Influence of nitrifying conditions on the ...

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Influence of nitrifying conditions on the biodegradation and sorption of emerging micropollutants E. Fernandez-Fontaina, F. Omil, J.M. Lema, M. Carballa* Department of Chemical Engineering, School of Engineering, University of Santiago de Compostela, Rua Lope Go´mez de Marzoa s/n, E-15782 Santiago de Compostela, Spain

article info

abstract

Article history:

High biodegradation efficiencies of different emerging micropollutants were obtained

Received 1 April 2012

with nitrifying activated sludge (NAS) working at high nitrogen loading rates (NLR), that

Received in revised form

boosted the development of biomass with high nitrifying activities (>1 g N-NHþ 4 /g VSS d).

17 July 2012

Come-tabolic biodegradation seemed to be responsible for the removal of most compounds

Accepted 18 July 2012

due to the action of the ammonium monooxygenase enzyme. NAS showed a different

Available online 28 July 2012

affinity for each compound, probably due to steric hindrance, activation energy limitations or the presence of specific functional groups. Increasing loading rates of micropollutants

Keywords:

were removed at shorter hydraulic retention times, although the biodegradation efficien-

Biodegradation

cies of compounds with slow/intermediate kinetics, such as fluoxetine, erythromycin,

Hydraulic retention time

roxithromycin and trimethoprim, diminished due to kinetic and/or stoichiometric limita-

Musk fragrance

tions. Solids retention time, always above the minimum to avoid the washout of nitrifiers,

Nitrifying sludge

did not enhance the biodegradation of any of the selected compounds, with the exception

Pharmaceutical

of diclofenac. Regarding sorption, the solideliquid distribution coefficients (Kd) obtained in NAS were very similar to those found in conventional activated sludge by other authors. No correlation between Kd values and any of the operational parameters was found for the selected substances. ª 2012 Elsevier Ltd. All rights reserved.

1.

Introduction

Continuous release of emerging micropollutants such as Pharmaceutical and Personal Care Products (PPCPs) from sewage treatment plant (STP) discharges could pose a risk for the environment as STPs have not been upgraded for the removal of this type of pollution. Sampling campaigns have been conducted in several STPs with different technologies and working at different operational conditions. In most cases, only overall removal efficiencies were determined (Simonich et al., 2002; Clara et al., 2005; Go¨bel et al., 2007; Vieno et al., 2007; Smook et al., 2008; Radjenovic et al., 2009), while few studies identified and quantified the removal efficiencies

related to the different mechanisms (Joss et al., 2004; Carballa et al., 2007a; Hoori et al., 2007; Wick et al., 2009; Xue et al., 2010). Activated sludge has proved to achieve a significant removal of many micropollutants (Joss et al., 2005), mostly due to biodegradation or to sorption on solids or colloids (Barret et al., 2010), but little is known about the influence of operational parameters on both mechanisms, which might explain the disparity of removal efficiencies found for similar technologies in the literature (Onesios et al., 2009). Hydraulic retention time (HRT) together with sludge retention time (SRT) govern both reaction time and loading (McAdam et al., 2010), thus affecting biomass activity and concentration. Activated sludge schemes for nutrient removal, operating at

* Corresponding author. Tel.: þ34 881816020; fax: þ34 881816702. E-mail addresses: [email protected] (E. Fernandez-Fontaina), [email protected] (F. Omil), [email protected] (J.M. Lema), [email protected] (M. Carballa). 0043-1354/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.watres.2012.07.037


long SRT, have been reported to achieve higher biodegradation efficiencies of different emerging micropollutants (Clara et al., 2005; Go¨bel et al., 2007), probably associated to the development of a more diverse microbial community, including the growth of nitrifying bacteria. Nitrifying activated sludge (NAS) has been first regarded as capable of degrading 17a-ethinylestradiol (EE2) through come-tabolism (Vader et al., 2000). Since then, other authors have tested the ability of nitrifying bacteria for the cometabolic degradation of a variety of emerging micropollutants (Kocamemi and Çeçen, 2005; Batt et al., 2006; Wahman et al., 2006; Yi and Harper, 2007; Forrez et al., 2008; Estrada-Arriaga and Mijaylova, 2010; Zhou and Oleszkiewicz, 2010; Martıńez-Hernańdez et al., 2011). Cometabolic oxidation by the ammonium monooxygenase (AMO) enzyme is probably ini-tiating the biotransformation of many of these substances. This enhanced elimination with NAS has been usually attributed to biodegradation by performing mass balances without measuring sorption onto sludge (Tran et al., 2009; Suarez et al., 2010). Moreover, the removal efficiencies reported are not homogeneous, which can be explained by the different operational conditions applied. Therefore, the purpose of this work was to determine the influence of nitrifying conditions, such as HRT, SRT, tempe-rature and nitrifying activity, on the biodegradation and sorption of 11 PPCPs in a pure nitrifying reactor. A synthetic feed rich in ammonium has been used, not only to obtain a pure nitrifying sludge, but also to avoid interaction of other pollutants with the compounds of interest. The experiments have been carried out in a long term operation, thus enabling more reliable conclusions.

2.

Materials and methods

2.1.

PPCPs

Three antiphlogistics (ibuprofen (IBP), naproxen (NPX) and diclofenac (DCF)), three antibiotics (trimethoprim (TMP), erythromycin (ERY) and roxithromycin (ROX)), an antidepressant (fluoxetine (FLX)), an antiepileptic (carbamazepine (CBZ)), a tranquillizer (diazepam (DZP)) and two musk fragrances (galaxolide (HHCB) and tonalide (AHTN)) were selected. Stock solutions (2000 and 5000 mg/L) in acetone or methanol were prepared prior to spike in the reactor feeding and the nominal concentrations of pharmaceuticals and musk fragrances fed to the reactor were 10 and 20 ppb, respectively.

2.2.

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develop autotrophic nitrifying biomass. A solution of trace elements (FeCl3, H3BO3, CuSO4, KI, ZnSO4, CoCl2 and MnCl2) and PPCPs (80e320 ppb) was also introduced in the synthetic feeding. The flowrates of the synthetic feeding and dilution water were adjusted in order to provide different influent concentrations: 40e500 mg N-NHþ 4 /L, 70e850 mg C-HCO3 /L, 3 10 mg P-PO4 /L and 10e20 ppb of PPCPs. Temperature, dissolved oxygen (DO) and pH were monitored online with a Hach HQ40d multi-parameter digital meter with data-logging capabilities. Influent, mixed liquor and effluent samples were taken twice a week for solids, ammonium, nitrite and nitrate determinations.

2.3.

Operational strategy

The operational strategy was designed to enrich an activated sludge inoculum with nitrifying bacteria. For that purpose, a synthetic feed was used, thus avoiding the side effects of other components present in sewage (interactions with AMO, growth of heterotrophic biomass, etc.). During the start-up period without PPCPs, the reactor was operated with an HRT of 4.3 d, an SRT of around 50 d and a nitrogen loading rate (NLR) of 0.02 g N-NHþ 4 /L d. From day 34 on, PPCPs were spiked in the feeding and the NLR was stepwisely raised to 0.12 g N-NHþ 4 /L d by increasing the ammonium concentrations in the influent, but maintaining the HRT in 4.3 d, in order to achieve higher nitrifying activities. From day 154 on, temperature started decreasing (winter period) reaching a minimum value of 15 2 C during days 195e205. In order to overcome this period of inhibition, the NLR was decreased to 0.01 g N-NHþ 4 /L d. Once the biomass recovered its nitrifying activity (i.e. nitrification was complete) at day 241, the NLR was again increased. From day 346, the temperature was controlled at 25 1 C, the HRT was lowered to 3.6 d and the strategy of nitrifiers enrichment by increasing the NLR was continued. From day 496, NLR was kept constant at around 0.1 g N-NHþ 4 /L d, and from day 566, HRT was decreased stepwise to 2.9, 2 and 1 day. Since the micropollutant concentrations in the feeding remained constant during the whole experiment, this HRT change derived in higher nominal micropollutant loading rates (from 2.5 to 10 mg/L d for pharmaceuticals and from 5 to 20 mg/L d for musk fragrances). The reactor was operated without sludge purge during the whole experimental period in order to avoid losses of the slowgrowing nitrifying bacteria. Consequently, SRT was only affected by solids sampling from the reactor and it remained above 20 days during the whole experiment, except for the last 20 days, which was around 10 days.

Experimental set-up 2.4.

A 30 L reactor coupled with a 5 L settler was inoculated with biomass collected from the nitrification/denitrification tanks of an STP (10,000 inh-eq) operated under a Biodenipho process for nutrient removal. The reactor was mechanically stirred and aeration was provided with diffusers located at the bottom of the reactor. Three peristaltic pumps were used to feed the concentrated synthetic feeding, the dilution water (tap water) and to recycle the biomass from the settler to the reactor. The concentrated synthetic feeding contained an inorganic carbon source (NaHCO3) and ammonium chloride (NH4Cl) in order to

Micropollutants analysis

Seven sampling campaigns (periods P1eP7) were conducted when the reactor was operated at different steady-state conditions (Table 1). After collecting the influent sample, the effluent and mixed liquor samples were taken after one residence time. Samples were collected in aluminum bottles, prefiltered (AP3004705, Millipore) and stored at 2 C prior to analysis. Mixed liquor samples were previously centrifuged (1200 rpm, 10 min) and the solids were frozen at 20 C. The soluble content of antiphlogistics, CBZ, DZP and musk

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Table 1 e Average operational conditions and performance of the nitrifying activated sludge (NAS) reactor during the sampling periods. Sampling period

Days T ( C) pH DO (mg/L) VSS (g/L) NLR (g N-NHþ 4 /L d) HRT (d) SRT (d) Nitrification (%) SNR (g N/g VSS d) SNA (g N/g VSS d)

P1

P2

P3

P4

P5

P6

P7

105e120 20 8.9 5.7 0.29 0.04 4.3 50 100 0.12 0.28

195e205 17 8.1 7.7 0.80 0.11 4.6 170 88 0.12 0.12

510e520 25 7.8 4.7 0.60 0.12 3.6 45 100 0.19 0.88

555e565 25 7.5 4.6 0.60 0.12 3.7 45 100 0.20 0.95

580e590 25 7.8 4.7 0.45 0.11 2.9 25 100 0.26 1.09

600e610 25 6.9 3.6 0.41 0.10 2.0 20 100 0.27 1.22

620e630 25 7.2 3.7 0.28 0.11 1.0 10 100 0.47 1.46

NLR, Nitrogen Loading Rate; SNR, Specific Nitrification Rate; SNA, Specific Nitrifying Activity. SNR represents the biomass activity in the reactor under the operational conditions and SNA represents the “maximum” activity of the biomass (see Section 2.6 for its determination).

fragrances was determined using Gas Chromatography coupled with Mass Spectrometry (GC/MS/MS), while antibiotics and fluoxetine were quantified using Liquid Chromatography coupled with Mass Spectrometry (LC/MS/MS) as described elsewhere (Serrano et al., 2011). Ultrasonic solvent extraction (USE) was performed as described by Ternes et al. (2005) in order to determine PPCPs concentrations on solids. Three sequential extractions with methanol and acetone were performed on the lyophilized solid samples. In each extraction, samples were sonicated for 15 min and centrifuged at 3000 rpm for 5 min. All supernatants were collected and combined, filtered through glass wool and concentrated by evaporation (R-205, Bu¨chi) under vacuum conditions at 35 C. After dilution with distilled water, solid phase extraction and quantification by GC/MS/MS and LC/MS/MS were performed similarly to the liquid samples.

2.5.

Micropollutants mass balances

CS TSS$CW

(1)

where CW and CS are the soluble and sorbed concentrations at equilibrium conditions (mg/L), respectively, and TSS is the total suspended solids concentration in the mixed liquor (g TSS/L). The fraction of each substance sorbed onto the solids, stripped by aeration and biodegraded was calculated with the following equations derived from the mass balance applied to the bioreactor. Solids withdrawal for analysis was also considered for an accurate calculation of micropollutants mass balances. Sorptionð%Þ ¼

CW;o $Kd $TSSo $100 CW;i

Volatilizationð%Þ ¼

H$qair $CW;o $100 CW;i

(2)

(3)

CW;o $100 CW;i

(4)

Biodegradationð%Þ ¼ 100 sorptionð%Þ volatilizationð%Þ effluentð%Þ

(5)

where CW,i and CW,o are the soluble concentrations of the substance in the feeding and the effluent (mg/L), respectively, TSSo is the total suspended solids concentration in the effluent (g TSS/L), H is the dimensionless Henry’s law constant (Joss et al., 2006) and qair the aeration applied per volume of reactor (Lair/Lreactor). Pseudo first-order kinetics was considered to describe biodegradation of micropollutants (rbiol ¼ kbiol $XVSS $CW ) according to Schwarzenbach et al. (2003). Biodegradation kinetic constants (kbiol, in L/g VSS d) were obtained performing micropollutants mass balances to the reactor: kbiol ¼

The solideliquid partition coefficient (Kd, in L/g TSS) of each PPCP was calculated with the following equation: Kd ¼

Effluentð%Þ ¼

CW;i CW;o 1 þ Kd $TSSo þ H$qair CW;o $VSS$HRT

(6)

where VSS is the volatile suspended solids concentration in the mixed liquor (g VSS/L) and HRT is the hydraulic retention time (d).

2.6.

Analytical techniques

Total and volatile suspended solids (TSS and VSS), nitrite and nitrate were determined following Standard Methods (APHA, 1999). Ammonium was determined after reaction with phenol and hypochlorite to give indophenol, whose absorbance was measured at 635 nm with a spectrophotometer (Shimadzu UV-1603, UVevisible). Total, inorganic and organic carbon (TC, IC and TOC) were determined by a Shimadzu analyzer (TOC-5000). Specific Nitrifying Activity (SNA), which is the maximum ammonia uptake rate per gram biomass (mg N-NHþ 4 /g VSS d), was determined experimentally in the reactor as follows: i) interruption of feeding and saturation of the reactor with oxygen; ii) interruption of aeration; iii) addition of a non-limiting concentration of substrate (4 mg N-NHþ 4 /L); iv) monitoring of DO concentration decrease.


Different bacterial populations were identified by fluorescence in situ hybridization (FISH). Biomass samples from the reactor were collected on days 0 and 565, disrupted and fixed according to the procedure described by Amman et al. (1995) with 4% paraformaldehyde solution. Hybridization of the FISH probes was performed at 46 C for 90 min adjusting formamide concentrations as defined at probeBase for the selected probes: EUB338 (Bacteria domain), ALF1B (a-proteobacteria, some d-proteobacteria, Spirochetes), GAM42a (g-proteobacteria), NEU653 (most halophilic and halotolerant Nitrosomonas spp.), NSO190 (ammonio-oxidizing b-proteobacteria), NIT3 (Nitrobacter spp.), Nstpa712 (most members of phylum Nitrospirae), which were labeled with fluorochromes Fluos and Cy3. Fluorescence signals were recorded with an acquisition system (Coolsnap, Roper Scientific Photometrics) coupled to an Axioskop 2 epifluorescence microscope (Zeiss, Germany).

3.

Results and discussion

3.1.

Nitrifying reactor performance

Several types of nitrifying rates were considered in this paper, each representing a different concept: Nitrogen Loading Rate (NLR), which is the amount of ammonia nitrogen fed per reactor volume (mg N-NHþ 4 /L d), and therefore only dependent on ammonium concentration in the feeding and on the flowrate; Specific Nitrification Rate (SNR), which is the amount of ammonia nitrogen consumed in the reactor per sludge mass (mg N-NHþ 4 /g VSS d) and it was determined by mass balance in the reactor; and Specific Nitrifying Activity (SNA), which is the maximum ammonia nitrogen uptake rate per sludge mass (mg N-NHþ 4 /g VSS d) determined experimentally as described in Section 2.6. During the start-up period, biomass concentrations lowered from 0.92 to 0.21 g VSS/L due to the lack of organic carbon in the feeding. Accordingly, heterotrophic activity decreased to 0.10 g O2/g VSS d and SNA attained 0.16 g N-NHþ 4 /g VSS d. After PPCPs addition, NLR was increased from 0.02 to 0.04 g N-NHþ 4 /L d /g VSS d during period P1, all this and SNA reached 0.28 g N-NHþ 4

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indicating an enrichment in ammonia oxidizing bacteria (AOB) and nitrite oxidizing bacteria (NOB). The temperature decrease from day 154 led to an improvement of sludge settleability, which resulted in a noticeable increase in solids concentration (and SRT), although this did not affect the SNR (0.12 g NNHþ 4 /g VSS d) due to the increase in NLR (period P2). The temperature control at 25 C worsened sludge settleability again, causing a reduction in VSS (and thus SRT) and an increase of SNR up to 0.19 g N-NHþ 4 /g VSS d (period P3). A further enrichment in AOB and NOB took place along the experiment, demonstrated by the gradual increase of SNA up to 1.46 g NNHþ 4 /g VSS d by the end of the reactor operation. Once HRT was stepwise reduced (from 3.7 to 1.0 d) in periods P4eP7, biomass concentrations halved (from 0.6 to 0.3 g VSS/L). As a consequence, SNR and SNA values increased (up to 0.47 and 1.46 g NNHþ 4 /g VSS d at biomass concentration of 0.28 g VSS/L) since the NLR was maintained almost constant and a complete nitrification took place during these periods. This AOB and NOB enrichment was also demonstrated by FISH (data not shown). After 565 days of operation, a large proportion of all bacteria were identified as Nitrosomonas spp. compared to the inoculum. Regarding NOB, bacteria of the phylum Nitrospirae was observed while the presence of Nitrobacter spp. was not detected.

3.2.

Micropollutants fate

CBZ, DCF and DZP displayed a recalcitrant behavior under all conditions tested and they were completely released with the effluent (data not shown). Only in P2, a biodegradation of 70% was achieved for DCF, fact that will be discussed more in detail in Section 3.3.3. Therefore, these substances were not considered in the analysis of operational conditions influence. The fate of the other 8 PPCPs in NAS in the periods with good nitrifying activities and similar HRT, SRT and biomass concentrations (P3 and P4) is shown in Fig. 1. Under these reference conditions, IBP, ERY, ROX, HHCB and AHTN were removed with efficiencies higher than 90%, while the elimination of NPX, FLX and TMP was lower (75e90%). A similar pattern was observed in the other sampling periods (data not shown). Suarez et al. (2010) also reported high removal efficiencies of all these compounds in NAS, with the exception of TMP

Fig. 1 e Fate of PPCPs in the nitrifying reactor during the sampling periods with extended HRT and 25 C (P3 and P4, average values with standard deviations).


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(14% vs. 78% in the present study), which has been reported to be hardly biodegradable in STPs (Paxeús, 2004; Go¨bel et al., 2007). Batt et al. (2006) also found higher biodegradation efficiencies of TMP in batch assays with NAS (70%) than with conventional activated sludge (CAS) (25%) and Ternes et al. (2007) reported the highest removal efficiency for TMP in an STP with nutrient removal. Sorption of micropollutants onto the biomass was almost negligible (75 mg biodegraded/g N removed) than for antibiotics and fluoxetine (1000 L/ kg TSS), while sorption of DZP, ROX, ERY and TMP was much more limited (100 L/kg TSS). Sludge concentrations of

Fig. 6 e Solideliquid partitioning coefficients (Kd) of different PPCPs in NAS.

antiphlogistics (IBP, NPX and DCF) and CBZ were always below the limit of quantification, and therefore, their Kd values could not be calculated. No bibliographic data were found regarding sorption of PPCPs on NAS, and therefore, the values obtained were compared with available data in CAS and membrane bioreactors (MBR). HHCB (2428 1297 L/kg TSS) and AHTN (3347 1900 L/kg TSS) showed lower Kd values than previous studies in CAS or MBR (Joss et al., 2005; Kupper et al., 2006; Reif, 2012), but higher than those reported by Ternes et al. (2004) in batch assays. The high Kd of FLX (1603 905 L/kg TSS) was also reported by Reif (2012) in an MBR. DZP showed an intermediate sorption behavior (116 52 L/ kg TSS) in the same range as those reported by Reif (2012) in MBR sludge, but higher than the Kd provided by Ternes et al. (2004) in batch operation. Kd for ERY (74 26 L/kg TSS) and ROX (75 48 L/kg TSS) were similar to those obtained by Radjenovic et al. (2009) and Reif (2012), while the value achieved for TMP (45 30 L/kg TSS) was lower. Negligible Kd values were also obtained by other authors (Ternes et al., 2004; Carballa et al., 2008; Radjenovic et al., 2009) for antiphlogistics and CBZ in different types of sludge. No correlations were found between Kd values of the different PPCPs in NAS and operational parameters analyzed, such as temperature, HRT, SRT or nitrifying activity (standard deviations in Fig. 6 could not be associated with any operational condition). This was already expected as, beside compounds physico-chemical properties and sludge characteristics, the only operating parameter affecting Kd values is pH, whose variation was not enough to exert a clear effect on Kd. Yet, after analyzing bibliographic data, it seems quite clear that Kd values determined in batch assays are significantly lower than those determined from continuous reactors, highlighting the importance of measuring sorption coefficients under the real operating conditions.

4.

Conclusions

Good nitrifying activities increased the biodegradation rates of different PPCPs (IBP, NPX, TMP, ROX, ERY, FLX, HHCB and AHTN), with AMO as the main responsible of the come-tabolic biodegradation. Thus, the higher the NLR in activated sludge


reactors the higher the removal of these emerging micropollutants. NAS showed a different affinity for each compound, pro-bably due to a preferential substrate selection between micropollutants, which might explain the discrepancies in removal efficiencies found in the literature. This competition among micropollutants for the biodegradation capacity of the activated sludge should be further researched. Those compounds with slow/intermediate kinetics such as FLX or the antibiotics will experience lower biodegradation efficiencies if shorter HRTs or increasing loading rates are applied. At this point, it cannot be concluded if biodegradation is limited by kinetics and/or by stoichiometry and future research is needed to clarify this point. Sorption coefficients (Kd) in NAS of most PPCPs were very similar to those found in CAS by other authors and no correlation between Kd values and any of the operational parameters was found.

Acknowledgments This research was supported by the Spanish Ministry of Education and Science through NOVEDAR_Consolider (CSD2007-00055) project, by the Spanish Ministry of Science and Innovation through INNOTRAZA (CTQ2010-20240) project and by the Xunta de Galicia through predoctoral (Lucas La-brada program) and postdoctoral (Isidro Parga Pondal program, IPP08-37) contracts.

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