Abstract
Nitrate removal from synthetic and real groundwater was investigated by using cassava distiller’s dried grains (CDDG), which served as sole carbon source as well as the only microbe seed. It was found that remarkably higher total nitrogen removal efficiency (96.8±0.6 %) could be reached; the accumulation of nitrite and the releases of organic compounds, meanwhile, were insignificant in the denitrification process. Scanning electron microscope (SEM) analysis showed that CDDG were degraded during the denitrification process. Further investigation showed that CDDG were anaerobically hydrolyzed and acidified to butyric acid, acetic acid, and carbohydrate, which could be utilized directly as the reducing equivalent providers for denitrification by the microorganisms separated from CDDG. Microbial community analysis revealed that the fungi and bacteria present in the original CDDG functioned as the denitrifiers, which mainly consisted of Aspergillus (69.8 %) and Rhizomucor (15.9 %) in the fungi community and Burkholderia (20.6 %) and Rhizobium (15.9 %) in the bacteria community, respectively. Finally, the use of CDDG as both carbon and microbial sources for real groundwater denitrification was testified to be feasible and safe with a total nitrogen removal efficiency of around 100 %.
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Agler MT, Werner JJ, Iten LB, Dekker A, Cotta MA, Dien BS, Angenent LT (2012) Shaping reactor microbiomes to produce the fuel precursor n-butyrate from pretreated cellulosic hydrolysates. Environ Sci Technol 46:10229–10238
Armstrong SK, Gross R (2007) Primary metabolism and physiology of Bordetella species. Bordetella: molecular microbiology. In: Locht C (ed). Horizon bioscience, Norfolk, pp: 165–190.
Berks BC, Ferguson SJ, Moir JWB, Richardson DJ (1995) Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. BBA-Bioenergetics 1232:97–173
Burow KR, Nolan BT, Rupert MG, Dubrovsky NM (2010) Nitrate in groundwater of the United States, 1991–2003. Environ Sci Technol 44:4988–4997
Cathrine SJ, Raghukumar C (2009) Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol Res 113:100–109
Chen J, Strous M (2013) Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution. BBA-Bioenergetics 1827:136–144
Chu L, Wang J (2011) Nitrogen removal using biodegradable polymers as carbon source and biofilm carriers in a moving bed biofilm reactor. Chem Eng J 170:220–225
Daniel RM, Limmer A, Steele K, Smith I (1982) Anaerobic growth, nitrate reduction and denitrification in 46 Rhizobium strains. J Gen Microbiol 128:1811–1815
Dhamole PB, Nair RR, D’Souza SF, Lele S (2007) Denitrification of high strength nitrate waste. Bioresour Technol 98:247–252
Eilersen AM, Henze M, Kløft L (1995) Effect of volatile fatty acids and trimethylamine on denitrification in activated sludge. Water Res 29:1259–1266
Ergas SJ, Rheinheimer DE (2004) Drinking water denitrification using a membrane bioreactor. Water Res 38:3225–3232
García-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martínez-Molina E, Mateos PF, Velázquez E (2007) Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol 57:844–848
Hagman M, Nielsen JL, Nielsen PH, Jansen JC (2008) Mixed carbon sources for nitrate reduction in activated sludge-identification of bacteria and process activity studies. Water Res 42:1539–1546
Jirout J, Simek M, Elhottova D (2013) Fungal contribution to nitrous oxide emissions from cattle impacted soils. Chemosphere 90:565–572
Kesserü P, Kiss I, Bihari Z, Polyák B (2002) The effects of NaCl and some heavy metals on the denitrification activity of Ochrobactrum anthropi. J Basic Microbiol 42:268–276
Kim MK, Jung H-Y (2007) Chitinophaga terrae sp. nov., isolated from soil. Int J Syst Evol Microbiol 57:1721–1724
Lim Y, Lee S, Kim SB, Yong H, Yeon S, Park Y, Jeong D, Park J (2005) Diversity of denitrifying bacteria isolated from Daejeon sewage treatment plant. J Microbiol 43:383–390
Lin Y, Tanaka S (2006) Ethanol fermentation from biomass resources: current state and prospects. Appl Microbiol Biotechnol 69:627–642
Liu SJ, Zhao ZY, Li J, Wang J, Qi Y (2013) An anaerobic two-layer permeable reactive biobarrier for the remediation of nitrate-contaminated groundwater. Water Res 47:5977–5985
Millati R, Edebo L, Taherzadeh MJ (2005) Performance of Rhizopus, Rhizomucor, and Mucor in ethanol production from glucose, xylose, and wood hydrolyzates. Enzym Microb Technol 36:294–300
Mohana S, Shah A, Divecha J, Madamwar D (2008) Xylanase production by Burkholderia sp. DMAX strain under solid state fermentation using distillery spent wash. Bioresour Technol 99:7553–7564
Mosquera-Corral A, Sanchez M, Campos J, Méndez R, Lema J (2001) Simultaneous methanogenesis and denitrification of pretreated effluents from a fish canning industry. Water Res 35:411–418
Mothapo NV, Chen H, Cubeta MA, Shi W (2013) Nitrous oxide producing activity of diverse fungi from distinct agroecosystems. Soil Biol Biochem 66:94–101
Mountfort DO, Rhodes LL (1991) Anaerobic growth and fermentation characteristics of Paecilomyces lilacinus isolated from mullet gut. Appl Environ Microbiol 57:1963–1968
Oehmen A, Keller-Lehmann B, Zeng RJ, Yuan Z, Keller J (2005) Optimisation of poly-β-hydroxyalkanoate analysis using gas chromatography for enhanced biological phosphorus removal systems. J Chromatogr A 1070:131–136
Papagianni M (2007) Advances in citric acid fermentation by Aspergillus niger: biochemical aspects, membrane transport and modeling. Biotechnol Adv 25:244–263
Polizeli M, Rizzatti A, Monti R, Terenzi H, Jorge J, Amorim D (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591
Rose R, Rose CL, Omi SK, Forry KR, Durall DM, Bigg WL (1991) Starch determination by perchloric acid vs enzymes: evaluating the accuracy and precision of six colorimetric methods. J Agric Food Chem 39:2–11
Sage M, Daufin G, Gesan-Guiziou G (2006) Denitrification potential and rates of complex carbon source from dairy effluents in activated sludge system. Water Res 40:2747–2755
Shen Z, Wang J (2011) Biological denitrification using cross-linked starch/PCL blends as solid carbon source and biofilm carrier. Bioresour Technol 102:8835–8838
Soares MIM, Abeliovich A (1998) Wheat straw as substrate for water denitrification. Water Res 32:3790–3794
Sun HY, Zhao PJ, Ge XY, Xia YJ, Hao ZK, Liu JW, Peng M (2010) Recent advances in microbial raw starch degrading enzymes. Appl Biochem Biotechnol 160:988–1003
Van Soest PV, Robertson J, Lewis B (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597
Volokita M, Belkin S, Abeliovich A, Soares MIM (1996) Biological denitrification of drinking water using newspaper. Water Res 30:965–971
Wang YY, Geng JJ, Ren ZJ, He WT, Xing MY, Wu M, Chen SW (2011) Effect of anaerobic reaction time on denitrifying phosphorus removal and N2O production. Bioresour Technol 102:5674–5684
Wang Y, Xue J, Zhou XD, You M, Du Q, Yang X, He JZ, Zou J, Cheng L, Li MY, Li YQ, Zhu YP, Li JY, Shi WY, Xu X (2014) Oral microbiota distinguishes acute lymphoblastic leukemia pediatric hosts from healthy populations. Plos One 9:e102116
Warneke S, Schipper LA, Matiasek MG, Scow KM, Cameron S, Bruesewitz DA, McDonald IR (2011) Nitrate removal, communities of denitrifiers and adverse effects in different carbon substrates for use in denitrification beds. Water Res 45:5463–5475
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
Yu HG, Wang QY, Wang ZW, Sahinkaya E, Li YL, Ma JX, Wu ZC (2014) Start-up of an anaerobic dynamic membrane digester for waste activated sludge digestion: temporal variations in microbial communities. Plos One 9:e93710
Yuan H, Chen Y, Zhang H, Jiang S, Zhou Q, Gu G (2006) Improved bioproduction of short-chain fatty acids (SCFAs) from excess sludge under alkaline conditions. Environ Sci Technol 40:2025–2029
Zablotowicz R, Eskew D, Focht D (1978) Denitrification in Rhizobium. Can J Microbiol 24:757–760
Zhang YQ, Yu LY, Wang D, Liu HY, Sun CH, Jiang W, Zhang YQ, Li WJ (2008) Roseomonas vinacea sp. nov., a Gram-negative coccobacillus isolated from a soil sample. Int J Syst Evol Microbiol 58:2070–2074
Zheng X, Chen YG, Wu R (2011) Long-term effects of titanium dioxide nanoparticles on nitrogen and phosphorus removal from wastewater and bacterial community shift in activated sludge. Environ Sci Technol 45:7284–7290
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This study was financially supported by the National Hi-Tech Research and Development Program (2011AA060903) and National Natural Science Foundation of China (51178324, 51278354, and 41301558).
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Wan, R., Zheng, X., Chen, Y. et al. Using cassava distiller’s dried grains as carbon and microbe sources to enhance denitrification of nitrate-contaminated groundwater. Appl Microbiol Biotechnol 99, 2839–2847 (2015). https://doi.org/10.1007/s00253-014-6155-z
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DOI: https://doi.org/10.1007/s00253-014-6155-z