:1147–1160. https://doi.org/10.1111/j.1365-2958.2004.04193.x
Murphy ME, Turley S, Adman ET (1997) Structure of nitrite bound to copper-containing nitrite reductase from Alcaligenes faecalis mechanistic implications. J Biol Chem 272:28455–28460. https://doi.org/10.1074/jbc.272.45.28455
O'Brien DJ, Birkner FB (1977) Kinetics of oxygenation of reduced sulfur species in aqueous solution. Environ Sci Technol 11:1114–1120. https://doi.org/10.1021/es60135a009
Oh SE, Kim KS, Choi HC, Cho J, Kim IS (2000) Kinetics and physiological characteristics of autotrophic dentrification by denitrifying sulfur bacteria. Water Sci Technol 42:59–68. https://doi.org/10.2166/wst.2000.0359
Oh SE, Bum MS, Yoo YB, Zubair A, Kim IS (2003) Nitrate removal by simultaneous sulfur utilizing autotrophic and heterotrophic denitrification under different organics and alkalinity conditions: batch experiments. Water Sci Technol 47:237–244. https://doi.org/10.2166/wst.2003.0061
Okabe S, Nielsen PH, Characklis WG (1992) Factors affecting microbial sulfate reduction by Desulfovibrio desulfuricans in continuous culture: limiting nutrients and sulfide concentration. Biotechnol Bioeng 40:725–734. https://doi.org/10.1002/bit.260400612
Pan Y, Ni BJ, Bond PL, Ye L, Yuan Z (2013) Electron competition among nitrogen oxides reduction during methanol-utilizing denitrification in wastewater treatment. Water Res 47:3273–3281. https://doi.org/10.1016/j.watres.2013.02.054
Park JY, Yoo YJ (2009) Biological nitrate removal in industrial wastewater treatment: which electron donor we can choose. Appl Microbiol Biotechnol 82:415–429. https://doi.org/10.1007/s00253-008-1799-1
Park KY, Inamori Y, Mizuochi M, Ahn KH (2000) Emission and control of nitrous oxide from a biological wastewater treatment system with intermittent aeration. J Biosci Bioeng 90:247–252. https://doi.org/10.1016/S1389-1723(00)80077-8
Pauleta SR, Dell’Acqua S, Moura I (2013) Nitrous oxide reductase. Coord Chem Rev 257:332–349. https://doi.org/10.1016/j.ccr.2012.05.026
Pokorna D, Zabranska J (2015) Sulfur-oxidizing bacteria in environmental technology. Biotechnol Adv 33:1246–1259. https://doi.org/10.1016/j.biotechadv.2015.02.007
Pomowski A, Zumft WG, Kroneck PM, Einsle O (2011) N2O binding at a [4Cu: 2S] copper–sulphur cluster in nitrous oxide reductase. Nature 477:234–237. https://doi.org/10.1038/nature10332
Pronk JT, Meulenberg R, Hazeu W, Bos P, Kuenen JG (1990) Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Lett 75:293–306. https://doi.org/10.1016/0378-1097(90)90540-7
Qian J, Lu H, Cui Y, Wei L, Liu R, Chen GH (2015) Investigation on thiosulfate-involved organics and nitrogen removal by a sulfur cycle-based biological wastewater treatment process. Water Res 69:295–306. https://doi.org/10.1016/j.watres.2014.11.038
Qian J, Zhou J, Zhang Z, Liu R, Wang Q (2016) Biological nitrogen removal through nitritation coupled with thiosulfate-driven denitritation. Sci Rep 6:27502. https://doi.org/10.1038/srep27502
Reis MAM, Almeida JS, Lemos PC, Carrondo MJT (1992) Effect of hydrogen sulfide on growth of sulfate reducing bacteria. Biotechnol Bioeng 40:593–600. https://doi.org/10.1002/bit.260400506
Richardson DJ, Watmough NJ (1999) Inorganic nitrogen metabolism in bacteria. Curr Opin Chem Biol 3:207–219. https://doi.org/10.1016/S1367-5931(99)80034-9
Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58:165–178. https://doi.org/10.1007/PL00000845
Richardson D, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle–could enzymic regulation hold the key? Trends Biotechnol 27:388–397. https://doi.org/10.1016/j.tibtech.2009.03.009
Rittmann BE, McCarty PL (2001) Environmental biotechnology - principles and applications. McGraw-Hill, New York
Saggar S, Jha N, Deslippe J, Bolan NS, Luo J, Giltrap DL, Kim D, Zaman M, Tillman RW (2013) Denitrification and N2O: N2 production in temperate grasslands: processes, measurements, modelling and mitigating negative impacts. Sci Total Environ 465:173–195. https://doi.org/10.1016/j.scitotenv.2012.11.050
Sahinkaya E, Dursun N (2012) Sulfur-oxidizing autotrophic and mixotrophic denitrification processes for drinking water treatment: elimination of excess sulfate production and alkalinity requirement. Chemosphere 89:144–149. https://doi.org/10.1016/j.chemosphere.2012.05.029
Sahinkaya E, Kilic A, Duygulu B (2014) Pilot and full scale applications of sulfur-based autotrophic denitrification process for nitrate removal from activated sludge process effluent. Water Res 60:210–217. https://doi.org/10.1016/j.watres.2014.04.052
Sahinkaya E, Yurtsever A, Ucar D (2017) A novel elemental sulfur-based mixotrophic denitrifying membrane bioreactor for simultaneous Cr (VI) and nitrate reduction. J Hazard Mater 324:15–21. https://doi.org/10.1016/j.jhazmat.2016.02.032
Saia FT, Souza TSO, Duarte RTD, Pozzi E, Fonseca D, Foresti E (2016) Microbial community in a pilot-scale bioreactor promoting anaerobic digestion and sulfur-driven denitrification for domestic sewage treatment. Bioprocess Biosyst Eng 39:341–352. https://doi.org/10.1007/s00449-015-1520-6
Sánchez I, Fernández N, Amils R, Sanz JL (2008) Assessment of the addition of Thiobacillus denitrificans and Thiomicrospira denitrificans to chemolithoautotrophic denitrifying bioreactors. Int Microbiol 11:179–184. https://doi.org/10.2436/20.1501.01.58
Sánchez O, Ferrera I, Dahl C, Mas J (2001) In vivo role of adenosine-5′-phosphosulfate reductase in the purple sulfur bacterium Allochromatium vinosum. Arch Microbiol 176:301–305. https://doi.org/10.1007/s002030100327
Sato N, Ishii S, Sugimoto H, Hino T, Fukumori Y, Sako Y, Shiro Y, Tosha T (2014) Structures of reduced and ligand-bound nitric oxide reductase provide insights into functional differences in respiratory enzymes. Proteins: Struct Funct Bioinf 82:1258–1271. https://doi.org/10.1002/prot.24492
Sauvé V, Bruno S, Berks BC, Hemmings AM (2007) The SoxYZ complex carries sulfur cycle intermediates on a peptide swinging arm. J Biol Chem 282:23194–23204. https://doi.org/10.1074/jbc.M701602200
Sengupta S, Ergas SJ, Lopez-Luna E (2007) Investigation of solid-phase buffers for sulfur-oxidizing autotrophic denitrification. Water Environ Res 79:2519–2526. https://doi.org/10.2175/106143007X254584
Shao MF, Zhang T, Fang HHP (2010) Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biotechnol 88:1027–1042. https://doi.org/10.1007/s00253-010-2847-1
Shao M-F, Zhang T, Fang HH-P, Li X (2011) The effect of nitrate concentration on sulfide-driven autotrophic denitrification in marine sediment. Chemosphere 83:1–6. https://doi.org/10.1016/j.chemosphere.2011.01.042
Shiro Y (2012) Structure and function of bacterial nitric oxide reductases: nitric oxide reductase, anaerobic enzymes. Biochim Biophys Acta Bioenerg 1817:1907–1913. https://doi.org/10.1016/j.bbabio.2012.03.001
Sierra-Alvarez R, Beristain-Cardoso R, Salazar M, Gómez J, Razo-Flores E, Field JA (2007) Chemolithotrophic denitrification with elemental sulfur for groundwater treatment. Water Res 41:1253–1262. https://doi.org/10.1016/j.watres.2006.12.039
Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74:1145–1156. https://doi.org/10.1128/AEM.01844-07
Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612–3622. https://doi.org/10.1128/AEM.02894-06
Sparacino-Watkins C, Stolz JF, Basu P (2014) Nitrate and periplasmic nitrate reductases. Chem Soc Rev 43:676–706. https://doi.org/10.1039/c3cs60249d
Sublette KL, Kolhatkar R, Raterman K (1998) Technological aspects of the microbial treatment of sulfide-rich wastewaters: a case study. Biodegradation 9:259–271. https://doi.org/10.1023/A:1008262522493
Suzuki I (1999) Oxidation of inorganic sulfur compounds: chemical and enzymatic reactions. Can J Microbiol 45:97–105. https://doi.org/10.1139/w98-223
Syed M, Soreanu G, Falletta P, Béland M (2006) Removal of hydrogen sulfide from gas streams using biological processes - a review. Can Biosyst Eng / Le Genie des Biosyst au Canada 48:2.1–2.14
Tang K, Baskaran V, Nemati M (2009) Bacteria of the sulphur cycle: An overview of microbiology, biokinetics and their role in petroleum and mining industries. Biochem Eng J 44:73–94. https://doi.org/10.1016/j.bej.2008.12.011
Thamdrup BO, Dalsgaard T (2008) Nitrogen cycling in sediments. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley, Hoboken, pp 527–568. https://doi.org/10.1002/9780470281840.ch14
Theissen U, Hoffmeister M, Grieshaber M, Martin W (2003) Single eubacterial origin of eukaryotic sulfide: quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Eovl 20:1564–1574. https://doi.org/10.1093/molbev/msg174
Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417. https://doi.org/10.1016/j.femsec.2004.04.011
Tourang M, Aminzadeh B, Torabian A (2018) Autotrophic denitrification of synthetic nitrate-contaminated groundwater in up-flow fixed-bed bioreactor by pumice as porous media. Environ Health Eng Manag 5:1–7. https://doi.org/10.15171/EHEM.2018.01
Trouve C, Chazal PM, Gueroux B, Sauvaitre N (1998) Denitrification by new strains of Thiobacillus denitrificans under non-standard physicochemical conditions. Effect of temperature, pH, and sulphur source. Environ Technol 19:601–610. https://doi.org/10.1080/09593331908616716
Tsuneda S, Mikami M, Kimochi Y, Hirata A (2005) Effect of salinity on nitrous oxide emission in the biological nitrogen removal process for industrial wastewater. J Hazard Mater 119:93–98. https://doi.org/10.1016/j.jhazmat.2004.10.025
Vaiopoulou E, Melidis P, Aivasidis A (2005) Sulfide removal in wastewater from petrochemical industries by autotrophic denitrification. Water Res 39:4101–4109. https://doi.org/10.1016/j.watres.2005.07.022
Vidal S, Rocha C, Galvao H (2002) A comparison of organic and inorganic carbon controls over biological denitrification in aquaria. Chemosphere 48:445–451. https://doi.org/10.1016/S0045-6535(02)00073-5
Visser JM, Robertson LA, Van Verseveld HW, Kuenen JG (1997) Sulfur production by obligately chemolithoautotrophic Thiobacillus species. Appl Environ Microbiol 63:2300–2305
Wang J, Lu H, Chen G-H, Lau GN, Tsang WL, van Loosdrecht MCM (2009) A novel sulfate reduction, autotrophic denitrification, nitrification integrated (SANI) process for saline wastewater treatment. Water Res 43:2363–2372. https://doi.org/10.1016/j.watres.2009.02.037
Wani AH, Lau AK, Branion RMR (1999) Biofiltration control of pulping odors - hydrogen sulfide: performance, macrokinetics and coexistence effects of organo-sulfur species. J Chem Technol Biotechnol 74:9–16. https://doi.org/10.1002/(SICI)1097-4660(199901)74:1<9:AID-JCTB981>3.0.CO;2-B
Wiesmann U (1994) Biological nitrogen removal from wastewater. In: Fletcher A (ed) Advances in biochemical engineering biotechnology. Springer-Verlag, Berlin, pp 113–154
Wu D, Ekama GA, Chui H-K, Wang B, Cui Y-X, Hao T-W, van Loosdrecht MCM, Chen G-H (2016) Large-scale demonstration of the sulfate reduction autotrophic denitrification nitrification integrated (SANI®) process in saline sewage treatment. Water Res 100:496–507. https://doi.org/10.1016/j.watres.2016.05.052
Wunderlin P, Mohn J, Joss A, Emmenegger L, Siegrist H (2012) Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res 46:1027–1037. https://doi.org/10.1016/j.watres.2011.11.080
Xu J, Fan Y, Li Z (2016) Effect of pH on elemental sulfur conversion and microbial communities by autotrophic simultaneous desulfurization and denitrification. Environ Technol 37:3014–3023. https://doi.org/10.1080/09593330.2016.1173117
Xu J, Ding K, Yang C, Huang T (2018) Regulation of influent sulfide concentration on anaerobic denitrifying sulfide removal. Environ Technol:1–9. https://doi.org/10.1080/09593330.2017.1422552
Yang W, Zhao Q, Lu H, Ding Z, Meng L, Chen GH (2016a) Sulfide-driven autotrophic denitrification significantly reduces N2O emissions. Water Res 90:176–184. https://doi.org/10.1016/j.watres.2015.12.032
Yang W, Lu H, Khanal SK, Zhao Q, Meng L, Chen GH (2016b) Granulation of sulfur-oxidizing bacteria for autotrophic denitrification. Water Res 104:507–519. https://doi.org/10.1016/j.watres.2016.08.049
Zhang TC, Lampe DG (1999) Sulfur: limestone autotrophic denitrification processes for treatment of nitrate-contaminated water: batch experiments. Water Res 33:599–608. https://doi.org/10.1016/S0043-1354(98)00281-4
Zhang Z, Lei Z, He X, Zhang Z, Yang Y, Sugiura N (2009) Nitrate removal by Thiobacillus denitrificans immobilized on poly (vinyl alcohol) carriers. J Hazard Mater 163:1090–1095. https://doi.org/10.1016/j.jhazmat.2008.07.062
Zhang L, Zhang C, Hu C, Liu H, Qu J (2015) Denitrification of groundwater using a sulfur-oxidizing autotrophic denitrifying anaerobic fluidized-bed MBR: performance and bacterial community structure. Appl Microbiol Biotechnol 99:2815–2827. https://doi.org/10.1007/s00253-014-6113-9
Zhao Z, Qiu W, Koenig A, Fan X, Gu JD (2004) Nitrate removal from saline water using autotrophic denitrification by the bacterium Thiobacillus denitrificans MP-1. Environ Technol 25:1201–1210. https://doi.org/10.1080/09593332508618387
Zhou Y, Pijuan M, Yuan Z (2007) Free nitrous acid inhibition on anoxic phosphorus uptake and denitrification by poly-phosphate accumulating organisms. Biotechnol Bioeng 98:903–912. https://doi.org/10.1002/bit.21458
Zhou W, Sun Y, Wu B, Zhang Y, Huang M, Miyanaga T, Zhang Z (2011) Autotrophic denitrification for nitrate and nitrite removal using sulfur-limestone. J Environ Sci 23:1761–1769. https://doi.org/10.1016/S1001-0742(10)60635-3
Zhou W, Liu X, Dong X, Wang Z, Yuan Y, Wang H, He S (2016) Sulfur-based autotrophic denitrification from the micro-polluted water. J Environ Sci 44:180–188. https://doi.org/10.1016/j.jes.2016.01.002
Zhu I, Getting T (2012) A review of nitrate reduction using inorganic materials. Environ Technol Rev 1:46–58. https://doi.org/10.1080/09593330.2012.706646
Zhu T, Cheng H, Yang L, Su S, Wang H, Wang S, Wang A (2019) Coupled Sulfur and Iron(II) Carbonate-Driven Autotrophic Denitrification for Significantly Enhanced Nitrate Removal. Environ Sci Technol 53:1545–1554. https://doi.org/10.1021/acs.est.8b06865
Zou G, Papirio S, Lakaniemi AM, Ahoranta SH, Puhakka JA (2016) High rate autotrophic denitrification in fluidized-bed biofilm reactors. Chem Eng J 284:1287–1294. https://doi.org/10.1016/j.cej.2015.09.074
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616
Funding
This study was financially supported by the Hong Kong Innovation and Technology Commission (grant no. ITC-CNERC14EG03), the National Natural Science Foundation of China (grant no. 51638005), and Shenzhen Science and Technology Innovation Committee Project (grant nos. JCYJ20170307174056499, JSGG2017101071620730).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cui, YX., Biswal, B.K., Guo, G. et al. Biological nitrogen removal from wastewater using sulphur-driven autotrophic denitrification. Appl Microbiol Biotechnol 103, 6023–6039 (2019). https://doi.org/10.1007/s00253-019-09935-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-09935-4
Keywords
Profiles
- Basanta Kumar Biswal View author profile