Abstract
This study demonstrated that a combined heterotrophic and autotrophic denitrification (HAD) process is highly effective for the simultaneous removal of acetate, nitrate, and sulfide at an efficiency of 100, 80, and 100 %, respectively. In the HAD system, simultaneous sulfide, acetate, and nitrate removals were observed, which indicated that heterotrophic and autotrophic denitrification occurred simultaneously. When the sulfide was existed in HAD reactor, the main product of sulfide biooxidation was S0. Once the sulfide was exhausted, the sulfate concentration in the HAD reactor increased and became the main end product. These results provided an alternative method to control the end sulfide biooxidation product by online monitoring sulfide concentration. Nearly half (43 %) of the total clones in our mix-trophic reactor were amphitrophy denitrifiers. The autotrophic denitrifiers, heterotrophic denitrifiers, and amphitrophy denitrifiers coexisted in the HAD reactor to complete the denitrification process. Retrieved bacterial 16S rRNA gene clones affiliated with uncultured Xanthomonadaceae, Thauera, Thiobacillus, and Chromatiales were dominant.
Similar content being viewed by others
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(5):1531–1541
An S, Loden B, Nemati M (2012) Evaluation of heterotrophic nitrite removal by a sulphide and acetate oxidizing mixed culture originated from an oil reservoir. J Chem Technol Biotechnol 87(3):410–417
APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington
Beller HR, Chain PSG, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP (2006) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitfificans. J Bacteriol 188(4):1473–1488
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(5):1293–1299
Cardoso RB, Sierra-Alvarez R, Rowlette P, Flores ER, Gomez J, Field JA (2006) Sulfide oxidation under chemolithoautotrophic denitrifying conditions. Biotechnol Bioeng 95(6):1148–1157
Chen C, Ren N, Wang A, Yu Z, Lee D-J (2008) Simultaneous biological removal of sulfur, nitrogen and carbon using EGSB reactor. Appl Microbiol Biotechnol 78(6):1057–1063
Chu L, Wang J (2013) Denitrification performance and biofilm characteristics using biodegradable polymers PCL as carriers and carbon source. Chemosphere 91(9):1310–1316
Cord-Ruwisch R (1985) A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 4(1):33–36
Demirel S, Uyanık İ, Yurtsever A, Çelikten H, Uçar D (2014) Simultaneous bromate and nitrate reduction in water using sulfur-utilizing autotrophic and mixotrophic denitrification processes in a fixed bed column reactor. Clean: Soil Air Water 42(9):1185–1189
Gao DW, Peng YZ, Wu WM (2010) Kinetic model for biological nitrogen removal using shortcut nitrification-denitrification process in sequencing batch reactor. Environ Sci Technol 44(13):5015–5021
Ginige MP, Keller J, Blackall LL (2005) Investigation of an acetate-fed denitrifying microbial community by stable isotope probing, full-cycle rRNA analysis, and fluorescent in situ hybridization-microautoradiography. Appl Environ Microbiol 71(12):8683–8691
Hong X, Zhang X, Liu B, Mao Y, Liu Y, Zhao L (2010) Structural differentiation of bacterial communities in indole-degrading bioreactors under denitrifying and sulfate-reducing conditions. Res Microbiol 161(8):687–693
Karanasios KA, Vasiliadou IA, Pavlou S, Vayenas DV (2010) Hydrogenotrophic denitrification of potable water: a review. J Hazard Mater 180(1–3):20–37
Koenig A, Liu LH (1996) Autotrophic denitrification of landfill leachate using elemental sulphur. Water Sci Technol 34(5–6):469–476
Koenig A, Liu LH (2001) Kinetic model of autotrophic denitrification in sulphur packed-bed reactors. Water Res 35(8):1969–1978
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175
Lee D-J, Wong B-T (2014) Denitrifying sulfide removal by enriched microbial consortium: kinetic diagram. Bioresour Technol 164:386–393
Lee D-J, Pan X, Wang A, Ho K-L (2013) Facultative autotrophic denitrifiers in denitrifying sulfide removal granules. Bioresour Technol 132:356–360
Li W, Q-l Z, Liu H (2009) Sulfide removal by simultaneous autotrophic and heterotrophic desulfurization–denitrification process. J Hazard Mater 162(2–3):848–853
Ligi T, Oopkaup K, Truu M, Preem J-K, Nõlvak H, Mitsch WJ, Mander Ü, Truu J (2014) Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecol Eng 72:56–66
Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29:173–174
Mao Y, Xia Y, Zhang T (2013) Characterization of Thauera-dominated hydrogen-oxidizing autotrophic denitrifying microbial communities by using high-throughput sequencing. Bioresour Technol 128:703–710
Mora M, Fernández M, Gómez J, Cantero D, Lafuente J, Gamisans X, Gabriel D (2015) Kinetic and stoichiometric characterization of anoxic sulfide oxidation by SO-NR mixed cultures from anoxic biotrickling filters. Appl Microbiol Biotechnol 99(1):77–87
Moraes BS, Foresti E (2012) Determination of the intrinsic kinetic parameters of sulfide-oxidizing autotrophic denitrification in differential reactors containing immobilized biomass. Bioresour Technol 104:250–256
Oh SE, Yoo YB, Young JC, Kim IS (2001) Effect of organics on sulfur-utilizing autotrophic denitrification under mixotrophic conditions. J Biotechnol 92(1):1–8
Osaka T, Yoshie S, Tsuneda S, Hirata A, Iwami N, Inamori Y (2006) Identification of acetate- or methanol-assimilating bacteria under nitrate-reducing conditions by stable-isotope probing. Microb Ecol 52(2):253–266
Osaka T, Shirotani K, Yoshie S, Tsuneda S (2008) Effects of carbon source on denitrification efficiency and microbial community structure in a saline wastewater treatment process. Water Res 42(14):3709–3718
Park S, Bae W, Rittmann BE, Kim S, Chung J (2010) Operation of suspended-growth shortcut biological nitrogen removal (SSBNR) based on the minimum/maximum substrate concentration. Water Res 44(5):1419–1428
Park S, Yu J, Byun I, Cho S, Park T, Lee T (2011) Microbial community structure and dynamics in a mixotrophic nitrogen removal process using recycled spent caustic under different loading conditions. Bioresour Technol 102(15):7265–7271
Pynaert K, Smets BF, Beheydt D, Verstraete W (2004) Start-up of autotrophic nitrogen removal reactors via sequential biocatalyst addition. Environ Sci Technol 38(4):1228–1235
Reyes-Avila J, Razo-Flores E, Gomez J (2004) Simultaneous biological removal of nitrogen, carbon and sulfur by denitrification. Water Res 38(14–15):3313–3321
Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, New York
Shao M-F, Zhang T, Fang H-P (2010) Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biotechnol 88(5):1027–1042
Shen Z, Zhou Y, Wang J (2013) Comparison of denitrification performance and microbial diversity using starch/polylactic acid blends and ethanol as electron donor for nitrate removal. Bioresour Technol 131:33–39
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(6):1253–1262
Smith RL, Ceazan ML, Brooks MH (1994) Autotrophic, hydrogen-oxidizing, denitrifying bacteria in groundwater, potential agents for bioremediation of nitrate contamination. Appl Environ Microbiol 60(6):1949–1955
Soto O, Aspe E, Roeckel M (2007) Kinetics of cross-inhibited denitrification of a high load wastewater. Enzym Microb Technol 40:1627–1634
Souza TSO, Foresti E (2013) Sulfide-oxidizing autotrophic denitrification: an evaluation for nitrogen removal from anaerobically pretreated domestic sewage. Appl Biochem Biotechnol 170(5):1094–1103
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tang K, An S, Nemati M (2010) Evaluation of autotrophic and heterotrophic processes in biofilm reactors used for removal of sulphide, nitrate and COD. Bioresour Technol 101(21):8109–8118
Torrentó C, Urmeneta J, Otero N, Soler A, Viñas M, Cama J (2011) Enhanced denitrification in groundwater and sediments from a nitrate-contaminated aquifer after addition of pyrite. Chem Geol 287(1–2):90–101
Trois C, Coulon F, de Combret CP, Martins JMF, Oxarango L (2010) Effect of pine bark and compost on the biological denitrification process of non-hazardous landfill leachate: focus on the microbiology. J Hazard Mater 181(1–3):1163–1169
Van Doan T, Lee TK, Shukla SK, Tiedje JM, Park J (2013) Increased nitrous oxide accumulation by bioelectrochemical denitrification under autotrophic conditions: kinetics and expression of denitrification pathway genes. Water Res 47(19):7087–7097
Wen J, Pan L, Du L, Mao G (2003) The denitrification treatment of low C/N ratio nitrate-nitrogen wastewater in a gas–liquid–solid fluidized bed bioreactor. Chem Eng J 94(2):155–159
Acknowledgments
This work was supported by the National Natural Science Foundation of China (51108439, 50778156, and 51008025) and the Natural Science Foundation of Chongqing (cstc2014jcyjA20010).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 247 kb)
Rights and permissions
About this article
Cite this article
Xu, G., Peng, J., Feng, C. et al. Evaluation of simultaneous autotrophic and heterotrophic denitrification processes and bacterial community structure analysis. Appl Microbiol Biotechnol 99, 6527–6536 (2015). https://doi.org/10.1007/s00253-015-6532-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6532-2