Denitrification (OLAND) for anaerobic latex processing wastewater treatment

International Biodeterioration & Biodegradation xxx (2017) 1e11

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Application of Oxygen Limited Autotrophic Nitritation/Denitrification (OLAND) for anaerobic latex processing wastewater treatment Nguyen Nhu Hien a, Doan Van Tuan b, Phan The Nhat c, Truong Thi Thanh Van c, Nguyen Van Tam c, V.O. Nguyen Xuan Que c, Nguyen Phuoc Dan c, * a b c

Institute for Environment and Resources, National University of Ho Chi Minh City, Viet Nam Department of Civil and Environmental Engineering, Yonsei University, Seoul, South Korea Faculty of Environment and Natural Resource, Ho Chi Minh City University of Technology, Viet Nam

a r t i c l e i n f o

a b s t r a c t

Article history: Received 18 March 2017 Received in revised form 18 July 2017 Accepted 18 July 2017 Available online xxx

The study aimed to remove nitrogenous compounds from anaerobic latex processing wastewater by using Oxygen Limited Autotrophic Nitritation/Denitrification (OLAND) process in a single reactor with rotating bio-carrier and sequencing batch regime. The anaerobic latex processing effluent, of which suspended solids (SS) and biodegradable COD (bCOD) were removed by latex scum trap, coagulationflocculation and followed by Upflow Anaerobic Sludge Blanket Reactor (UASB), contained 100
1 total nitrogen (TN) and 50e80 mg l
1 COD. Dissolved oxygen (DO) e200 mg l
1 NHþ 4 -N, 150e250 mg l in the experiment was maintained at different concentration ranges of 0.4e0.8 mg l
1; 0.2e0.4 mg l
1 and 0.1e0.2 mg l
1. The highest performance (TN and COD removals, 94% and 61%, respectively) obtained at DO range of 0.10e0.20 mg l
1. Moreover, the low effluent nitrate (8.5 ± 3.1 mg l
1 NO
3 -N), which was less than that of theoretical reaction of OLAND, shown that, in the single reactor, co-existence of denitrifiers using the remaining bCOD (less than 50 mg l
1) in the feed wastewater or carbon source from cell lysis at high sludge retention time (about 90 days). Analysis of bacteria community showed that Candidatus Kuenenia, anammox bacteria, was dominant species in the sludge mixture of biofilm and bioflocs (4.8%) with 99% of sequence identities. AOB species, nitrifying bacteria, had 6.6% with 98% of sequence identities. Besides, denitrifying Proteobacterium E4-1 was found in the reactor. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Anaerobic latex processing wastewater Anammox nitrOgen removal Oxygen limited OLAND

1. Introduction Vietnam is a top five of countries having the biggest growing area and natural latex production of rubber industry in the world (Le, 2010). Natural latex production has strongly developed in the South-East region of Vietnam. This industry generates heavy water pollution in term of large discharge of wastewater containing high COD (3500e14000 mg l
1), SS (200e700 mg l
1) and total nitrogen (200e1800 mg l
1) (Mohammadi et al., 2010). Most of current latex processing wastewater treatment plants use traditional biological treatment methods such as anaerobic process followed by activated sludge processes (Anoxic-Oxic process, SBR, and oxidation ditch) or anaerobic-cum-facultative lagoon/aerated lagoon system to remove organic matter and nitrogen (Nguyen and Luong, 2012). These techniques require large space, high aeration energy

* Corresponding author. E-mail address: [email protected] (N. Phuoc Dan).

consumption, external organic carbon supply and high sludge treatment cost. In recent years, several promising biological technologies, which consume less energy and chemicals, have applied for removal of nitrogen compounds in wastewater. A new invention that created a “short-cut” in the nitrogen cycle called ANaerobic AMMonium OXidation (anammox) has become an interesting topic for many researches. In fact, the process has more advantages than traditional nitrification-denitrification due to the engagement of autotrophic bacteria that contributed to eliminating supplement of exogenous organic carbon source, less sludge production, reducing energy demand for aeration and CO2 emission. The current anammoxebased technologies classify as follows: (i) two separate stage process, in which a partial nitritation reactor followed by an anammox one, and (ii) single stage process, in which the partial nitritation and anammox occurs in a single reactor. The single sludge system is widely used for wastewater with high load organic matter, which strongly inhibits anammox bacteria (Van Hulle et al.,

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2010). The single sludge process includes Sharon-Anammox processes (Van Dongen et al., 2001; Fux et al., 2002), completely autotrophic nitrogen removal over nitrite (CANON) (Sliekers et al., 2002) and Single stage Nitrogen removal using the Anammox and Partial nitritation (SNAP) (Lieu et al., 2006), Simultaneous partial Nitrification Anammox and Denitrification (SNAD) (Chen et al., 2009) and Oxygen-limited Autotrophic nitrification/denitrification (OLAND) developed at Ghent University (Kuai and Verstraete, 1998). In OLAND process, a mixed bacterial community, which comprises aerobic ammonium-oxidizing bacteria (AOB) and anoxic ammonium-oxidizing or anammox bacteria, well grows in a single reactor like rotating biological contactor (RBC) (Kuai and Verstraete, 1998). AOB partially convert about a half of the ammonium to nitrite at low concentration of dissolved oxygen as the electron acceptor (partial nitritation) and anammox bacteria subsequently use ammonium coupled with the produced nitrite as the electron acceptor (Strous et al., 1998; Pynaert et al., 2003). Some previous studies shown high performance of OLAND process for ammonium-rich wastewater. Windey et al. (2005) reported that a lab-scale RBC running under OLAND condition obtain nitrogen removal of 84% at NLR of 0.73 g N l
1 day
1 under high salinity (30 g l
1). OLAND process achieved a stable nitrogen removal rate of 0.71 g N l
1 day
1 and 0.41 g N l
1 day
1 for digested black water from vacuum toilet with ammonium concentration of above 1000 mg N l
1 (Vlaeminck et al., 2009) and landfill leachate with ammonium concentration of 250 mg N l
1 (Siegrist et al., 1998), respectively. Moreover, OLAND RBC also efficiently used for low ammonium strength wastewater like sewage with ammonium concentration less than 66 mg N l
1. However, application of OLAND to obtain a good performance has the following challenges in the practice (Vlaeminck et al., 2009): (i) Slow growth rate of the anammox bacteria in granules, flocs or biofilms results in long start-up period of rector as well as requires a high biomass retention (Van der Star et al., 2007), (ii) high nitrogen removal depends on limited nitrite accumulation obtained when AOB activity does not excess anammox one and (iii) high nitrogen efficiency requires a limited nitrate production. Anammox bacteria convert 11% of the oxidized ammonium into nitrate in OLAND reactor (Vlaeminck et al., 2009). Dissolve oxygen (DO) plays an important role in maintaining coexistence of AOB and anammox bacteria in a single reactor. The study of Windey et al. (2005) maintained DO level in an OLAND RBC less than 1 mg l
1 by controlling rotation peed of 2.5 rpm with 58% submergence of the disk surface area. AOB need 1.8 g O2 g-1 N to oxidize sufficiently ammonium while formations of excess nitrite level require avoiding. On the other hand, low DO concentrations (0.3 mg l
1) are required to limit excess nitrate production by NOB (Joss et al., 2009). Beside anammox bacteria, which develop under the anaerobic condition was reversibly inhibited by DO concentration above 0.25 mg l
1 (Egli et al., 2001). Effluents from upflow anaerobic sludge blanket reactor (UASB), anaerobic waste stabilization pond or anaerobic filter, which are the preferred technique to remove biodegradable COD (bCOD) from the natural rubber processing wastewater, contained high ammonium concentration and low soluble COD/N ratio (Mohammadi et al., 2010; Jawjit and Liengcharernsit, 2010). Thus, application of OLAND for the anaerobic latex processing effluent may be a feasible technique. The fact that an evaluation of sludge reject water treatment showed that OLAND can save 30e40% of the overall nitrogen treatment costs (Fux and Siegrist, 2004), due to a lower aeration requirement, sludge production, and organic carbon addition. Until now, use of OLAND process for wastewater treatment of rubber processing industry has not studied before. Therefore, the

aims of the study were (i) to successfully inoculate nitrifiers, denitrifiers and anammox bacteria in a single stage reactor coupled with rotating bio-carrier and sequencing batch regime, and then (ii) to evaluate the performance of the single reactor for nitrogen and COD removals from the anaerobic latex processing effluent at the different DO levels. 2. Materials and method 2.1. Reactor Hybrid oxygen limited nitritation autotrophic denitrification process in a single stage reactor coupled with vertical-axis rotating bio-carrier and sequencing batch mode (SBR) was used in the study (Fig. 1). The reactor with total working volume of 34.4 L was an acrylic plastic cylinder with height of 61 cm and inner diameter of 30.5 cm. The bio-carrier was 32 porous non-woven polyester pieces (lengthxwidth x thickness of 9.0  8.5  1.0 cm each piece) which were mounted on a stainless steel bar turbine-shaped frame with diameter of 19.6 cm. A vertical axis motor mounted to the support frame rotated at 10 rpm. Total surface area of all polyester pieces with the porosity of 80% is about 700 cm2. Air was supplied through air diffusors placed at the reactor bottom. Air flow was adjusted by an automatic control system including DO sensor connected to an air compressor to maintain the desired DO concentration. 2.2. Synthetic wastewater for enrichment Enrichment in this study using synthetic wastewater aimed to develop AOB and anammox bacteria in biofilm and bioflocs. The synthetic wastewater I for anammox bacteria included 20e125 mg l
1 NH4Cl-N, 20e125 mg l
1 NaNO2-N, 500 mg l
1 KHCO3, 54 mg l
1 KH2PO4, 180 mg l
1 CaCl2$2H2O, 120 mg l
1 MgSO4$7H2O, 2 ml l
1 of trace solutions, whereas the solution II for AOB enrichment contained 250 mg l
1 NH4Cl-N, 3000 mg l
1 NaHCO3, 15.5 mg l
1 KH2PO4, 27.7 mg l
1 CaCl2, 500 mg l
1 NaCl, 5 ml l
1 of trace solution (Belser and Schmidt, 1978; Van de Graaf et al., 1996). 2.3. Anaerobic latex processing effluent The feed wastewater used in the study was latex processing effluent of which bCOD (biodegradable COD) was significantly removed. The effluent was taken from Upflow Anaerobic Sludge Blanket (UASB) reactor of a wastewater treatment plant of Phuoc Hoa Latex processing Company located in Binh Duong province, Vietnam. To remove the remaining bCOD, the sampled wastewater was stored an influent tank at least 7 days at the ambient air temperature (25e32  C) before feeding into the reactor. The characteristics of the feed wastewater were shown in Table 1. 2.4. Anammox bacteria and AOB seeds Anammox bacteria and AOB seeds were collected from a pilotscale old landfill leachate treatment system including a partial nitritation sequencing batch reactor followed by an anammox internal contactor. 90 g of anammox biomass in granular sludge was harvested from the anammox internal contactor which was running at nitrogen loading rate (NLR) of 10 kg m
3 day
1 TN. Anammox granule sludge was characterized with ratio MLVSS: MLSS ratio of 0.6, granule diameter of 0.5e3.0 mm and maximum anammox activity of 0.58 gN2-N g
1VSS h
1. 30 g of AOB sludge was collected from the partial nitritation sequencing batch reactor running at 0.9 kg N m
3 day
1. AOB in bioflocs had MLVSS:MLSS
1
1 ratio of 0.76 and maximum activity of 8.9 gNHþ 4 -N g VSS h .

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Fig. 1. Schematic diagram of the experiment: (1) NaHCO3 solution tank, (2) influent tank, (3) reactor and (4) effluent tank.

Table 1 Characteristic of the feed anaerobic latex processing wastewater in the study. Parameter

Unit

Range

Mean value ± std (n ¼ 75)

pH sCOD(*) SS TKN NHþ 4 -N NO
2 -N
NO3 -N Alkalinity

e mg mg mg mg mg mg mg

7.2e7.5 47e80 56e82 118e198 112e179 0.1e1.56 0.52e4.24 507e865

7.3 ± 0.1 59 ± 9 75 ± 7 166 ± 25 153 ± 21 0.49 ± 0.45 1.56 ± 1.12 721 ± 137

l
1 l
1 l
1 l
1 l
1 l
1 l
1 CaCO3

Note: (*) samples for sCOD (soluble COD) analysis were filtered using Whatman 0.45 mm filter papers.

2.5. Operating conditions The experiment was carried out at the laboratory of Ho Chi Minh City University of Technology, Vietnam National University-HCM. The room temperature ranged from 25  C to 32  C. The single reactor daily run with three 480-min cycles including four stages: (a) 10 min for feeding, (b) 420 min for reacting, (c) 40 min for settling and (d) 10 min for discharging. The reactor was operated at the volume exchange ratio of 0.5 and hydraulic retention time (HRT) of 0.6 days.

2.6. Enrichment using synthetic wastewater The anammox bacteria enrichment was conducted with step increase of nitrogen loading rates of 0.08, 0.16 and 0.42 kgN m
3 day
1. The reactor was maintained in anaerobic condition with complete mixing by the rotating turbine-shaped frame. To avoid impact of DO in the feed, 8% Na2SO3 solution was added into the influent tank to obtain DO of the feed wastewater less than 0.5 mg l
1. pH values during the enrichment were 6.8e7.2. The enrichment was finished until the nitrogen removal reached over

80%. Afterwards, the AOB enrichment using synthetic wastewater II was carried out at NLR of 0.42 kgN m
3 day
1. Low DO concentration range of 0.4e0.8 mg l
1 and pH values of 7.5e7.8 were controlled during the enrichment. 2.7. Operation using anaerobic latex processing effluent Anaerobic latex processing effluent containing 118e198 mg l
1 Total Kjeldahl Nitrogen (TKN) was fed into the reactor after the nitrogen removal of the AOB enrichment was above 80%. All operation conditions including pH, DO, HRT and time of stages in the cycle were similar to those during the AOB enrichment. After a long-term stable operation at DO of 0.4e0.8 mg l
1, the DO concentration was stepwise decreased to 0.2e0.4 mg l
1 and 0.1e0.2 mg l
1. 2.8. Analytical methods 2.8.1. Chemical analysis Total suspended solids (TSS), volatile suspended solids (VSS),

sCOD, NHþ 4 -N, NO2 -N, NO3 -N, TKN and alkalinity were measured according to Standard Methods for examination of Water and Wastewater (Apha, 1998). 2.8.2. Maximum biomass activity tests Maximum AOB, NOB and anammox bacteria activity tests using a 2-L batch reactor for both bioflocs and biofilm were performed according to the method described by Third et al. (2001). The maximum AOB and NOB activity tests were conducted under oxygen saturation condition. 100 ml of biomass mixed with 1500 mL of solution containing 70 mg l
1 NHþ 4 -N and trace nutrients were added to the batch reactor placed on a magnetic stirrer. Ammonium, nitrate and nitrite were measured every half hour for up to two hours. To measure the maximum anammox bacteria activity, bioflocs

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or biofilm was taken from the single reactor and put into the airtight batch reactor containing nutrient solution with 70 mg l
1
1 NHþ NO
4 -N and 70 mg l 2 -N. The anaerobic condition was made by adding Na2SO3 solution into the batch test. Consumption of both nitrite and ammonium and nitrate production were measured every haft hour for up to four hours. All activities were calculated from the substrate consumption rate or nitrate production rate for biomass unit. Maximum denitrification activity of bioflocs or biofilm was measured by incubating biomass with excess glucose and 50 mg l
1 NO
3 -N in the batch test under anaerobic condition. Nitrate was measured every half hour for up to two hours. 2.8.3. Maximum microbial community analysis Biofilm in the single reactor was sampled for analysis of microbial community. Extraction of Metagenomic DNA from the biofilm was followed with the procedure described by GonzalezMartinez et al. (2015). The extraction used FastDNA SPIN Kit for Soil (MP Biomedicals, Solon, OH, USA) according to the instruction manual. Metagenomic DNA samples were then processed for Polymerase Chain Reaction (PCR). V3-4 region of 16S rRNA gene of bacteria was selected to evaluate in this study. PCR was performed in a thermal cycler using the following program: 3 min for initial denaturation at 95  C, followed 25 cycles of 30 s at 95  C, 30 s at 55  C, 30 s at 72  C, and then 5 min at final elongation at 72  C. The amplicon DNAs were performed PCR cleanup, 2nd stage PCR, PCR Clean-Up 2 and finally Library Quantification and Normalization that is described in the 16S Library Preparation Workflow. Raw sequences were then filtered, aligned, and clustered at 0.03 distances using the furthest algorithm to generate operational taxonomic units (OTUs), OTUs were then classified using the same database from Mothur software package (Version 1.34.3). OTUs of dominant groups were again classified again using the Blastn (online database) for finding closet matches. The gene specific sequences used in this study targeted the 16S V3 and V4

region. The full-length primer sequences, using standard IUPAC nucleotide nomenclature, to follow the protocol targeting this region as shown in Table 2. They were selected from Klindworth et al. (2013) primers for next generation sequencing (NGS)-based diversity studies. The overhang adapter sequence was added to the locus specific primer for the target region. 3. Results and discussion 3.1. Enrichment The reactor was run at NLRs of 0.08; 0.16 and 0.42 kg N m
3 day
1 for 30 days of the anammox enrichment. Fig. 2 presents the result of influent and effluent nitrogenous concentrations during the anammox enrichment. The anammox enrichment finished
when the obtained NHþ 4 -N: NO2 -N ratio was 1:1.25, reaching around value of 1:1.31 ± 0.06 (Van de Graaf et al., 1996), at NLR of 0.42 kg N m
3 day
1. The produced nitrate content in the effluent was equal to 11% of the removed TN. Almost anammox biomass in granules attached on the bio-carrier after 30 days, while less amount of granules existed in the flocs. Fig. 3 shows influent and effluent nitrogenous concentrations during the AOB enrichment at the influent NHþ 4 N concentration of 250 mg l
1. The AOB enrichment took place for 60 days at the NLR of 0.42 kg N m
3 day
1. The AOB enrichment completed when NHþ 4 -N completely converted and TN removal reached about 80% during the last ten days (from 51st day to 60th day). AOB biomass existed in both bioflocs and biofilm in the reactor after 60 days. The maximum AOB and anammox bacteria activities of both bioflocs and biofilm were tested on the day 58th before the enrichment finished. The maximum anammox bacteria activities of biofilm and flocs were 0.29 and 0.01 gN2-N gVSS
1 day
1, respectively. Low maximum anammox bacteria activity of bioflocs illustrated anammox bacteria insignificantly existed in the flocs, whereas AOB of bioflocs had higher activity than that of biofilm.

Table 2 Primers of V34 region of 16S rRNA gene. Gene

Primer name

Sequence (50 -30 )

Amplified products (bp)

Reference

16S rDNA

16S Amplicon PCR Forward Primer 16S Amplicon PCR Reverse Primer

TCGTCGGCAGCGTCAGATGTGTATAAGAGACAGCCTACGGGNGGCWGCAG

460

Klindworth et al., 2013

GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGGACTACHVGGGTATCTAATCC

Fig. 2. Influent and effluent nitrogenous concentrations during the anammox enrichment.

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1 Fig. 3. Influent and effluent nitrogenous concentrations during the AOB enrichment at the influent NHþ 4 -N concentration of 250 mg l .

Fig. 4. Time course of influent and effluent nitrogen compounds at different DO levels.

Fig. 5. Time course of influent and effluent sCOD concentrations at different DO levels.

Indeed, the maximum AOB activities of biofilm and bioflocs were
1
1 0.34 and 0.81 gNHþ 4 -N g VSS day , respectively. 3.2. Nitrogen removal performance After completing biomass enrichment, the reactor was

continuously operated with the anaerobic latex processing effluent for 75 days with 3 batches per day. Total Kjeldahl Nitrogen (TKN) of the feed wastewater was 166 ± 25 mg l
1, of which organic nitrogen content was 8.5 ± 3.1% (n ¼ 75). Thus, the nitrogen compound in the feed wastewater was mainly NHþ 4 -N. Fig. 4 and Fig. 5 show the variation of influent and effluent nitrogen compound concentration

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versus the operating time at three different controlled DO ranges. Difference of NHþ 4 -N concentrations in the feed wastewater was due to sampling from the site at different times. During the first 15 days of operation, DO was controlled at 0.4e0.8 mg l
1. The result shows that total nitrogen removal was unstable and fluctuated from 7.6% to 88%. After day 7th, NHþ 4 -N was completely converted, whereas the effluent nitrite (around 16 mg l
1 N) and nitrate concentrations (11 mg l
1N) were high. This points out that poor performance of anammox bacteria may be due to inhibition of DO levels above 0.4 mg l
1. The result was similar to that presented by Jetten et al. (1998); Egli et al. (2001). The reactor run at DO levels of 0.2e0.4 mg l
1 during from day 15th to day 30th. As a result, the mean total nitrogen removal increased to 93 ± 7% after day 22nd. Even though high TN removal efficiency obtained and effluent NHþ 4 -N was completely converted, the effluent nitrite-N and nitrate-N concentrations were relatively high at 15 ± 10 mg l
1 and 9 ± 7 mg l
1 (n ¼ 15), respectively. Thus, NHþ 4 -N ion that contributed as electronic donor in anammox reaction was deficient. In the next stage, lower DO range was maintained at 0.1e0.2 mg l
1during 45 days in order to reduce conversion rate of NHþ 4 -N to nitrite. The result reveals that total nitrogen removal efficiency was 92 ± 2% (n ¼ 45) with total nitrogen (TN) of 13 ± 4 mg l
1, free of
1 NHþ in the 4 -N and nitrate concentration of 8.5 ± 3.1 mg N l effluent. It is claimed that DO level of 0.1e0.2 mg l
1 was suitable for the combined partial nitritation and anammox process into a single reactor. Fig. 4 reveals that the effluent nitrate concentrations at all different DO levels were significantly lower than the therorical value defined in anammox reaction (0.26 g NO
3 -N produced from
1.0 g NHþ 4 -N and 1.32 g NO2 -N (Strous et al., 1998)). Moreover, COD removal of 36e56% was found in the reactor. This pointed out presence of denitrifiers which consumed bCOD and nitrate. The result also showed that at DO of 0.1e0.2 mg l
1, the effluent quality in terms of TN, NHþ 4 -N and COD concentrations meets the industrial effluent quality standards QCVN 01:2015/BTNMT, column A. A comparison of NHþ 4 -N and total nitrogen conversion rates between this study and some studies on CANON, OLAND and SNAP processes was shown in Table 3. The result shows that the total nitrogen removal efficiency of the reactor at DO of 0.1e0.2 mg l
1 and NLR of 0.42 kgN m
2 day
1 for synthetic wastewater was higher than OLAND/CANON reactors of Kuai and Verstraete (1998); Sliekers et al. (2002). However, the performance of this study in term of nitrogen removal rate (kgN m
3 day
1) was not better than that of Pynaert et al. (2003, 2004) that utilized a OLAND RBC (with specific surface area of 133 m2 m
3) for synthetic wastewater treatment at NLR of 1.19 kg N m
3 day
1 and that of Qiao et al. (2010) used biofilm SNAP reactor (with specific surface area of 147 m2 m
3) for high nitrogen-strength sludge digester liquor

treatment at NLR of 0.94 kgN m
3 day
1. The lower nitrogen removal rate of this study may be due to (i) less specific surface area of the carrier (with specific surface area of 2.2 m2 m
3), and (ii)
1 lower influent NHþ 4 -N concentration (250 mg l ) in comparison with high NHþ 4 -N-strength feed of the previous studies (600e1400 mg l
1) that strongly inhibited NOB and made easily þ substrates with NO
2 -N:NH4 -N ratio suitable for autotrophic denitrification process. This study obtained high nitrogen removal for the anaerobic latex processing wastewater at NLR of 0.25 kgN m
3 day
1. The average effluent TN (14 mg l
1) and NHþ 4 -N concentrations (0.3 mg l
1) of the single reactor at DO levels of 0.1e0.2 mg l
1 met the thresholds of the industrial effluent quality standards QCVN 01:2015-BMTTN (40 mg l
1 TN and 10 mg l
1 NHþ 4 -N). 3.3. Effect of DO DO concentration is a key factor in single-stage reactor such as OLAND, SNAP or SNAD process, which directly effects on population and activity of AOB, NOB, anammox and denitrifying bacteria. Indeed, the partial nitritation is mainly dependent on DO level that ensures to maintain NHþ 4 -N conversion rate of AOB and restricts NOB activity to avoid producing nitrate (Chang et al., 2013). Moreover, improper DO and NLR adjustments in single stage reactor may reduce nitrogen removal because of large amount of unconverted ammonium or excessive accumulation of nitrite that negatively effects on anammox bacteria in the inner layer of biofilm (Strous et al., 1999; Qiao et al., 2012). Fig. 6 presents variation of nitrogen compounds during the reacting phase with 7 h of aeration of batches running at different DO levels. Fig. 6 shows in the batches with DO levels of 0.4e0.8 mg l
1 and 0.2e0.4 mg l
1, NHþ 4N completely converted after 5 and 6 h, respectively. Nitrite and nitrate concentrations in both batches increased to 10e14 mg l
1 and 7 mg l
1, respectively at the batch end (hour 8th). This illustrates DO level above 0.2 mg l
1 was high enough for NOB growth and inhibited anammox bacteria. Whilst, in the batch at DO levels of 0.1e0.2 mg l
1, NHþ 4 -N fully converted after 6 h of aeration and
1
the obtained NO
and 3 -N and NO2 -N concentrations were 15 mg l
1 less than 0.2 mg l at hour 8th, respectively. Therefore, TN removal of batches at DO levels of 0.1e0.2 mg l
1 more improved as comparison to those with DO above 0.2 mg l
1. Similarly to the previous studies, under oxygen limiting condition, variation of the bulk DO concentration in small range (0.2 mg l
1) did not remarkably effected on the CANON process (Hao et al., 2002) and anammox bacteria can consume the nitrite generated from AOB, while NOB were hardly involved (Sliekers et al., 2002). 3.4. Nitrogen balance Analysis of nitrogen balance in the single reactor based on the

Table 3 Comparison of the performance of this study with that of other single-stage systems for nitrogen removal. Substrate

Sludge digester liquor Synthetic wastewater Synthetic wastewater Synthetic wastewater Synthetic wastewater Synthetic wastewater Synthetic wastewater Sludge digester liquor Synthetic wastewater Latex wastewater

Process

SNAP CANON CANON OLAND OLAND OLAND OLAND OLAND OLAND OLAND

Reactor regime

Biofilm SBR-biofilm Biofilm air-lift SBR-suspended growth SBR-suspended growth RBC-plug flow RBC- plug flow RBC- plug flow RBC-SBR RBC-SBR

NLR

ACR

Nitrogen removal

kgN m
3 day
1

%

kgN m
3 day
1

0.93 0.13 3.70 0.13 0.25 1.19 2.04 0.91 0.42 0.25

89 57 42 62 26 89 88 47 90 92

0.83 0.06 1.44 0.05 0.04 1.06 1.08 0.42 0.38 0.23

0.83 0.08 1.50 0.08 0.07 1.14 1.82 0.50 0.42 0.25

Reference

Qiao et al. (2010) Sliekers et al. (2002) Sliekers et al. (2003) Kuai and Verstraete (1998) Kuai and Verstraete (1998) Pynaert et al. (2003) Pynaert et al. (2004) Pynaert et al. (2004) This study

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Fig. 6. Profile of the bulk DO concentration in the single batches at DO of: (a) 0.4e0.8 mg l
1; (b) 0.2e0.4 mg l
1 and (c) 0.1e0.2 mg l
1.

results obtained from runs of the OLAND reactor with synthetic wastewater (Fig. 7a) and anaerobic latex processing wastewater (Fig. 7b). The nitrogen balance for the synthetic wastewater based on NHþ 4 -N removal obtained at ammonium loading rate of 0.42 kgN m
3 day
1 and DO of 0.4e0.8 mg l
1, whereas the balance for the anaerobic latex processing wastewater relied on the measured influent and effluent TN, COD, SS concentrations at ammonium loading rate of 0.26 kgN m
3 day
1 and DO of 0.1e0.2 mg l
1. Besides, results of the COD, nitrogen and SS balance was

determined based on the following values: (a) NHþ 4 -N:NO2 -N:NO3 N ratio of the anammox (1:1.32:0.26) (Strous et al., 1998); (b) NO
3N:bCOD ratio of the denitrification (1:1.74) (Lan et al., 2011), (c) Nitrogen content in the biomass (0.124 g N g
1 VS of bacterial cell) (Ekama, 1984), and (d) COD equivalent of biomass unit (1.42 gCOD gVS
1) (Tchobanoglous et al., 2014). Fig. 7a indicates that in the enrichment phase using synthetic wastewater, 77% of influent TN was removed by combination of the partial nitritation and anammox. Denitrifiers utilized NO
3 -N (6% of influent TN) produced from anammox process coupled with bCOD formed from cell decay in the reactor at long sludge retention time (above 80 days). 14% and 2% of TN were in the effluent TNOx (NO
2 -N þ NO
3 -N) and suspended solids, respectively. Fig. 7b presents that in the phase using the anaerobic latex processing effluent, 82% and 6% of TN removals were obtained by AOB coupled with anammox bacteria and denitrifiers, respectively. About 2% of TN was uptaken in the cells. 14% and 35% of feed sCOD were utilized by heterotrophic bacteria and denitrifiers, respectively. 51% of influent sCOD, that is mainly non-biodegradable organic matter, washed out in effluent. Similarly, Lan et al. (2011) reported SNAD process using synthetic wastewater using glucose had TN removal was 92%e96%, in which NO
3 -N removal of 7e9% was conducted by denitrifiers. The experiment using the anaerobic

latex processing wastewater that bCOD was available is similar to SNAD process, instead of OLAND for study using synthetic wastewater. In fact, the observation showed that anammox co-existed with heterotrophic bacteria in the presence of biodegradable COD in the latex processing wastewater. Jenni et al. (2014) and Lackner et al. (2014) also reported that co-existence of anammox and denitrification is available at high influent COD/N ratios and long Sludge Retention Time (SRT) in the single-stage reactor. 3.5. Biomass observation The flocs and biofilm were collected at steady state condition of the experiment using the anaerobic latex processing effluent on day 75th for analysis Metagenomics DNA analysis and maximum activity tests. The maximum activities of AOB, NOB, anammox bacteria and denitrifiers of flocs and biofilm are presented in Table 4. After 90 days of enrichment and 75 days of running with the real wastewater, TS contents of biofilm and bioflocs were not much different in the reactor. Table 4 shows the maximum activity of AOB in bioflocs was higher than that in biofilm, whereas, higher maximum activity of anammox bacteria was found in the biofilm. Thus, it is claimed that floc biomass plays in main role of partial nitritation, whilst biofilm biomass plays in key role of nitrogen removal by anammox. Visual observation indicates that the color of biofilm was brownish with many red granules, which is specified as anammox bacteria, while the color of flocs was also light brownish and less red spots. Besides, NOB and denitrifiers with low maximum activity were available in the flocs and biofilm. The fact that denitrifiers insignificantly contributed to nitrogen removal performance (<7%) that presented in the nitrogen balance (Fig. 7). Presence of NOB in the single reactor, which inhibited anammox

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N. Nhu Hien et al. / International Biodeterioration & Biodegradation xxx (2017) 1e11

Fig. 7. Nitrogen and COD balance for (a) enrichment using synthetic wastewater and (b) running with anaerobic latex processing wastewater.

bacteria growth by nitrite competition, may be due to long SRT and low initial ammonium concentration in this study. However, the DO limiting condition (0.1e0.2 mg l
1) resulted in low maximum NOB activity (5e7 mgN-NO-3 g
1 VS h
1) in comparison to that of A-O process (13e23 mgN-NO-3 g
1 VS h
1). The average effluent SS concentration during the enrichment and real wastewater run were 40 ± 12 mg l
1 (n ¼ 60) and 60 ± 17 mg l
1 (n ¼ 75), respectively (Fig. 8a and b). The effluent

suspended solid concentration was mainly attributed to washing out fine flocs in the reactor running at long SRT (by 85 days). Long SRT coupled with DO-limiting condition promoted presence of anammox bacteria in both bioflocs and biofilms (Pynaert et al., 2003). Table 3 illustrates that the maximum activity of anammox bacteria in this study was lower than those of some previous researches. This may be due to low initial ammonium (NHþ 4 -N) concentration in the batch reactor (around 80 mg l
1) using the latex

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N. Nhu Hien et al. / International Biodeterioration & Biodegradation xxx (2017) 1e11

9

Table 4 Maximum activities of AOB, NOB, anammox bacteria and denitrifiers and biomass concentration. Other studies

References

5.83 8.33

8.8; 18; 38; 33

14.2

32.1 13.3

13-23; 43-47

Van Dongen et al., 2001; Sliekers et al., 2002; Dapena-Mora et al., 2004. Gil et al., 2002; Jia et al., 2012.

7.08

5.00

6.25 4.58

0.42

1.25

5.42 7.92

0.51e1.6; 6e13; 3- Ekama, 1984; Gil et al., 2002; Bernat et al., 2003. 30 6.3; 7.5; 18-21 Van de Graaf et al., 1996; Strous et al., 1997.

Parameter

Unit

Synthetic wastewater

Maximum Anammox bacteria activity Maximum AOB activity

mgN-N2 gVS
1 h
1 0.42

12.1


1 mgN-NHþ 4 gVS h
1 mgN-NO-3 gVS
1 h
1 mgN-NO-3 gVS
1 h
1 mg TS l
1 e

33.8

Anaerobic latex processing wastewater

Flocs Biofilm Flocs Biofilm

Maximum NOB activity Maximum Denitrifiers activity Total dry weight VS/TS

3100 3498 0.625 0.63

3000 4700 0.63 0.67

Fig. 8. Time course of influent and effluent SS concentrations in (a) enrichment and (b) running with anaerobic latex processing wastewater.

Table 5 Microbial community analysis for mixture of biofilm and bioflocs in the OLAND reactor. OTU Taxonomy

# of Sequence RA (%) Accession

Similarity References

1

Flavobacteriaceae bacterium

1163

10.7

KJ195329

100%

2

Uncultured Deinococci bacterium (found in leachate sediment) Deinococcus-Thermus Nitrosomonas sp. B2 (AOB) Candidatus Kuenenia sp. (Anammox isolated from wastewater sludge for Biological nutrient removal) Proteobacterium E4-1 (denitrifying bacterium isolated from bioreactor for Tannery wastewater) Flavobacterium Uncultured Bacteroidetes bacterium clone Skagenf21 Beta-proteobacterium HS5/S24542 (Proteobacteria) Uncultured Actinobacteridae bacterium Acidisphaera (Proteobacteria) Others (<1% RA)

622

5.7

HQ183955 97%

Lee et al., 2011 Ngwa et al., 2013 Rainey et al., 1997

721

6.6

AB093545 98%

Matsuba et al., 2003

522 983

4.8 9.0

HM769655 99% AB823383 100%

Speth et al., 2012 Tse et al., 2014

2672

24.5

DQ640684 100%

Park and Lee, 2008

929 424 315

8.5 3.9 2.9

AY337603 100% KC018129 97% KM369919 97%

Croue et al., 2013 Adekambi et al., 2011 Hiraishi et al., 2000

2554

23.4

3 4 6 7 8 10 17 18

OTU: Operational Taxonomic Unit; RA: Relative abundance (%).

wastewater (Fig. 6c). Blackburne et al., 2008; Hendrickx et al., 2012 indicated that the influent ammonium concentration less than 100 mg l
1 was against anammox bacteria growth. In fact, maximum anammox bacteria activity of biofilm during the enrichment using synthetic wastewater containing the bulk initial
1 NHþ was higher than that 4 -N concentration of around 125 mg l

during running with the anaerobic latex processing wastewater. 3.6. Microbial community analysis Analysis of bacterial community by 16S ribosomal RNA using 16S V3 and V4 region presented that 10.9 clones with sequence of

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N. Nhu Hien et al. / International Biodeterioration & Biodegradation xxx (2017) 1e11

156 representatives. Anammox bacteria was dominant species in the mixture of biofilm and bioflocs (Relative abundance (RA) of 4.8% and similarity of 99% of sequence identities) in comparison with Candidatus Kuenenia sp. AOB species had RA of 6.6% and similarity of 98% of sequence identities, as comparison with Nitrosomonas sp. B2. Thus, Nitrosomonas and Candidatus Kuenenia were the key functional microorganisms responsible for nitrogen removal in the OLAND reactor. Besides, Proteobacterium E4-1 and Uncultured Bacteroidetes bacterium (Flavobacterium), denitrifiers, which were found (Table 5) in the OLAND reactor contributed to the removal of the remaining bCOD in the real anaerobic latex processing wastewater. 4. Conclusion This study applied OLAND process using synthetic wastewater for enrichment and then anaerobic latex processing effluent as feed wastewater. The enrichment completed for 49 days and obtained TN removal above 80% at NLR of 0.42 kg N m
3 day
1. The highest TN removal (94%) for the real wastewater achieved at DO ranging from 0.1 to 0.2 mg l
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