Abstract
Up to date, the intrinsic association of nitrate loading rate (NLR) with treatment performance of solid-phase denitrification (SPD) systems is still ambiguous. To address this issue, three continuous up-flow bioreactors were configured. They were packed with polycaprolactone (PCL) under a filling ratio of 30%, 60% or 90% and were operated under a varying NLR of 0.34 ± 0.01–3.99 ± 0.12 gN/(L·d). Results showed that the denitrification efficiency was high (RE > 96%) and stable except the case with the highest NLR, which was mainly attributed to the lack of available carbon sources. At the phylum or genus level, most of the detected dominant bacterial taxa were either associated with organics degradation or nitrogen metabolism. The difference in bacterial community structure among the three stages was mainly caused by NLR rather than the filling ratio. Moreover, as the NLR got higher, the Bray–Curtis distance between samples from the same stage became shorter. By the results of gene or enzyme prediction performed in PICRUSt2, the main nitrogen metabolism pathways in these reactors were denitrification, dissimilatory nitrate reduction to ammonium (DNRA), assimilatory nitrate reduction to ammonium (ANRA) and nitrogen fixation. Moreover, aerobic and anaerobic nitrate dissimilation coexisted in the systems with the latter playing a dominant role. Finally, denitrification and DNRA occurred under both high and low NLR conditions while nitrogen fixation and ANRA preferred to occur under low NLR environments. These findings might help guide practical applications.
Similar content being viewed by others
References
APHA (2017) Standard methods for the examination of water and wastewater, 23rd edn. American Public Health Association, American Water Works Association, Washington, DC, Water Environment Federation
Ashok V, Hait S (2015) Remediation of nitrate-contaminated water by solid-phase denitrification process-a review. Environ Sci Pollut Res 22(11):8075–8093. https://doi.org/10.1007/s11356-015-4334-9
Aslan S, Turkman A (2003) Biological denitrification of drinking water using various natural organic solid substrates. Water Sci Technol 48(11–12):489–495. https://doi.org/10.2166/wst.2004.0898
Chu L, Wang J (2011) Comparison of polyurethane foam and biodegradable polymer as carriers in moving bed biofilm reactor for treating wastewater with a low C/N ratio. Chemosphere 83(1):63–68. https://doi.org/10.1016/j.chemosphere.2010.12.077
Chu L, Wang J (2016) Denitrification of groundwater using PHBV blends in packed bed reactors and the microbial diversity. Chemosphere 155:463–470. https://doi.org/10.1016/j.chemosphere.2016.04.090
Deng YL, Ruan YJ, Zhu SM, Guo XS, Han ZY, Ye ZY, Liu G, Shi MM (2017) The impact of DO and salinity on microbial community in poly(butylene succinate) denitrification reactors for recirculating aquaculture system wastewater treatment. AMB Express 7(1):113. https://doi.org/10.1186/s13568-017-0412-3
Deygout C, Lesne A, Campillo F, Rapaport A (2013) Homogenised model linking microscopic and macroscopic dynamics of a biofilm: application to growth in a plug flow reactor. Ecol Model 250:15–24. https://doi.org/10.1016/j.ecolmodel.2012.10.020
Ding W, Liu H, Zhang K, Lv D, Wang S (2020) Effective control of the carbon release of starch/polyvinyl alcohol based on a polyamide coating in solid-phase denitrification. Environ Sci-Wat Res Technol 6(12):3293–3305. https://doi.org/10.1039/d0ew00721h
Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38(6):685–688. https://doi.org/10.1038/s41587-020-0548-6
Elefsiniotis P, Li D (2006) The effect of temperature and carbon source on denitrification using volatile fatty acids. Biochem Eng J 28(2):148–155. https://doi.org/10.1016/j.bej.2005.10.004
Fang D, Wu A, Huang L, Shen Q, Zhang Q, Jiang L, Ji F (2020) Polymer substrate reshapes the microbial assemblage and metabolic patterns within a biofilm denitrification system. Chem Eng J 387:124128. https://doi.org/10.1016/j.cej.2020.124128
Feng LJ, Jia R, Zeng Z, Yang GF, Xu XY (2018) Simultaneous nitrification-denitrification and microbial community profile in an oxygen-limiting intermittent aeration SBBR with biodegradable carriers. Biodegradation 29(5):473–486. https://doi.org/10.1007/s10532-018-9845-x
Feng L, Yang J, Yu H, Lan Z, Ye X, Yang G, Yang Q, Zhou J (2020) Response of denitrifying community, denitrification genes and antibiotic resistance genes to oxytetracycline stress in polycaprolactone supported solid-phase denitrification reactor. Bioresour Technol 308:123274. https://doi.org/10.1016/j.biortech.2020.123274
Ghafari S, Hasan M, Aroua MK (2008) Bio-electrochemical removal of nitrate from water and wastewater—a review. Bioresour Technol 99(10):3965–3974. https://doi.org/10.1016/j.biortech.2007.05.026
Groß-Schmölders M, Klein K, Birkholz A, Leifeld J, Alewell C (2021) Rewetting and drainage of nutrient-poor peatlands indicated by specific bacterial membrane fatty acids and a repeated sampling of stable isotopes (δ15N, δ13C). Front Environ Sci 9:730106
Hosokawa S, Kuroda K, Narihiro T, Aoi Y, Ozaki N, Ohashi A, Kindaichi T (2021) Cometabolism of the superphylum patescibacteria with anammox bacteria in a long-term freshwater anammox column reactor. Water 13(2):208. https://doi.org/10.3390/w13020208
Huang XJ, Weisener CG, Ni JP, He BH, Xie DT, Li ZL (2020) Nitrate assimilation, dissimilatory nitrate reduction to ammonium, and denitrification coexist in Pseudomonas putida Y-9 under aerobic conditions. Bioresour Technol 312:123597. https://doi.org/10.1016/j.biortech.2020.123597
Jafari SJ, Moussavi G, Yaghmaeian K (2015) High-rate biological denitrification in the cyclic rotating-bed biological reactor: effect of COD/NO3(-), nitrate concentration and salinity and the phylogenetic analysis of denitrifiers. Bioresour Technol 197:482–488. https://doi.org/10.1016/j.biortech.2015.08.047
Jiang L, Wu AQ, Fang DX, Zhang YF, Shen QS, Xu XY, Ji FY (2020) Denitrification performance and microbial diversity using starch-polycaprolactone blends as external solid carbon source and biofilm carriers for advanced treatment. Chemosphere 255:126901. https://doi.org/10.1016/j.chemosphere.2020.126901
Kang Y, Xie HJ, Zhang J, Zhao CC, Wang WG, Guo Y, Guo ZZ (2018) Intensified nutrients removal in constructed wetlands by integrated Tubifex tubifex and mussels: Performance and mechanisms. Ecotox Environ Safe 162:446–453. https://doi.org/10.1016/j.ecoenv.2018.07.009
Kong DD, Li WB, Deng YL, Ruan YJ, Chen GS, Yu JH, Lin FC (2018) Denitrification-potential evaluation and nitrate-removal-pathway analysis of aerobic denitrifier strain Marinobacter hydrocarbonoclasticus RAD-2. Water 10(10):1298. https://doi.org/10.3390/w10101298
Kumar M, Lin JG (2010) Co-existence of anammox and denitrification for simultaneous nitrogen and carbon removal–strategies and issues. J Hazard Mater 178(1–3):1–9. https://doi.org/10.1016/j.jhazmat.2010.01.077
Li P, Zuo JE, Wang YJ, Zhao J, Tang L, Li ZX (2016) Tertiary nitrogen removal for municipal wastewater using a solid-phase denitrifying biofilter with polycaprolactone as the carbon source and filtration medium. Water Res 93:74–83. https://doi.org/10.1016/j.watres.2016.02.009
Li R, Feng C, Xi B, Chen N, Jiang Y, Zhao Y, Li M, Dang Q, Zhao B (2017) Nitrate removal efficiency of a mixotrophic denitrification wall for nitrate-polluted groundwater in situ remediation. Ecol Eng 106:523–531. https://doi.org/10.1016/j.ecoleng.2017.06.010
Li YX, Ling JY, Chen PC, Chen JL, Dai RZ, Liao JS, Yu JJ, Xu YB (2021) Pseudomonas mendocina LYX: a novel aerobic bacterium with advantage of removing nitrate high effectively by assimilation and dissimilation simultaneously. Front Env Sci Eng 15(4):57. https://doi.org/10.1007/s11783-020-1349-3
Lindstrom K, Mousavi SA (2020) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13(5):1314–1335. https://doi.org/10.1111/1751-7915.13517
Liu L, Li N, Tao C, Zhao Y, Gao J, Huang Z, Zhang J, Gao J, Zhang J, Cai M (2021a) Nitrogen removal performance and bacterial communities in zeolite trickling filter under different influent C/N ratios. Environ Sci Pollut Res Int 28(13):15909–15922. https://doi.org/10.1007/s11356-020-11776-y
Liu SY, Dai JC, Wei HH, Li SY, Wang P, Zhu TB, Zhou JZ, Qiu DR (2021b) Dissimilatory nitrate reduction to ammonium (DNRA) and denitrification pathways are leveraged by cyclic AMP receptor protein (CRP) paralogues based on electron donor/acceptor limitation in Shewanella loihica PV-4. Appl Environ Microbiol 87(2):e01964-e2020. https://doi.org/10.1128/aem.01964-20
Luo XS, Qian H, Wang L, Han S, Wen SL, Wang BR, Huang QY, Chen WL (2020) Fertilizer types shaped the microbial guilds driving the dissimilatory nitrate reduction to ammonia process in a Ferralic Cambisol. Soil Biol Biochem 141:107677. https://doi.org/10.1016/j.soilbio.2019.107677
Mohan TVK, Nancharaiah YV, Venugopalan VP, Sai PMS (2016) Effect of C/N ratio on denitrification of high-strength nitrate wastewater in anoxic granular sludge sequencing batch reactors. Ecol Eng 91:441–448. https://doi.org/10.1016/j.ecoleng.2016.02.033
Nguyen TNP, Chao SJ, Chen PC, Huang CP (2018) Effects of C/N ratio on nitrate removal and floc morphology of autohydrogenotrophic bacteria in a nitrate-containing wastewater treatment process. J Environ Sci 69:52–60. https://doi.org/10.1016/j.jes.2017.04.002
Peixoto J, Silva LP, Kruger RH (2017) Brazilian Cerrado soil reveals an untapped microbial potential for unpretreated polyethylene biodegradation. J Hazard Mater 324(Pt B):634–644. https://doi.org/10.1016/j.jhazmat.2016.11.037
Qiu T, Liu L, Gao M, Zhang L, Tursun H, Wang X (2016) Effects of solid-phase denitrification on the nitrate removal and bacterial community structure in recirculating aquaculture system. Biodegradation 27(2–3):165–178. https://doi.org/10.1007/s10532-016-9764-7
Roussel-Delif L, Tarnawski S, Hamelin J, Philippot L, Aragno M, Fromin N (2005) Frequency and diversity of nitrate reductase genes among nitrate-dissimilating pseudomonas in the rhizosphere of perennial grasses grown in field conditions. Microb Ecol 49(1):63–72. https://doi.org/10.1007/s00248-003-0228-3
Sakoula D, Koch H, Frank J, Jetten MSM, van Kessel MAHJ, Lucker S (2021) Enrichment and physiological characterization of a novel comammox Nitrospira indicates ammonium inhibition of complete nitrification. ISME J 15(4):1010–1024. https://doi.org/10.1038/s41396-020-00827-4
Shen Z, Zhou Y, Hu J, Wang J (2013a) Denitrification performance and microbial diversity in a packed-bed bioreactor using biodegradable polymer as carbon source and biofilm support. J Hazard Mater 250–251:431–438. https://doi.org/10.1016/j.jhazmat.2013.02.026
Shen Z, Zhou Y, Wang J (2013b) 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. https://doi.org/10.1016/j.biortech.2012.12.169
Shen Z, Yin Y, Wang J (2016) Biological denitrification using poly(butanediol succinate) as electron donor. Appl Microbiol Biotechnol 100(13):6047–6053. https://doi.org/10.1007/s00253-016-7435-6
Shen Q, Ji F, Wei J, Fang D, Zhang Q, Jiang L, Cai A, Kuang L (2020) The influence mechanism of temperature on solid phase denitrification based on denitrification performance, carbon balance, and microbial analysis. Sci Total Environ 732:139333. https://doi.org/10.1016/j.scitotenv.2020.139333
Wang JL, Chu LB (2016) Biological nitrate removal from water and wastewater by solid-phase denitrification process. Biotechnol Adv 34(6):1103–1112. https://doi.org/10.1016/j.biotechadv.2016.07.001
Wang DP, Li T, Huang KL, He XW, Zhang XX (2019) Roles and correlations of functional bacteria and genes in the start-up of simultaneous anammox and denitrification system for enhanced nitrogen removal. Sci Total Environ 655:1355–1363. https://doi.org/10.1016/j.scitotenv.2018.11.321
Wu W, Yang F, Yang L (2012) Biological denitrification with a novel biodegradable polymer as carbon source and biofilm carrier. Bioresour Technol 118:136–140. https://doi.org/10.1016/j.biortech.2012.04.066
Wu W, Yang L, Wang J (2013) Denitrification using PBS as carbon source and biofilm support in a packed-bed bioreactor. Environ Sci Pollut Res Int 20(1):333–339. https://doi.org/10.1007/s11356-012-0926-9
Wu Y, Zaiden N, Cao B (2018) The core- and pan-genomic analyses of the genus Comamonas: from environmental adaptation to potential virulence. Front Microbiol 9:3096. https://doi.org/10.3389/fmicb.2018.03096
Xiang Y, Shao Z, Chai H, Ji F, He Q (2020) Functional microorganisms and enzymes related nitrogen cycle in the biofilm performing simultaneous nitrification and denitrification. Bioresour Technol 314:123697. https://doi.org/10.1016/j.biortech.2020.123697
Xu ZS, Dai XH, Chai XL (2018) Effect of different carbon sources on denitrification performance, microbial community structure and denitrification genes. Sci Total Environ 634:195–204. https://doi.org/10.1016/j.scitotenv.2018.03.348
Yang Z, Sun H, Zhou Q, Zhao L, Wu W (2020) Nitrogen removal performance in pilot-scale solid-phase denitrification systems using novel biodegradable blends for treatment of waste water treatment plants effluent. Bioresour Technol 305:122994. https://doi.org/10.1016/j.biortech.2020.122994
Yi CH, Qin W, Wen XH (2020) Renovated filter filled with poly-3-hydroxybutyrateco-hydroxyvalerate and granular activated carbon for simultaneous removal of nitrate and PPCPs from the secondary effluent. Sci Total Environ 749:141494. https://doi.org/10.1016/j.scitotenv.2020.141494
Zaki SA, Eltarahony MM, Abd-El-Haleem DA (2019) Disinfection of water and wastewater by biosynthesized magnetite and zerovalent iron nanoparticles via NAP-NAR enzymes of Proteus mirabilis 10B. Environ Sci Pollut Res 26(23):23661–23678. https://doi.org/10.1007/s11356-019-05479-2
Zhang Q, Ji FY, Xu XY (2016) Effects of physicochemical properties of poly-epsilon-caprolactone on nitrate removal efficiency during solid-phase denitrification. Chem Eng J 283:604–613. https://doi.org/10.1016/j.cej.2015.07.085
Zhang SJ, Zhang G, Wu M, Wang DJ, Liu Q (2021b) Straw return and low N addition modify the partitioning of dissimilatory nitrate reduction by increasing conversion to ammonium in paddy fields. Soil Biol Biochem 162:108425. https://doi.org/10.1016/j.soilbio.2021.108425
Zhang SS, Fan YT, Zhang N, Wang XM (2021c) Relationship between denitrification performance and microbial community structure in a PHBV-supported denitrification reactor. Desalin Water Treat 215:23–30. https://doi.org/10.5004/dwt.2021.26768
Zhang S, Xiao L, Tang Z, Zhang X, Wang Z (2022) Microbial explanation to performance stratification along up-flow solid-phase denitrification column packed with polycaprolactone. Bioresour Technol 343:126066. https://doi.org/10.1016/j.biortech.2021.126066
Zhang S, He X, Prodanovic V, Zhang K (2021) Effect of filling ratio and backwash on performance of a continuous-flow SPD reactor packed with PCL as carbon source. Water Environ Res 93(8):1381–1390. https://doi.org/10.1002/wer.1530
Zhao J, Feng C, Tong S, Chen N, Dong S, Peng T, Jin S (2018) Denitrification behavior and microbial community spatial distribution inside woodchip-based solid-phase denitrification (W-SPD) bioreactor for nitrate-contaminated water treatment. Bioresour Technol 249:869–879. https://doi.org/10.1016/j.biortech.2017.11.011
Zhong H, Cheng Y, Ahmad Z, Shao Y, Zhang H, Lu Q, Shim H (2020) Solid-phase denitrification for water remediation: processes, limitations, and new aspects. Crit Rev Biotechnol 40(8):1113–1130. https://doi.org/10.1080/07388551.2020.1805720
Acknowledgements
This work was financially supported by the Open Research Program from the Key Lab of Basin Water Resource and Eco-Environmental Science in Hubei Province, Changjiang River Scientific Research Institute (Program SN: CKWV2019765/KY), and the Fundamental Research Funds for the Central Universities (WUT: 2019III107CG).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Informed consent
All authors agree to submit the manuscript to Biodegradation for potential publication.
Research involving human participants and/or animals
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.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, S., Tang, Z., Xia, S. et al. The intrinsic relevance of nitrogen removal pathway to varying nitrate loading rate in a polycaprolactone-supported denitrification system. Biodegradation 33, 317–331 (2022). https://doi.org/10.1007/s10532-022-09981-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-022-09981-2