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1 저작자표시 2.0 대한민국 이용자는아래의조건을따르는경우에한하여자유롭게 이저작물을복제, 배포, 전송, 전시, 공연및방송할수있습니다. 이차적저작물을작성할수있습니다. 이저작물을영리목적으로이용할수있습니다. 다음과같은조건을따라야합니다 : 저작자표시. 귀하는원저작자를표시하여야합니다. 귀하는, 이저작물의재이용이나배포의경우, 이저작물에적용된이용허락조건을명확하게나타내어야합니다. 저작권자로부터별도의허가를받으면이러한조건들은적용되지않습니다. 저작권법에따른이용자의권리는위의내용에의하여영향을받지않습니다. 이것은이용허락규약 (Legal Code) 을이해하기쉽게요약한것입니다. Disclaimer

2 工學碩士學位請求論文 ANAMMOX 공정을이용한저농도질소폐수의 처리효율평가 Evaluation of Nitrogen Removal Efficiency for Low Strength Wastewater with ANAMMOX Process 2012年 2月 仁荷大學校大學院 環境工學科 郭源智

3 工學碩士學位請求論文 ANAMMOX 공정을이용한저농도질소폐수의 처리효율평가 Evaluation of Nitrogen Removal Efficiency for Low Strength Wastewater with ANAMMOX Process 2012年 2月 指導敎授裵在鎬 이論文을碩士學位論文으로提出함 仁荷大學校大學院 環境工學科 郭源智

4 이論文을郭源智의碩士學位論文으로認定함 2012年 2月 主審 印 副審 印 委員 印

5 ABSTRACT Complete anaerobic treatment for organic removal followed by autotrophic nitrogen removal offers a low-energy alternative for sewage treatment. In order to achieve efficient nitrogen removal by this process, a single-stage nitrogen removal biological filter (NRBF) via autotrophic pathway was developed. Effects of oxygen supply on the performance of the NRBF was evaluated with a synthetic organic-free wastewater containing 50 mg NH 3 -N/L at 25 o C. Dissolved oxygen (DO) supply to the reactor was controlled and limited in an external oxygen supply approach in order to promote nitrite formation and subsequent autotrophic conversion to N 2 via anaerobic ammonium oxidation (anammox). Maximal total nitrogen (TN) removal efficiencies under HRTs of 15, 8, 4, 1 h were 95±4, 88±7, 91±5, 73±5, and 80±2 %, respectively. A stoichiometric model was developed to describe the process performance and it confirms benchmark oxygen rate (BOR) is a vital control strategy to accomplish maximal ammonia conversion as well as maximal TN removal. Removals at oxygen supply rates lower than BOR were accompanied by no or less formation of nitrate, which contradicts reported stoichiometry for the process which involves nitrate formation. However, the stoichiometric model of oxygen consumption describing no nitrate production via autotrophic pathway was well-fit with the experimental oxygen supply data, signifying anammox might yield less or none nitrate as a product in a substrate limited condition. Microbial analyses using the polymerase chain reaction (PCR) confirmed that the ammonia oxidizing and anammox bacteria required for nitrogen removal were present. Candidatus Kuenenia stuttgartiensis and Candidatus Brocadia anammoxidans, were both present in the seed sludge, were found while the latter was dominant. i

6 요약문 하수와같은저농도폐수를혐기성으로처리한후잔류질소를독립영 양미생물을이용하여처리하는공정은저에너지하수처리대안이될 수있다. 본연구에서는독립영양경로를이용하는단일질소제거생 물학적여상 (nitrogen removal 질소농도가 biological filter, NRBF) 에암모니아성 50 mg/l인폐수를주입하며 25 o C에서산소공급량이 질소처리효율에미치는영향을평가하였다. 반응조의 DO(dissolved oxygen) 는외부산소공급장치를이용하여조절하였으며, 조절량은아 질산성질소생성및후속 anammox(anaerobic ammonium oxidation) 반응을통한 N 2 로전환에초점을맞추었다. NRBF 에서총질소제거율은수리학적체류시간 (HRT) 15, 8, 4, 1 시간 에서각각 95±4, 88±7, 91±5, 73±5, 그리고 80±2 % 이었다. 화학양론모 델을개발하여공정에적용한결과 BOR(benchmark oxygen rate) 이암 모니아및총질소제거효율을결정하는주요인자임을확인하였다. 산 소공급속도가 BOR 보다낮으면질산성질소생성량이적거나없었다. 공기공급량에따라질산성질소가생성되지않은실험결과는기존 anammox 반응의양론식과일치하지않지만본연구에서제시된양론 모델의결과와일치하여 anammox 공정이기질이제한조건에서는기 존에제시된양론식과는다르게일어나는것을확인하였다. PCR (polymerase chain reaction) 을분석한결과, 암모니아산화균과 anammox 균의존재를확인하였다. NRBF내 anammox 미생물균으로 는식종슬러지에존재하였던 Candidatus Kuenenia stuttgartiensis 과 Candidatus Brocadia anammoxidans이있었으며, 이중후자가우점종이었 다. ii

7 Contents Abstract ⅰ 요약문 ⅱ Contents ⅲ List of Tables ⅴ List of Figures ⅵ 1. Introduction 1 2. Literature Review Conventional nitrification denitrification Anaerobic ammonium oxidation Combined SHARON and ANAMMOX process CANON process 9 3. Material and Methods Reactor system and operational strategy Inoculum and synthetic wastewater Analytical Procedures Microbial Analysis Mass balance and rate equation Results and Discussion Reactor Performance HRT effect DO effect Thermodynamic aspect 27 iii

8 4.3 Oxygen supply control Microbial community analysis Discussion and Conclusions 38 References 41 iv

9 List of Tables Table 1. A comparison of the new processes of nitrogen removal and conventional nitrification/denitrification 10 Table 2. Stoichiometric equations of N-removal processes and their standard free energies at Table 3. Reactor performance as function of HRT 24 Table 4. Summary of reaction rates for the different operational periods 30 v

10 List of Figures Fig. 1 Metabolic Pathway for anammox bacteria 6 Fig. 2 Combined SHARON and ANAMMOX process 8 Fig. 3 Schematic diagram of autotrophic nitrogen removal filter 11 Fig. 4 Effect of the oxygen supply rate (OSR) to benchmark oxygen rate (BOR) ratio on ammonia and total nitrogen removal efficiencies 31 Fig. 5 PCR results of the original seeding with different primer sets 35 Fig. 6 PCR results at phases IV at HRT = 2 h, DO = mg/l with different primer sets 36 Fig. 7 PCR results at phases V samples at HRT = 2 h and DO= mg/l with different primer sets 37 vi

11 1. Introduction Complete anaerobic treatment of domestic wastewater with simultaneous energy recovery (in the form of methane) has proven to be a feasible net energy-producing approach rather than an energy-consuming one for wastewater treatment [1,2]. However, anaerobic treatment by itself can only treat carbonaceous compounds, and thus, lacks the ability to remove ammonia nitrogen. Thus, there is a need to treat nitrogen from anaerobically treated wastewater, because excessive nitrogen can be toxic to aquatic life, causing oxygen depletion and eutrophication in receiving waters. Even though nitrogen compounds in the wastewater can be removed by a variety of processes, biological nitrogen removal has been widely adopted. Conventionally biological nitrogen removal process is achieved by nitrification followed by denitrification. Nitrification carries out ammonia to nitrite and further oxidation to nitrate with oxygen as the electron acceptor, and then denitrification reduces nitrate to nitrogen gas using organic matter as carbon or energy source. It requires extensive energy for aeration to carry out nitrification, and an external carbon source for denitrification. A much more suitable and energy-efficient process for this purpose is autotrophic nitrogen removal, which couples nitritation of a portion of the ammonia to nitrite, which is then used for anaerobic oxidation of the remaining ammonia to N 2 via anaerobic ammonium oxidation (anammox). The merits of the process compared with conventional nitrification-denitrification are: (1) a 60 % reduction in energy consumption for aeration [3,4]; (2) no organics requirement for denitrification, which otherwise can be converted to methane for energy production [2]; (3) a 90 % reduction in sludge handling and transportation costs [5,6]. 1

12 Most previous studies of autotrophic nitrogen removal have emphasized the treatment of concentrated wastewaters [7,8]. but the potential for extending process application to dilute wastewaters as well has recently been emphasized [9]. Most recently, treated a low ammonia-containing synthetic wastewater in an oxygen limited autotrophic nitrification/denitrification (OLAND) rotating biological contactor (RBC) and obtained TN removal percentages at an 1 h HRT of 35±7 and 46±6 % at DO levels of 1.4 and 1.2 mg/l, respectively [6]. They indicated the limited nitrogen removal efficiencies were due to the unfavorable maintenance of lower DO for suppressing nitrite oxidizing bacteria (NOB) in the RBC reactor. The objective of this study is to develop a single-stage nitrogen removal biological filter (NRBF) via autotrophic pathway for nitrogen removal. Moreover NRBF is applied to dilute wastewater at short detention time and at ambient temperature. 2

13 2. Literature Review 2.1 Conventional nitrification/ denitrification Conventional biological nitrogen treatment requires a two-step process involving nitrification followed by denitrification. The conventional nitrogen removal includes autotrophic nitrification by chemolithoautotrophic bacteria to nitrite and further to nitrate with oxygen as the electron acceptor and heterotrophic denitrification by heterotrophic denitrifying bacteria using organic matter as carbon and energy source. The complete nitrification reaction which involves aerobic nitrification and nitrification with oxygen as the electron acceptor are shown as follows : (1) (2) The anoxic denitrification reduced the oxidized form of nitrogen - -, compounds, i.e. NO 3 or NO 2 to gaseous nitrogen, nitric oxide (NO), or nitrous oxide (N 2 O). Denitrification could be accomplished with a variety of electron donors, including methanol, acetate, ethanol, lactate and glucose [10]. The potential denitrification reaction are as follows: 3

14 (3) (4) Nitrification and denitrification require different operational conditions carried by different microorganisms. The nitrification reaction consumes 4.2 g of oxygen per gram of ammonia to nitrate [11], and denitrification requirement of organic carbon is significant. For example, 2.47 g of methanol is required of nitrate nitrogen for complete denitrification [12]. If the influent ratio of COD to N is too low, organic substrate should be added to achieve complete denitrification. In sum, the nitrification and denitrification is a cost-intensive process for oxygen demand of aeration and carbon source addition. There is, thus, a need to develop a more sustainable process for nitrogen removal. 4

15 2.2 Anaerobic ammonium oxidation The anaerobic ammonium oxidation (anammox) is a newly developed process for nitrogen removal. The process was first predicted based on thermodynamic calculations [13]. It was originally discovered in a denitrifying fluidized-bed reactor in 1995 [14]. It uses ammonia as the electron donor for oxidation by nitrite as the electron acceptor to produce nitrogen gas as the final end product [15]. The stoichiometry of anammox proposed by strous et al. [16] is presented in Equation 5. It could remove about 90 % of incoming nitrogen as ammonium and nitrite, and leaves 10 % of nitrogen as nitrate in the effluent. This process is considered to be a promising and sustainable process, because of no need for aeration and external carbon addition with its low biomass yield. (5) The anammox reaction could carry out by two identified bacteria "Brocadia anammoxidans" and "Kuenenia stuugartiensis" [16]. These two bacteria have a similar structure and produce hydrazine from exogenously supplied hydroxylamine. Figure 1 shows a possible metabolic pathway for anammox bacteria. Th e electron acceptor nitrite is converted to hydroxylamine and that hydroxylamine somehow reacts with the electron donor ammonium, leading to the ultimate production of dinitrogen gas [8]. Except for these two species, other anammox bacteria identified include Candidatus Kuenenia stuttgartiensis [17], Candidatus Scalindua brodae, Candidatus Scalindua wagneri [18], Candidatus Anammoxoglobus propionius [19], Candidatus Brocadia [20], and Candidatus Jettenia asiatica [21]. 5

16 Figure 1. Metabolic Pathway for anammox bacteria. HH: Hydrazine hydrolase; HZO: Hydrazine oxidizing enzyme; NR: Nitrite reducing enzyme The optimal anammox activity of a ph range between 7.0 and 8.5 and a temperature between 30 o C and 37 o C has been reported [22]. The process, thus, has been recognized as a good potential process for ammonium removal from sludge digestion supernatant. The anammox process combines with a preceding partial nitrification step, only about half part of ammonium needs to be nitrified to nitrite. The merits of the process include reducing oxygen demand in nitrification and eliminating organic supply. However, the longer start-up period is required to obtain a sufficient biomass concentration, since anammox bacteria doubling time is about 11 or 21 days [24], because anammox bacteria growth rate was per hour [8]. 6

17 2.3 Combined SHARON and ANAMMOX process The principle of the combined SHARON (Single reactor system for high ammonia removal over nitrite process) and anammox process (Figure 2) is that 50 % of containing ammonium from wastewater is oxidized in the SHARON reactor to nitrite by controlling solid retention time (SRT), since ammonium oxidizing bacteria (AOB) grow faster than nitrite oxidizing bacteria (NOB) at higher or equal to mesophilic temperature. Thus, it fits to treat reject waters from anaerobic digestors. The SHARON reaction is presented as follow : (6) The effluent of SHARON reactor containing equal amount of ammonium and nitrite as the influent for the anammox process form Equation 1 (partial nitrification) and 5 (anammox). The SHARON-ANAMMOX process could greatly improve nitrogen wastewater management cost-effectively [24], because the combined process dose not required COD (chemical oxygen demand) resulting in no need of the required influent ratio between COD and N (nitrogen) in the conventional nitrogen removal process [18]. The combined system save 60 % on required oxygen compared to nitrification/denitrification. Overall, the combined process is 90 % less expensive than the conventional nitrogen removal processes [25]. 7

18 Figure 2. Combined SHARON and ANAMMOX process 8

19 2.4 CANON process The CANON (completely autotrophic nitrogen removal over nitrite) process is a single-stage autotrophic nitrogen removal system. It can be carried out in a single reactor under oxygen-limited condition by incorporating partial nitrification and anoxic oxidation of ammonia. The process interaction between the two groups of autotrophic microorganisms such as Nitrosomonas, an aerobic bacterium, and Planctomycete, an anammox bacteria, under oxygen limited conditions [26]. These two group autotrophic microorganisms sequentially react simultaneously. The combination of the two reactions for nitrogen removal is shown as follows: (7) A DO concentration of up to 0.5 mg/l has no effect on ammonia oxidation, but nitrite oxidation is strongly inhibited in suspended growth reactors [27]. So the combined process can occur under oxygen-limited condition. The CANON process is completely autotrophic and requires no added COD. In addition, nitrogen removal can be achieved in a single reactor with oxygen limited condition. This greatly reduces the space and energy requirements. The autotrophic process consumes 60 % less oxygen and 100 % less reducing agents, organics, than the conventional nitrogen removal process [28]. 9

20 Table 1. A comparison of the new processes of nitrogen removal and conventional nitrification/ denitrification [23] Nitrification System SHARON ANAMMOX CANON /denitrification Reactors Feed wastewater wastewater NH 4 + +NO 2 - wastewater Discharge NO 2 -, NO 3 -, N 2 NH 4 +, NO 2 - NO 3 -, N 2 NO 3 -, N 2 Condition oxic, anoxic oxic anoxic oxygen limited Oxygen requirement high low none low COD requirement yes none none none Sludge production high low low low Table 1 represents the comparative performance of various processes [23]. Nitrification/denitrification requires high oxygen and organic carbon, however, the SHARON, ANAMMOX, CANON processes offer various advantages such as less oxygen and no need for organic carbon. So it saves costs for energy 10

21 3. Material and Methods 3.1 Reactor system and operational strategy Figure 3. Schematic diagram of autotrophic nitrogen removal filter Figure 3 is a schematic diagram of the autotrophic nitrogen removal system used in this study. It consisted of a nitrogen-removal biological filter (NRBF) and an external aeration cell with effective volumes of 0.38 and 0.05 L, respectively. The NRBF and aeration cell were fabricated with internal diameters of 4 and 2.5 cm and heights of 34 11

22 and 19 cm, respectively. For biological attachment and growth, the NRBF contained 44 pieces of 1.2 cm by 1.5 cm Siporax plastic media (Sera Co., Germany). The plastic media were stacked from the bottom up to 18 cm height inside the NRBF. DO and ph probes (Thermo Fisher Scientific, Waltham, MA, USA) were installed at 11 cm height from the bottom point in the NRBF to monitor the DO and ph of the biological treatment system. The NRBF was operated in an up-flow mode. The aeration cell was placed within an effluent to influent recirculation line, and was equipped with a diffuser for air sparging to add near-saturation concentrations of oxygen into the recirculated water prior to mixing with influent wastewater. DO added to the recirculating water was determined with a DO probe (Thermo Fisher Scientific, Waltham, MA, USA) inserted periodically into the aeration cell. A peristaltic pump (Masterflex, Model No , USA) was used for water recirculation. The influent reactor feed was flushed with nitrogen gas to reduce influent DO in the feed stream, and the influent tank was sealed to maintain anaerobic conditions. By manually measuring and controlling the respective influent and recirculation flow rates, as well as the DO added to the recirculating water, the mass flow rate of DO could be precisely controlled to match the influent ammonia concentration as desired. With this approach the reactor could be maintained aerobic near the bottom inlet of the NRBF for partial ammonia oxidation, while becoming anoxic in the upper portion as necessary for the anammox process to function. Temperature of operation was maintained at 25 o C in a temperature-controlled laboratory. The reactor hydraulic retention time (HRT) was decreased step-wise from 15 to 1 h 12

23 in five steps, while maintaining operation at each step until quasi-steady-state conditions were reached. 13

24 3.2 Inoculum and synthetic wastewater The NRBF was inoculated with 170 ml of activated sludge (4000 mg/l mixed liquor suspended solids) from Bucheon sewage treatment facility, South Korea, plus 200 ml of an anammox-organism-containing culture (2500 mg MLSS/L) from a 3.35 L anaerobic bioreactor treating a synthetic wastewater with a nitrogen loading of 2.5 kg/m 3 d at 35 o C. Using tap water, each liter of synthetic wastewater feed contained g (NH 4 ) 2 SO 4, g KH 2 PO 4, 0.3 g CaCl 2 2H2O, 0.2 g MgSO 4 7H 2 O, and 1 ml each of trace element solutionsⅠand Ⅱ. Each liter of trace elements solution I contained 5 g EDTA and 5 g FeSO 4 and of trace elements solution II contained 15 g EDTA, 0.43 g ZnSO 4 7H2O, 0.24 g CoCl 2 6H2O, 0.99 g MnCl 2 4H2O, 0.25 g CuSO 4 5H2O, 0.22 g NaMoO 4 2H 0.14 g H 3 BO 4 [31]. 2O, 0.19 g NiCl 2 6H2O, 0.21 g NaSeO 4 10H2O, and 14

25 3.3 Analytical Procedures Influent and effluent samples were collected periodically for analyses. To determine ammonia, nitrite, and nitrate concentrations, all influent and effluent samples were filtered through a 0.20 μm filter (PVDF syringe, Whatman, Springfield Mill, UK) before analysis. Ammonia was measured by an ion-selective electrode (Thermo Fisher Scientific, Waltham, MA, USA) according to Standard Methods [30]. Nitrite and nitrate were analyzed with an ion-chromatograph (DX 500, Dionex, Sunnyvale, CA, USA) equipped with a column (AllsepTM Anion IC, Deerfield, IL, USA) and a conductivity detector (CD20, Dionex, Sunnyvale, CA, USA). The ph and DO concentrations were determined using ph and DO electrodes (Thermo Fisher Scientific, Waltham, MA, USA). 15

26 3.4 Microbial Analysis The presences of ammonia-oxidizing bacteria (AOB), nitrite-oxidizing bacteria (NOB), denitrifiers and anammox bacteria in the inoculum and NRMF were determined using appropriate primers and the polymerase chain reaction (PCR). For this, the total genomic DNA of sample was extracted by using an UltraClean Microbial DNA isolation kit (MO BIO Laboratories, CA, USA). The DNA concentration was determined on a photometer ASP-3700 (ACTGene, NJ, USA). PCR was then performed in a 96 well Gradient Palm-Cycler (Corbett Research Pty Ltd, Austria). The primers sets used in this study were 11F and 1512R for all bacteria [31], amoa-1f and amoa-2r for AOB [32], nirs-1f and nirs-6r for NOB [33], cnorb-2f and cnorb-6r for denitrifiers [34], Brod541F [35] and Amx820R [19] for all anammox bacteria. For individual anammox bacteria, the primer sets were AnnirS379F and AnnirS821R for Kuenenia stuttgartiensis (KS) and Candidatus Scalindua genus [36], KS-qF3 and KS-qR3 for KS [37], and BAqF and BAqR for Brocadia anammoxidans (BA) [37]. Each reaction was performed in a 25 μl volume containing 1 μl of DNA template (average 40 ng), 1 μl of each primer (10 μm), 9.5 μl of sterilized water and 12.5 μl of 2X Taq PCR Master Mix (Genomics BioSd & Tech, Taiwan). The cycling parameters were 3 min at 95 C and 35 cycles of 30s at 95 C, 30s at 57 C for 11f/1512r and CTO189fA/B+CTO189fC (2:1 ratio)/cto654r, or 53 C for amoa-1f/amoa-2r and Brod541F/ Amx820R, or 51 C for nirs-1f/nirs-6r, cnorb-2f/cnorb-6r and AnnirS379F/AnnirS821R and 1 min at 72 C, with finally 5 min at 72 C. Results of PCR were checked by agarose gel electrophoreses. 16

27 3.5 Mass balance and rate equations The four basic energy reactions involved in autotrophic nitrogen removal are summarized in Table 2. Reaction I represents the autotrophic oxidation of ammonia to nitrite (nitritation) by AOB. Reaction III represents the anaerobic autotrophic oxidation of ammonia with nitrite by anammox microorganisms. Reaction IV represents the overall autotrophic nitrogen removal process, which is a combination of Reactions I and III. Reaction II represents the complete autotrophic oxidation of ammonia to nitrate, an undesired overall competing reaction carried out by AOB and NOB. Some nitrate might also be formed by anammox organisms in conjunction with the reduction of carbon dioxide to cellular organic carbon in a biological synthesis reaction [38]. 17

28 Table 2. Stoichiometric equations of N-removal processes and their standard free energies at 25 Reaction Reaction No. Ⅰ (donor/acceptor) Nitritation (ammonium/oxygen) Stoichiometric equation Free energy (ΔG o,kj/mol) NH O 2 NO 2 - +H 2 O+2H Ⅱ Ⅲ Ⅳ Ⅴ Ⅵ Ⅶ Nitrification (ammonium/oxygen) Anammox without nitrate production (ammonium/nitrite) Nitritation and anammox without nitrate production (ammonium/oxygen) Nitriatation (nitrite/oxygen) Anammox with nitrate production (ammonium/nitrite) Nitriation and anammox with nitrate production (ammonium/oxygen) NH O 2 NO 3 - +H 2 O+2H NH 4 + +NO 2 - N 2 +H 2 O NH O 2 0.5N 2 +H H 2 O NO O 2 NO NH NO N 2 +NO NH O N NO H H 2 O

29 The four Table 2 reactions were used to develop dissolved oxygen (DO) and nitrogen transformation mass balance rate equations for the reactor. A key assumption is that the reactor is operating at quasi-steady-state conditions. The oxygen supply rate (OSR, mg O 2 /d) to the NRBF was then determined as follows: (8) where DO r is the DO concentration in the recycle stream (mg/l), and Q r is the recycle flow rate from the aeration cell into the biological filter (L/d). The oxygen consumption rate (OCR, mg O 2 /d) is used to quantify oxygen consumption and was estimated as follows from the influent and effluent concentrations of ammonia, nitrite, nitrate based upon the stoichiometric equations presented in Table 2: (9) where Q i is the influent flow rate (L/d), NH 3, NO - - 2, and NO 3 (mg N/L) represent the ammonia, nitrite, and nitrate concentrations, respectively; the subscripts i and e represent influent and effluent stream concentrations, respectively; and the ratio of 32/14 represents the ratio of the formula weights for O 2 and N. The coefficients 0.75, 0.75, and 1.25 were derived from Table 2 equations and represent the 19

30 moles of oxygen per mole of ammonia nitrogen for oxidation of ammonia to N 2 (Reaction IV), for the further oxidation of ammonia to nitrite (difference between Reactions Ⅰ and IV), and for the further oxidation of ammonia to nitrate (difference between Reactions Ⅱand IV), respectively. Equation 2 is an empirical equation based upon the assumption that ammonia is removed only through conversion to N 2, NO - 2, or NO - 3. A comparison between OSR and OCR should provide some measure of how well this assumption may hold in an operating system, and thus the usefulness of using the OSR as a system control parameter to achieve optimum nitrogen removal. If a wastewater contains other potential electron donors such as organics or sulfide, the calculated OCR might be lower than OSR as such donors could result in additional oxygen consumption or a decrease in nitrate concentration through denitrification. No such reducing compounds were contained in the synthetic wastewater used for this study, and so sulfide oxidation and denitrification should not be significant factors here. Nitrogen transformation to N 2 O or other more oxidized species than N 2 would also produce a ratio of OCR to OSR lower than 1. Conversion of ammonia to organic nitrogen through biosynthesis would cause the ratio to be higher than 1. Analytical or other experimental measurement errors could cause the ratio to be either greater or less than 1. For comparison between the oxygen supply rate and nitrogen removal efficiencies, a benchmark oxygenation rate (BOR, mg O 2 /d) is defined to represent the oxygen requirement associated only for autotrophic 20

31 nitrogen removal to N 2 as governed by Reaction IV: (10) Of particular interest to this study was an evaluation of ammonia and TN removal efficiencies as a function of the OSR/BOR ratio under different reactor operating conditions. This comparison together with an evaluation of the match between OSR and OCR should indicate whether BOR might serve as a control parameter to achieve optimal ammonia conversion as well as optimal overall TN removal efficiencies in a single-stage autotrophic nitrogen removal system such as the NRBF. 21

32 4. Results and Discussion 4.1 Reactor Performance HRT effect During startup, mixing of the influent flow with recirculated DO-containing water was controlled in order to maintain adequate DO near the reactor inlet to achieve ammonia oxidation to nitrite, but not in the upper portion of the reactor where the desired autotrophic ammonia oxidation was to take place. In order to do this, the DO in the upper portion was maintained at no higher than 0.1 to 0.3 mg/l by controlling the recirculation rate, and slowly increasing this rate as DO conditions allowed. With this approach quasi-steady-state conditions were reached within about 21 days. Table 3 summarizes the performance of the one-stage autotrophic nitrogen removal filter at various conditions. TN removal efficiencies at this and subsequent steady-state periods at DO of 0.1 mg/l were 95±4, 88±7, 91±5, and 73±7 % for HRTs of 15, 8, 4, and 1 h, respectively. This corresponding nitrogen removal rate (NRR) achieved was up to 890 mg N/Ld at a nitrogen loading rate of 1219 mg N/ Ld at 1 h HRT. Meanwhile, ammonium, nitrite and nitrate concentrations of the effluent in the operation period ranging from HRTs of 15 to 1 h at DO of 0.1 mg/l were less than 12.7±4.0, not detectable, and less than 2.6±2.5 mg N/L, respectively, which indicates the dominate nitrogen compound was in the form of ammonium at 22

33 DO of 0.1 mg/l. The observation clearly demonstrates that nitritation and anammox reactions were prevailing and nitratation was inhibited during the operation period of DO level of 0.1 mg/l, regardless of the varied HRTs. The used filter set-up did not allow to well-mix in the reactor, and, accordingly, resulted in smaller decrease of TN efficiency with HRT decrease. Though, the stable as the performance of the one-stage autotrophic nitrogen removal filter was less affected by the HRT, indicating other factors such as the OSR may be of more importance. 23

34 Table 3. Reactor performance as function of HRT Phase Ⅰ Ⅱ Ⅲ Ⅳ Ⅴ Ⅵ Ⅶ HRT (h) Duration (d) Number of samples Q i(l/d) Q r(l/d) NRBF DO Recycle DO 8.0± ± ± ± ± ± ±0.4 ph 7.6± ± ± ± ± ± ±0.2 Influent NH 3-N 51±2 51±2 48±9 48±1 50±2 51±2 48±1 Effluent NH 3-N 3±2 6±4 2±1 3±2 7±2 13±4 1±1 Effluent NO - 2 -N ND ND ND ND ND ND ND Effluent NO - 3 -N ND 0±1 3±3 10±2 12±1 1±1 10±1 TN removal 95±4 88±7 91±5 73±5 62±3 73±7 80±2 (%) NH 3-N removal 95±4 88±7 97±3 95±4 86±3 75±8 99±1 (%) NLR (mgn/l d) NRR (mgn/l d) NO 3formed/ NH 3removed (%) 0±0 1±1 6±4 23±3 27±4 2±2 20±2 * Unit is mg/l, if not specified. Dissolved Oxygen (DO); Influent flow rate (Q i); Recycle flow rate from the DO supply stream (Q r); Not detectable (ND): the detection limit is under 1 mg N/L; Nitrogen loading rate (NLR); Nitrogen removal rate (NRR) 24

35 4.1.2 DO effect Higher DO levels of 0.1 to 0.2 and 0.2 to 0.3 mg/l during the phases of Ⅳ, Ⅴand Ⅶ were evaluated their effectiveness at relative short HRTs of 2 and 1 h (Table 3). Phases of Ⅳ and Ⅶ With DO concentration of mg/l, TN removal efficiencies at HRTs of 2 (phase Ⅳ) and 1 h (phase Ⅶ) were 73±5 and 80±2 %, respectively. However, at HRT of 2 h with DO concentration of mg/l (phase Ⅴ), TN removal efficiency declined to 62±3 %. Interesting to be noted, nitrate concentrations from the effluents stayed stable in the range of 10±2 to 12±1 mg N/L regardless of the DO level range of 0.1 to 0.3 mg/l in these three phases. However, ammonia concentrations of the effluents in the DO dosage ranging from 0.1 to 0.2 mg/l were approximately in lower levels (3±2 and 1±1 mg N/L), while the one in the DO concentration of mg/l HRT were 7±2 mg N/L. The dominant effluent nitrogen compound at a higher DO level switched to nitrate, instead of ammonium which was overriding at a lower DO level of 0.1 mg/l (phases Ⅰ, Ⅱ, Ⅲ and Ⅵ). The results clearly exhibit a higher DO level of mg/l increases NOB activity, indicating NOB could be cable of competing oxygen with AOB and nitrite with anammox bacteria resulting in declining TN treatment performance. Similar discovery was also reported by De Clippeleir et al. [6] that TN removal performance via the autotrophic pathway increased 11 % by reducing DO level of 1.4 to 1.2 mg/l at HRT of 1 h. As a result, for optimization the treatment efficiency in the autotrophic nitrogen removal system, oxygen supply rate is a key feature which will be discussed more in the results of the mass balance and rate equations. 25

36 The ratio of ammonia consumption to nitrate production, 10 %, is a pivotal parameter of the stable assessment of anammox, since anammox treats only 90 % of the incoming nitrogen as ammonia/nitrite and leaves 10 % of the effluent nitrogen as nitrate based on the empirical stoichiometry of anammox (Equation 5) without active NOB metabolic involvement [38]. In this present study, less or even none nitrate formation was observed Table 2 which contradicts reported stoichiometric 10 % nitrate nitrogen production from influent ammonium/nitrite nitrogen. The ratios at HRTs of 15, 8, 4 and 1 h in the limited DO situation of 0.1 mg/l were 0, 1, 6, and 2 %, respectively (Table 3). This leads to a hypothesis that anammox may adapt Reaction Ⅲ (Table 2) completely using ammonium as the electron donor and nitrite as the electron acceptor, which is similar to AOB. However, the concept is needed to be studied further in the near future. 26

37 4.2 Thermodynamic aspect A thermodynamic evaluation was made to overlook the results of less stoichiometric nitrate production in our observations, which is different from the well-reported empirical anammox stoichiometry by Strous et al. [38]. Table 2 lists the seven energy reactions associated with ammonia oxidation to nitrite and ultimate conversion of ammonia and nitrite to nitrogen along with their Gibbs standard free energy values at 25 o C. Reaction Ⅱ represents the combined Reaction Ⅰand Ⅴ of ammonia oxidation to nitrite via nitriation and further oxidization to nitrate via nitratation, while Reaction Ⅲ and Ⅵ represent the anammox reactions without and with nitrite production, respectively. Assume that Reaction Ⅴ (nitrite oxidation) could not occur by the selection pressure of a low DO dosage in the NRBF so that anammox and nitritation reactions could carry out without any substrate competition by NOB from Reaction Ⅴ. Anammox reactions carrying either by Reaction Ⅲ or Ⅵ could proceed spontaneously, since their ΔG o values are negative. Even though the ΔG o value of anammox reaction of Reaction Ⅵ with nitrate production is lower than that of Reaction Ⅲ without nitrate production, Reaction Ⅵ requires a higher nitrite stoichiometric coefficient as the electron acceptor. Yet, in the limited substrate (such as the electron acceptor: nitrite) condition from this study, the produced nitrite by AOB with NOB inhibition via the selection pressure of a lower DO environment may be consumed immediately by anammox bacteria via Reaction Ⅲ, instead of Reaction Ⅵ. Similar concept of another limited substrate (the electron acceptor: 27

38 oxygen) condition in the combined nitritation and anammox reaction could also explain the occurrence of the anammox reaction without nitrate production in the effluent. Reaction Ⅳ and represent the combined nitritation and anammox reaction without and with nitrate production, respectively. Reaction Ⅳ is performed by combing Reaction Ⅰ and Ⅲ per mole of ammonia as the electron donor, while Reaction Ⅶ is performed by combing the Reaction Ⅰ, Ⅲ and Ⅵ based on the 10 % of the incoming nitrogen leaving as the form of nitrate in the effluent from Strous et al. [38]. The ΔG o values of both reactions are somewhat similar, while Reaction Ⅳ without nitrate production obliges less oxygen stoichiometric coefficient, which fits for the experimental condition in this study. This demonstrates a lower or no nitrate production of an anammox reaction compared with the well-implemented anammox stoichiometry (Equation 10) by Strous et al. [38] is capable of proceeding based on thermodynamics. In consequence, this less nitrate production pathway of anammox found in this study provides a better alternative outcome of nitrogen removal treating the relatively-dilute ammonia-containing effluent from anaerobic sewage treatment, since it completely converts all of the incoming nitrogen (ammonia/nitrite) into dinitrogen gas. Improving TN efficiency with more energy savings by the newly founded anammox stoichiometry is, therefore, expected resulting from less nitrate stoichiometric production rate and less oxygen demand. Ⅶ 28

39 4.3 Oxygen supply control Table 4 indicates that the ratios of OCR to OSR varied between 0.99 and 1.07 with an average of This close agreement between the two suggests that reactions other than those listed in Table 2 were not dominant in the NRBF. The slight average above 1.00 might be associated with use of some ammonia in biological synthesis, which would be expected, but the range of values obtained is within normal analytical and experimental errors so that firm conclusions even here would be difficult to make. In any event, the computed rates of supply and consumption of oxygen are quite close and confirm that Table 2 reactions were the dominant reactions in this NRFB, as also suggested by the microbial findings. Ammonia and TN removal percentages were found not to be correlated with HRT, but could be correlated with the OSR/BOR ratio as illustrated in Figure 4. This figure includes Table 4 results for all of the HRTs studied. Of significant interest is that the maximum TN removal efficiency was achieved when the OSR/BOR ratio was close to 1.0. The importance of controlling OSR near BOR was not evident until the completion of this study when all of data were available for evaluation. Nevertheless, the combined set of data confirms that, regardless of the HRT of operation, an OSR/BOR ratio either much greater or much less than 1.0 leads to a TN removal efficiency below the maximum value. With an OSR/BOR ratio less than 1.0, the removal efficiencies for ammonia and TN were essentially the same, both decreasing in direct relationship with a decrease in the ratio. Here, ammonia was the dominant effluent nitrogen compound. With 29

40 an OSR/BOR ratio greater than 1.0, the ammonia removal efficiency remained quite high, but with increasing conversion to nitrate rather than to N 2. The oxygen supply was then in surplus, resulting in nitrate then being the dominant effluent nitrogen compound. Table 4. Summary of reaction rates for the different operational periods Phases Ⅰ Ⅱ Ⅲ Ⅳ Ⅴ Ⅵ Ⅶ HRT (h) r ammonia : NH 3 -N removal rate (mg/d) r nitrite: NO - 2 -N production rate (mg/d) r nitrate : NO - 3 -N production rate (mg/d) OSR (mg/d) OCR (mg/d) BOR (mg/d) OCR/OSR OSR/BOR Oxygen supply rate (OSR); Oxygen utilization rate (OUR); Benchmark oxygen rate (BOR) 30

41 Figure 4. Effect of the oxygen supply rate (OSR) to benchmark oxygen rate (BOR) ratio on ammonia and total nitrogen removal efficiencies The above findings are illustrated through a comparison of the two quasi-steady-state operating conditions evaluated with an HRT of 1 h, one with an OSR/BOR ratio of 0.78 (Phase VI) and the other at 1.26 (Phase V), about 25 % too low in the first case and 25 % too high in the second. With a ratio of 0.78, ammonia and total nitrogen removal were about the same, 75 and 73 %. At the higher 1.26 ratio, ammonia removal was very high at 99 % respectively, but significant nitrate was formed, causing TN removal to be only 80 %. While the optimum setting for OSR had not been used for the lowest HRT of 1 h, it had been for the 4 h HRT (Phase III). For the later, 97 % ammonia removal and 91 % total N removal was achieved, indicating the high efficiencies of nitrogen removal that can be obtained with dilute wastewater with proper setting of the oxygen supply rate. These 31

42 results indicate the sensitivity removal efficiency has to the OSR/BOR ratio and the importance of control of this ratio near to

43 4.4 Microbial community analysis A microbial community analysis was conducted to determine the possible presence of anammox organisms as well as AOB, NOB, and denitrifiers in the NRBF. The mixed seed culture and samples collected from four different heights in the NRBF during phases IV and V (Table 3) were used for PCR analysis. Results using primers for AOB, NOB, denitrifiers, and anammox bacteria indicated all were present in the seed culture (Figure 5). The possible presence of given anammox species was of particular interest for this study, the targets here being three well known species of anammox bacteria: Candidatus Scalindu gender, Candidatus Kuenenia stuttgartiensis (KS), and Candidatus Brocadia anammoxidans (BA). For the seed culture the positive responses with primers KS-qF3 and KS-qR3 for KS, primers BAqF and BAqR for BA, and AnnirS379F and AnnirS821R for KS/Candidatus Scalindua genus confirmed the presence of KS and BA and perhaps Candidatus Scalindua genus as well, although the latter probes were not specific for this particular genus (Figure 5). Culture samples were collected during phases IV and V from the four NRBF ports illustrated in Figure 3. AOB, NOB, and anammox bacteria were found present in all samples. Conversely, denitrifying bacteria were not detected using the cnorb based primers, suggesting denitrification was not a prevalent reaction in the NRBF as expected since no organics were present in the influent feed (Figure 6a and 7a). As for anammox organisms, the negative response to the AnnirS primers for KS and Candidatus Scalindua in all reactor samples in these two phases indicated these organisms were not the dominant anammox 33

44 species present (Figure 6b and Figure 7b). However, there were clear signs for the presence of BA in all NRBF samples, indicating its preferential dominance over KS under reactor conditions with the low substrate feed ammonia concentration and the oxygen limited conditions. 34

45 Figure 5. PCR results of the original seeding with different primer sets 35

46 (a) (b) Figure 6. PCR results at phases IV at HRT = 2 h, DO = mg/l with different primer sets (a) amoa, nirs, and cnorb; (b) TA abd AnnirS 36

47 (a) (b) Figure 7. PCR results at phases V samples at HRT = 2 h and DO = mg/ L with different primer sets (a) amoa, nirs, cnorb and TA; (b) BA and KS 37

48 5. Discussion and Conclusion The results of this study demonstrate that efficient total nitrogen removal with dilute wastewaters can be achieved in a single-stage reactor through control of the dissolved oxygen supply rate to the reactor. The optimal removal of both ammonia and total nitrogen was found to occur when the OSR just equaled BOR, that is when 0.75 mol O 2 was supplied as DO for each mole of ammonia nitrogen in the feed stream. This conclusion appears to hold for the 50 mg/l ammonia nitrogen concentration in the feed, whether the NRBF was operating at a 15 h HRT or at the more preferable 1 h HRT. A most unexpected result of this study was the near complete absence of nitrate formation with autotrophic nitrogen removal with OSR/BOR less than 1.0. From a mass-balance experimental study of the anammox reaction, Strous et al. [38] reported that nitrate was a general product of the reaction and resulted because some nitrite was used as a reductant for biomass formation from carbon dioxide. Based upon previous stoichiometric findings, Third et al. [28] calculated that the nitrate formed through the overall anammox process would equal at least 13% of the ammonia removed. In their reactor studies, they found nitrate formation to be in general agreement with this expectation. This appears typical of what others have found. Such reports suggest that because of such nitrate formation, total nitrogen removal with the anammox process alone cannot be higher than 87 %, and probably much lower with less than 100 % ammonia conversion. However, we have found that with close oxygen supply control, nitrate formation can be eliminated and TN removals higher than 90 % can 38

49 be achieved. It is not clear why nitrate formation was not found in our study when the OSR/BOR was maintained below 1.0, perhaps some anammox organisms can use ammonia rather than nitrite as a reductant for formation of cell carbon from carbon dioxide just as AOB can. Another hypothesis is that nitrate that may have been formed was removed through denitrification. The experimental results do not support this hypothesis. No organic or other reduced compounds were present in the influent to support denitrification. No denitrifiers were found with the molecular probes. In addition, the OCR/BOR ratio tended to be slightly greater than 1.0 rather than less than 1.0, which supports a hypothesis that ammonia was the reductant for cell carbon formation rather than nitrite. In any event, our experimental results are consistent with a conclusion that the anammox reaction can proceed in some cases without nitrate formation as long as the oxygen supply rate is maintained at or below the BOR. The advantage of the reactor system that we used with an external aeration cell is that this allows rather precise control of oxygen supply to the reactor as necessary for efficient nitrogen removal. A potential operational concern with this approach is the high recycle rate required to supply DO using this approach. The use of pure oxygen rather than air in the external aeration cell would result in a higher DO content in the recycled water, which would reduce recycle requirements by a factor of 4 to 5. Another current concern for direct application of the NRMR to remove nitrogen from an anaerobically treated wastewater effluent is the likely demand for oxygen for oxidation of remaining organics, including dissolved methane and inorganics such as sulfide. 39

50 These issues may be handled using different possible approaches. For example, both dissolved methane and sulfide might be gas stripped from the supply stream before passing to the NRBF. In another possible approach, dissolved methane, which is a poorly soluble gas, could be gas stripped and the remaining solution sulfide might then be oxidized to sulfur either in a separate reactor or simultaneously in the same reactor as used from autotrophic nitrogen removal. Further studies to evaluate these and other possible approaches would be beneficial. 40

51 References [1] Kim, J., Kim, K., Ye, H., Lee, E., Shin, C., McCarty, P. L., Bae, J. Anaerobic fluidized bed membrane bioreactor for wastewater treatment. Environ. Sci. Technol., 2011, 45 (2), [2] McCarty, P. L.; Bae, J., Kim, J. Domestic wastewater treatment as a net energy producer can-this be achieved?. Environ. Sci. Technol., 2011, 45 (17), [3] Van Dongen, U., Jetten, M.S.M., Van Loosdrecht, M.C.M. The SHARON Anammox process for treatment of ammonium rich wastewater. Wat. Sci. Tech., 2001, 44 (1), [4] Siegrist, H., Salzgeber, D., Eugster, J., Joss, A. Anammox brings WWTP closer to energy autarky due to increased biogas production and reduced aeration energy for N-removal. Wat. Sci. Tech., 2008, 57 (3), [5] Mulder, A. The quest for sustainable nitrogen removal technologies. Wat. Sci Technol., 2003, 48 (1), [6] De Clippeleir, H., Yan, X., Verstraete, W., Vlaeminck, S. E. OLAND is feasible to treat sewage-like nitrogen concentrations at low hydraulic residence times. Appl. Microbiol. Biotechnol., 2011, 90 (4), [7] Kuenen, J. G. Anammox bacteria: from discovery to application. Nat. Rev. Microbiol., 2008, 6 (4), [8] Jetten, M.S.M., Wagner, M., Fuerst, J., van Loosdrecht, M., Kuenen, G., Strous, M. Microbiology and application of the anaerobic ammonium oxidation (anammox) process. Curr. Opi. Biotechnol., 2001, 12 (3), [9] Kartal, B., Kuenen, J. G., van Loosdrecht, M. C. M. Sewage Treatment with Anammox. Science., 2010, 328 (5979), [10]Grabinska-Loniewska, A. Denitrification unit biocenosis. Water Res., 1991, 25, [11]Gujer, W., Jenkins, D., The contact stabilization process-oxygen and 41

52 nitrogen mass balances. University of California, Berkeley, Sanitary Engineering Research Laboratory Report., 1974, [12]McCarty, P. L., Beck, L., St Amant, P. Biological denitrification of wastewaters by addition of organic materials. Proc 24th Industrial Waste Conference, West Lafayette, IN, USA, 1969, [13]Broda, E. Two kinds of lithotrophs missing in nature. Zeitschrift für allgemeine Mikrobiologie., 1977, 17 (6), [14]Mulder, A., Vandegraaf, A. A., Robertson, L. A. and Kuenen, J. G. Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. Fems Microbiology Ecology., 1955, 16 (3), [15]Goreau, T.J., Kaplan, W. A,, Wofsy, S. C., McElroy, M. B., Valois, F.W., Watson, S.W. Production of NO 2 and N 2 O by nitrifying bacteria at reduced concentration of oxygen. Appl Environ Microbiol., 1980, 40, [16]Strous, M., Fuerst, J. A., Kramer, E. H. M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T. Missing lithotroph identified as new Planctomycete. Nature., 1999a, 400, [17]Strous, M., Kuenen, J. G., Jetten, M. S. M., Key physiology of anaerobic ammonium oxidation. Appl Environ Microbiol., 1999b, 65, [18]Jetten, M. S. M., Horn, S. J., van Loosdrecht, M. C. M., Towards a more sustainable municipal wastewater treatment system. Water Sci Technol., 1997, 35, [19]Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., Metzger, J. W., Schleifer, K. H. and Wagner, M. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Systematic and Applied Microbiology, 2000, 23 (1), [20]Schmid, M., Walsh, K., Webb, R., Rijpstra, W. I., van de Pas-Schoonen, K., Verbruggen, M. J., Hill, T., Moffett, B., Fuerst, J., Schouten, S., Sinninghe Damsté, J. S., Harris, J., Shaw, P., Jetten, M. 42

53 and Strous, M. Two New Species of Anaerobic Ammonium Oxidizing Bacteria. Systematic and Applied Microbiology., 2003, 26 (4), [21]Kartal, B., Rattray, J., van Niftrik, L. A., van de Vossenberg, J., Schmid, M. C., Webb, R. I., Schouten, S., Fuerst, J. A., Damste, J. S. S., Jetten, M. S. M. and Strous, M. Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Systematic and Applied Microbiology., 2007, 30 (1), [22]Kartal, B., Van Niftrik, L., Rattray, J., Van de Vossenberg, J. L. C. M., Schmid, M. C., Sinninghe Damsté, J., Jetten, M. S. M. and Strous, M. Candidatus Brocadia fulgida : an autofluorescent anaerobic ammonium oxidizing bacterium. Fems Microbiology Ecology., 2008, 63 (1), [23]Quan, Z. X., Rhee, S. K., Zuo, J. E., Yang, Y., Bae, J. W., Park, J. R., Lee, S. T. and Park, Y. H. Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environmental Microbiology., 2008, 10 (11), [24]Van Loosdrecht, M. C. M., Jetten, M. S. M. Microbiological conversions in nitrogen removal. Water Sci Technol., 1998, 38, 1-7. [25]Dijkman, H., Strous, M. Process for ammonia removal from wastewater. Patent., 1999, [26]Third, K., Sliekers, O. A., Kuenen, J. G., Jetten, M. S. M. The CANON system (completely autotrophic nitrogen removal over nitrite in one single reactor) under ammonium limitation: interaction and competition between three groups of bacteria. Syst Appl Microbiol., 2001, 24, [27]Hanaki, K., Wantawin, C., Ohgaki, S. Nitrification at low level of DO with and without organic loading in a suspended growth reactor. Water Res., 1990, 24, [28]Kuai, L., Verstraete, W. Ammonium removal by the oxygen-limited 43

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