Nitrate (NO3−) loads from domestic and industrial wastewater contribute to surface and groundwater pollution and can have detrimental effects on human health and the environment. In this study, a particulate pyrite autotrophic denitrification (PPAD) process was compared with sulfur-oxidizing denitrification (SOD) in batch microcosms using a domestic wastewater seed. During a 65-day acclimation period, denitrification rates for PPAD reached 3.19 mg/(L·d), but were slower than the maximum rate for SOD (∼5 mg/[L·d]). Lower sulfate (SO42−) production (5.66 mg SO42−/mg NO3−-N) and alkalinity consumption (1.70 mg CaCO3/mg NO3−-N) were observed with PPAD than with SOD (7.54 mg SO42−/mg NO3−-N and 4.57 mg CaCO3/mg NO3−-N). Acetone pretreatment of pyrite particles initially resulted in a transient increase in the denitrification rate; however, the rate of denitrification was similar to untreated pyrite in subsequent cycles. Box–Behnken design and response surface methodology were used to optimize biomass concentration, pyrite dose, and particle size. Denitrification rates were highest at a volatile suspended solids concentration of 1,250 mg/L, a pyrite dose of 125 g/L, and a particle size of 0.815–1.015 mm. The PPAD process is a promising technology for the treatment of NO3−-contaminated water and wastewater due to low biomass and sulfur by-product production, low alkalinity consumption and low carry-over of organic carbon to the effluent.
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References
1.
AkcilA., and KoldasS. (2006). Acid mine drainage (AMD): Causes, treatment and case studies. J. Clean. Prod., 14, 1139.
2.
AnnaduraiG., and SheejaR.Y. (1998). Use of Box-Behnken design of experiments for the adsorption of verofix red using biopolymer. Bioprocess. Eng., 18, 463.
3.
APHA. (2012). Standard Methods for the Examination of Water & Wastewater. Washington, DC: American Public Health Association (APHA), American Water Works Association (AWWA) & Water Environment Federation (WEF).
4.
BaesemanJ.L., SmithR.L., and SilversteinJ. (2006). Denitrification potential in stream sediments impacted by acid mine drainage: Effects of pH, various electron donors, and iron. Microbial. Ecol., 51, 232.
5.
BatchelorB., and LawrenceA.W. (1978). A kinetic model for autotrophic denitrification using elemental sulfur. Water Res. 12, 1075.
6.
BernerR.A., and PetschS.T. (1998). The sulfur cycle and atmospheric oxygen. Science, 282, 1426.
7.
BingölD., VeliS., ZorS., and ÖzdemirU. (2012). Analysis of adsorption of reactive azo dye onto CuCl2 doped polyaniline using Box–Behnken design approach. Synth. Met., 162, 1566.
8.
Bonnissel-GissingerP., AlnotM., EhrhardtJ., and BehraP. (1998). Surface oxidation of pyrite as a function of pH. Environ. Sci. Technol., 32, 2839.
9.
BoschJ., LeeK., JordanG., KimK., and MeckenstockR.U. (2012). Anaerobic, nitrate-dependent oxidation of pyrite nanoparticles by Thiobacillus denitrificans. Environ. Sci. Technol., 46, 2095.
10.
BoxG.E.P., and BehnkenD.W. (1960). Some new three level design for the study of quantitative variables. Technometrics, 2, 455.
11.
BuscaG., LiettiL., RamisG., and BertiF. (1998). Chemical and mechanistic aspects of the selective catalytic reduction of NOx by ammonia over oxide catalysts: A review. Appl. Catal. B Environ., 18, 1.
12.
ClémentJ.C., ShresthaJ., EhrenfeldJ.G., and JafféP.R. (2005). Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol. Biochem., 37, 2323.
13.
GlassC., and SilversteinJ. (1998). Denitrification kinetics of high nitrate concentration water: pH effect on inhibition and nitrite accumulation. Water Res. 32, 831.
14.
GlassC., and SilversteinJ. (1999). Denitrification of high-nitrate, high-salinity wastewater. Water Res. 33, 223.
15.
HaaijerS.C.M., LamersL.P.M., SmoldersA.J.P., JettenM.S.M., and Op den CampH.J.M. (2007). Iron sulfide and pyrite as potential electron donors for microbial nitrate reduction in freshwater wetlands. Geomicrobiol. J., 24, 391.
16.
HongS., ZhangJ., FengC., ZhangB., and MaP. (2012). Enhancement of nitrate removal in synthetic groundwater using wheat rice stone. Water Sci. Technol., 66, 1900.
17.
IvanovV., WangJ.Y., StabnikovaO., KrasinkoV., StabnikovV., TayS.L., and TayJ.H. (2004). Iron-mediated removal of ammonium from strong nitrogenous wastewater from food processing. Water Sci. Technol., 49, 421.
18.
JørgensenC.J., JacobsenO.S., ElberlingB., and AamandJ. (2009). Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment. Environ. Sci. Technol., 43, 4851.
19.
KiskiraK., PapirioS., van HullebuschE.D., and EspositoG. (2017). Fe(II)-mediated autotrophic denitrification: A new bioprocess for iron bioprecipitation/biorecovery and simultaneous treatment of nitrate-containing wastewaters. Int. Biodeter. Biodegr., 119, 631.
20.
KluegleinN., ZeitvogelF., StierhofY.D., FloetenmeyerM., KonhauserK.O., KapplerA., and ObstM. (2014). Potential role of nitrite for abiotic Fe (II) oxidation and cell encrustation during nitrate reduction by denitrifying bacteria. Appl. Environ. Microbiol., 80, 1051.
21.
KolleW., StrebelO., and BottcherJ. (1985). Formation of sulfate by microbial denitrification in a reducing aquifer. Water Supply, 3, 35.
22.
KoromS.F. (1992). Natural denitrification in the saturated zone: A review. Water Resour. Res., 28, 1657.
23.
KrossD.C., HallbergG.R., BrunerD.R., CherryholmesK., and JohnsonJ.K. (1993). The nitrate contamination of private well water in Iowa. Am. J. Public Health, 83, 270.
24.
LiR., MorrisonL., CollinsG., LiA., and ZhanX. (2016). Simultaneous nitrate and phosphate removal from wastewater lacking organic matter through microbial oxidation of pyrrhotite coupled to nitrate reduction. Water Res. 96, 32.
25.
LiuH., JiangW., WanD., and QuJ. (2009). Study of a combined heterotrophic and sulfur autotrophic denitrification technology for removal of nitrate in water. J. Hazard. Mater., 169, 23.
26.
LiuL.H., and KoeingA. (2002). Use of limestone for pH control in autotrophic denitrification: Batch experiments. Process. Biochem., 37, 885.
27.
Lopez-PonnadaE.V., LynnT.J., PetersonM., ErgasS.J., and MihelcicJ.R. (2017). Application of denitrifying wood chip bioreactors for management of residential non-point sources of nitrogen, J. Biol. Eng., 11, 16.
28.
LuH., WangJ., LiS., ChenG., van LoosdrechtM.C.M., and EkamaG.A. (2009). Steady-state model-based evaluation of sulfate reduction, autotrophic denitrification and nitrification integrated (SANI) process. Water Res. 43, 3613.
29.
LvX., SongJ., LiJ., and WuF. (2017). Tertiary denitrification by sulfur/limestone packed biofilter. Environ. Eng. Sci., 34, 103.
30.
McCartyP.L. (1975). Stoichiometry of biological reactions. Prog. Water Technol., 7, 157.
31.
MirzoyanN., KamyshnyA., and HalevyI. (2014). An improved pyrite pretreatment protocol for kinetic and isotopic studies. Geochem. Trans., 15, 1.
32.
NordhoffM., TominskiC., HalamaM., ByrneJ.M., ObstM., KleindienstS., and KapplerA. (2017). Insights into nitrate-reducing Fe (II) oxidation mechanisms through analysis of cell-mineral associations, cell encrustation, and mineralogy in the chemolithoautotrophic enrichment culture KS. Appl. Environ. Microbiol., 83, e00752-17.
33.
OhJ., and SilversteinJ. (1999). Effect of air on-off cycles on activated-sludge denitrification. Water Environ. Res., 71, 1276.
34.
OhS.E., YooY.B., YoungJ.C., and KimI.S. (2001). Effect of organics on sulfur-utilizing autotrophic denitrification under mixotrophic conditions. J. Biotechnol., 92, 1.
35.
OteroN., TorrentóC., SolerA., MencióA., and Mas-PlaJ. (2009). Monitoring groundwater nitrate attenuation in a regional system coupling hydrogeology with multi-isotopic methods: The case of Plana de Vic (Osona, Spain). Agric. Ecosyst. Environ., 133, 103.
36.
PengY.Z., and ZhuG.B. (2006). Biological nitrogen removal with nitrification and denitrification via nitrite pathway. Appl. Microbiol. Biotechnol., 73, 15.
37.
PourghahramaniP., and AkhgarB.N. (2015). Characterization of structural changes of mechanically activated natural pyrite using XRD line profile analysis. Int. J. Miner. Process., 134, 23.
38.
PuJ., FengC., LiuY., LiR., KongZ., ChenN., TongS., HaoC., and LiuY. (2014). Pyrite-based autotrophic denitrification for remediation of nitrate contaminated groundwater. Bioresour. Technol., 173, 117.
39.
RimstidtJ.D., and VaughanD.J. (2003). Pyrite oxidation: A state-of-the-art assessment of the reaction mechanism. Geochim. Cosmochim. Acta, 67, 873.
40.
SchippersA., and BoB.J. (2002). Biogeochemistry of pyrite and iron sulfide oxidation in marine sediments. Geochim. Cosmochim. Acta, 66, 85.
41.
SenguptaS., ErgasS.J., and Lopez-LunaE. (2007). Investigation of solid-phase buffers for sulfur-oxidizing autotrophic denitrification. Water Environ. Res., 79, 2519.
42.
SievertS.M., ScottK.M., KlotzM.G., ChainP.S., HauserL.J., HempJ., HüglerM., LandM., LapidusA., LarimerF.W., LucasS., MalfattiS.A., MeyerF., PaulsenI.T., RenQ., and SimonJ. (2008). Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol., 74, 1145.
43.
SuminoT., IsakaK., IkutaH., SaikiY., and YokotT. (2006). Nitrogen removal from wastewater using simultaneous nitrate reduction and anaerobic ammonium oxidation in single reactor. J. Biosci. Bioeng., 102, 346.
44.
TongS., ChenN., WangH., LiuH., TaoC., FengC., ZhangB., HaoC., PuJ., and ZhaoJ. (2014). Optimization of C/N and current density in a heterotrophic/biofilm-electrode autotrophic denitrification reactor (HAD-BER). Bioresour. Technol., 171, 389.
45.
TongS., Rodriguez-GonzalezL.C., FengC., and ErgasS.J. (2017a). Comparison of particulate pyrite autotrophic denitrification (PPAD) and sulfur oxidizing denitrification (SOD) for treatment of nitrified wastewater. Water Sci. Technol., 75, 239.
46.
TongS., StocksJ.L., Rodriguez-GonzalezL.C., FengC., and ErgasS.J. (2017b). Effect of oyster shell medium and organic substrate on the performance of a particulate pyrite autotrophic denitrification (PPAD) process. Bioresour. Technol., 244, 296.
47.
TongS., ZhangB., FengC., ZhaoY., ChenN., HaoC., PuJ., and ZhaoL. (2013). Characteristics of heterotrophic/biofilm-electrode autotrophic denitrification for nitrate removal from groundwater. Bioresour. Technol., 148, 121.
48.
TorrentóC., CamaJ., UrmenetaJ., OteroN., and SolerA. (2010). Denitrification of groundwater with pyrite and Thiobacillus denitrificans. Chem. Geol., 278, 80.
49.
TorrentóC., UrmenetaJ., OteroN., SolerA., ViñasM., and CamaJ. (2011). Enhanced denitrification in groundwater and sediments from a nitrate-contaminated aquifer after addition of pyrite. Chem. Geol., 287, 90.
50.
USEPA. (1997). Methods for the Determination of Organic and Inorganic Compounds in Drinking Water. EPA/815-R-00-014. Washington, DC: United States Environmental Protection Agency.
51.
VaclavkovaS., Schultz-JensenN., JacobsenO.S., ElberlingB., and AamandJ. (2015). Nitrate-controlled anaerobic oxidation of pyrite by cultures. Geomicrobiol. J., 32, 412.
52.
VogtsM., IkumiD.S., and EkamaG.A. (2015). The removal of N and P in aerobic and anoxic-aerobic digestion of waste activated sludge from biological nutrient removal systems. Water SA, 41, 199.
53.
YavuzB., TürkerM., and EnginG.Ö. (2007). Autotrophic removal of sulphide from industrial wastewaters using oxygen and nitrate as electron acceptors. Environ. Eng. Sci., 24, 457.
54.
ZhangJ., FengC., HongS., HaoH., and YangY. (2012a). Behavior of solid carbon sources for biological denitrification in groundwater remediation. Water Sci. Technol., 65, 1696.
55.
ZhangY., SlompC.P., BroersH.P., BostickB., PassierH.F., BöttcherM.E., OmoregieE.O., LloydJ.R., PolyaD.A., and CappellenP.V. (2012b). Isotopic and microbiological signatures of pyrite-driven denitrification in a sandy aquifer. Chem. Geol., 300–301, 123.
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