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2 International Journal of Chemical and Environmental Engineering
Bio-electrochemical denitrification -A review
S.A.R. Mousavi1,2 , S. Ibrahim1, M.K. Aroua1, S. Ghafari1 1 Department of Civil Engineering, Faculty of Engineering, University of Malaya, 50603 Kuala Lumpur, Malaysia. 2 Department of Environmental health, Kermanshah University of Medical Sciences and Health Services, Kermanshah, Iran. Corresponding author: email@example.com
Discharge of nitrogen components into the environment can be a cause of serious problems such as eutrophication of rivers and deterioration of water sources, as well as hazard for human and animal health. Ammonia (NH 3) and nitrate (NO3-) are the most problematic nitrogen compounds in water and wastewaters. Nitrification is a common way to eliminate ammonia in municipal and industrial wastewater, which during this process ammonia oxidizes to nitrate. Nitrate removal from these types of wastewaters is an inevitable step in the treatment. Biological nitrate removal is a suitable but slow method to remove nitrate from water and wastewater. Therefore, in treatment plants, some abiotic methods have been commonly applied. However, these methods have indicated some drawbacks such as highly concentrated brine solution, which compels complexity for further treatment or disposal. Consequently, efforts have focused on speeding up microbial denitrification techniques, and different methods have been investigated in the last two decades. Among them bio–electrochemical reactors (BERs) which are equipped with immobilized autohydrogenotrophic microorganisms on cathode showed good efficiency for implementation of denitrification for any nitrate–contaminated water stream. This article reviews the diversity of nitrate source, various designs, and aspects of BERs. In addition, it discusses the variation of pH, carbon source, electric current (EC) and hydraulic retention time (HRT) as some main effective parameters on denitrification rates, and different configurations of BERs. Keywords: Nitrate, Denitrification, Bio-electrochemical reactor
Ammonia (NH3), ammonium (NH4+), nitrite ion (NO2), and nitrate ion (NO3-) are the important form of nitrogen components in aqueous solution and soil . These kinds of pollutants enter the environment from a variety of sources as contaminants, which have increased environmental problems in recent years. Therefore, effort to reduce emission and improve treatment methods for water and wastewater should be highlighted as a main public concern in the future [2-4]. Among these nitrogen components, NO3- is discharge into the environment from various sources (natural cycle, and human activities), and is known as a worldwide health hazard. In some parts of the world such as USA, India, Japan, Saudi Arabia, China, UK and several parts of Europe people consume drinking water with high concentration of nitrate , as it is increasingly becoming an important worldwide challenge. Nitrate in drinking water may reduce to nitrosamines in the stomach which is believed to cause gastric cancer[6, 7]. In addition, drinking of water contain high concentration of nitrate can be cause of disease “blue baby syndrome” due to reduction of nitrate to nitrite inside the stomach of fetus, and nitrite reacts with the hemoglobin in blood and converts the hemoglobin into methemoglobin. This new compound does not carry oxygen to cell tissues . Moreover, nitrate known as a carcinogenic compounds. To protect consumers from the adverse effects of high nitrate intake,
standards were determined for it in drinking water. The World Health Organization (WHO), US Environmental Protection Agency (EPA), and European Community establishes the limit Maximum contaminant level(MCL) for nitrates in drinking water at 50 mg NO3-/L, 12 mg/L N , and on 50 mg NO3-/L and 0.5 mg NO2-/L, respectively [10, 11]. Furthermore, different discharge standards were defined based on the receiving environment, fresh water (10 and 30 mg NO3--N/L ), seawater (50 mg NO3--N/L), and in sensitive areas discharge concentration is 10 and 15 mg TN/L . In recent years, researchers have tried to improve the removal of nitrogen component especially nitrate from water and wastewater, and have had some achievements. The aim of this review is to briefly mention the health risks of nitrate and its sources, and summarize various treatment methods of nitrate. The paper focuses on the BERs mechanism, effective factors that contribute to process efficiency, and the performance of bioelectrochemical reactors.
2. Source of nitrate
The sources of nitrate can divided to two subdivision “point sources” and “nonpoint sources”. The non–point agricultural source is confirmed as one of the important nitrate sources to pollute groundwater due to extreme use of fertilizers. Some other sources of nitrate in ground water and surface water are from uncontrolled land
discharges of treated or raw domestic and industrial wastewaters, landfills , and animal wastes predominantly from animal farms . Some industries wastewater such as dairy and swine are reported as wastewaters containing more than 200 mg NO3--N/L. Furthermore, some industries produce wastewater containing greater than 1000 mg NO3--N/L such as those producing explosives, fertilizer [7, 17, 18], cellophane, pectin, and metals finishing industries. Also, a number of activities like the processing of radioactive metal products at nuclear weapons production plants and research labs produce wastewater that consist high concentrations of nitrate that exceed 50000 mg NO3–N/L .
3. Nitrate removal methods
There are regulations made compulsory to minimize environmental problems and health risks due to uncontrolled discharge of nitrate. To achieve discharge standards, reduction of nutrients in wastewater is thus required. Research on nitrogen component removal has been ongoing for treatment of domestic and industrial wastewaters, water resources, aquaculture ponds, and aquaria. The most commonly used methods to remove nitrogen components from liquid waste especially ammonia are: chemical precipitation with magnesium ammonium phosphate, ion exchange, bio-filtration, ammonia-stripping, electrolysis, break point chlorination, and electrochemical conversion [2, 4, 20, 21]. The most common nitrate reduction method is either physicochemical or biological process . The common abiotic process consists of ion exchange (IE), electro– dialysis (ED), reverse osmosis (RO) and activated carbon adsorption in combination with pH adjustment [14, 17, 22]. The biological nitrification/denitrification is only suitable for the removal of relatively low concentration of ammonia and nitrate due to the requirement of appropriate C/N ratio [2, 4, 20, 21], Nitrate removal from drinking water and wastewater is difficult. Therefore, complementary techniques are required for obtaining a free nitrate stream in treatment plants [14, 17, 22]. Biological denitrification is a suitable method to treat wastewater contain nitrate because nitrate is transformed to harmless nitrogen gas with the present of an electron donor. However, biological remediation of wastewater with high concentration of nitrate with low chemical oxygen demand (COD) as carbon source and or internal electron donor, using an external source as electron donor is indispensable. Heterotrophic denitrification processes using methanol and acetate have been proposed in a suspended or attached growth reactor [11, 23]. Also, a wide interest towards some new methods such as metallic iron–aided abiotic nitrate reduction is recently reported by several researchers [23-25]. Ghafari et al.  stated the disadvantages along with diverse abiotic techniques, which remove nitrate from water and generate a brine solution. But, denitrifying bacteria, which are ubiquitous in nature, are responsible for biological denitrification and use oxygen in nitrate as electron acceptor during their
respiratory process instead of oxygen in anoxic condition and produce harmless gas “N2” by reduction of nitrate/ nitrite through four steps below . (1) Denitrifying microorganisms belong to several taxonomic groups and physiological groups such as lithotrophs, organotrophs, and phototrophs. Denitrifying bacteria are common among the gram-negative alpha and beta classes of the Proteobacteria, such as Pseudomonas, Alcaligenes, Paracoccus, and Thiobacillus. Some grampositive bacteria are denitrifying such as Bacillus, and a few halophilic Archaea like Halobacterium [27, 28]. Based on utilized food and energy sources, denitrifying bacteria are classified in another two major groups namely “heterotrophs” and “autotrophs” [1, 29]. Heterotrophs make use of organic carbon compounds as the carbon source , while autotrophic bacteria utilize inorganic carbons such as carbon dioxide or bicarbonate as the carbon source. In contrast to heterotrophs who use organic carbons as energy source, autotrophs make use of reduced inorganic compounds (e.g. ferrous iron, manganese, hydrogen sulfide) or molecular hydrogen (H2) as electron sources to obtain energy [19, 30-32]. Heterotrophs are more preferable for denitrification of wastewaters due to availability of organic compounds in wastewaters. In addition, they apply for biological denitrification of drinking water. However, methods applying this kind microorganism are associated with some problematic consequences such as clogging in reactors, residual carbon sources and by-products, which typically imply a further costly post treatment [33-35]. On the other hand, autotrophic denitrifying bacteria offered conditions that are more favorable: they need inorganic compounds which are less expensive compared to organics, and their residuals in treated drinking water are harmless (for H2) or less problematic (for reduced components) [35, 36]. Therefore, in recent years researchers have focused on denitrification by autohydrogenotrophic as autotrophic denitrifying, which is more promising than other autotrophic methods. Equation (2) shows reduction of nitrate to N2 by hydrogenotrophic denitrification .
4. Theory of denitrification by autohydrogenotrophic bacteria
To use this group of autodenitrifying bacteria preparing of hydrogen as electron donor plays an important role. Some researchers supply H2 by sparging in reactor as initial method. But this method have some shortcoming such as the costly provision of hydrogen gas, risking the flammable and explosive mixtures of H2 with air, transportation and storage problems [19, 26, 37]. Furthermore, It was mainly because of low solubility of H2 in water (1.6 mg/L at 20 C), which decline its availability and contact time for microbial reaction, and hence, it directly results in lower denitrification rates compared to heterotrophic denitrification [26, 35]. Therefore, in recent years researchers focus on newer
methods to solve sparging limitation, via two pathways: chemical generation of H2 and electrolysis of water [26, 38, 39]. Due to certain weakness such as slow reaction rate and generation of unwanted by-products, researchers confirmed that the electrolysis of water is a clean method to generate of hydrogen . Consequently, exploitation of electricity in denitrification process led to generation of new types of reactors named bio-electrochemical reactors (BERs) . In this reactor according to Table 1 some reactions take place during bio-electrochemical denitrification, which result in the generation of H2 on cathode by electrolysis of water according to Equations (3) and (4). Autohydrogenotrophs bacteria consume generated H2 as electron donor and during reactions (5) to (8) transfer nitrate to N2 [19, 37, 40, 41].
Table 1. Bio-electrochemical denitrification reaction in BERs Electrolysis of water in BERs:
Steps of nitrate reduction to nitrogen gas:
Net reaction overall reaction
5. Effective parameters on performance of BERs
The denitrification efficiency by BERs depend on many parameters; the key parameters in assembling of reactors are: material, geometry, number of electrodes as well as BERs design [19, 42, 43]. Influencing operational and environmental parameters are pH, HRT, carbon source and EC as theses are known to be important in denitrification by EBRs [44-46]. To reduce some drawbacks in BERs, the determination of the parametric effects and optimization of these parameters are necessary. According to Table 2 previous studies showed that various types of metals and carbons were used as electrode material; carbon in the form of granular activated carbon (GAC) and graphite as well as metals such as stainless steel, titanium, nickel and copper [40, 46, 47]. Also, various denitrifiers in different condition such as suspended in fluidized bed or immobilized on different permeable media (e.g. soil, GAC, plastic particles, mesh or reticulated planes), have been applied for different treating aqueous solution such as surface and groundwater, municipal and industrial wastewater, aquatic and river water . Many types of reactors used in bio-electrochemical system, have been investigated. In recent years, researchers have strived to improve denitrification performance, and decrease the hydraulic retention time from 10 h to several days to achieve complete denitrification , and investigated other alternatives for BERs configuration. Among them that had good results
are integrated systems, tow parts reactor (electrochemical and biological), and multi-electrode systems or threedimensional (3D) electrode [32, 48, 49]. For example Wan et al.  and Wang and Qu,  to improve effectiveness of BERs or eliminate drawbacks of integrated methods combined sulfur limestone autotrophic denitrification method (SLAD) with BER, and developed a new integrated method (bio-electrochemical combine with sulfur autotrophic denitrification (CBSAD). In the new system, the limestone for pH adjustment is not necessary. Therefore, with H+ consumption, which was produced by sulfur denitrification in the bioelectrochemical reactor, increase of effluent hardness can be prevented. In addition, the produced CO2 on anode complement process as inorganic carbon source and pH buffer, and efficiently removed nitrate more than 95% without nitrite accumulation and the sulfate concentration of effluent was lower than 250 mg/L . Two parts reactor “electrochemical cell and bioreactor” is another alternative for BERs. Flexibility in operation and simplified maintenance are the preferences of this configuration. This arrangement is economical, because of separating parts of H2 generation and biomass. Therefore, it was a possible jointing of a small electrochemical cell with a large bioreactor. Moreover, the treated water with this method even in very high nitrate concentrations is proper. In addition, the pH changes is little . The result of several study showed suitable denitrification performance with multi-electrode system compared to previous BERs because of large effective surface area of the electrodes, the charge transfer mechanism by dissociative electrolyte, and the formation of highly reducing (or oxidizing) . The pH values is one of the main factors for controlling of denitrification because it can be as limit denitrification activity and cause of nitrite accumulation . Based on equation (3) researchers have mentioned during denitrification process when NO3- change to NO2-, pH does not change. Nevertheless, in the second stage (change of nitrite to nitrogen gas) pH will increase, and nitrite accumulation occur because of pH elevation, which is one of the main reason for agglomeration of nitrite in denitrification [39, 52, 53]. However, hydrogen as an electron donor has many advantages which were confirmed, but as with traditional biological processes control of pH is also necessary. Some substrates such as carbon, nitrogen, phosphorous, and mineral components have key role on denitrification rate because substrates are necessary to grow various species of denitrifying bacteria in pure or mixed cultures [28, 52]. Among them carbon as food and energy source is a important parameter on denitrification rate by two group of denitrifyers “heterotrophic” and “autotrophic” [49, 54]. Researchers mentioned, depending on COD/N ratio of influent it may be necessary to have external carbon in BERs to denitrification of wastewater . It was stated that when the COD/N ratio of influent is lower than 3.4 gCOD/gN, extra organic matter needs to
be added . Therefore, to improve nitrate removal in water and wastewater various carbon sources [19, 56, 57] such as methanol, ethanol, sucrose, acetate, industrial and demotic wastewaters, and other industrial wastes , also bicarbonate and carbon dioxide [52, 59] have been explored. Other important effective parameters on denitrification rate in bio-electrochemical reactor is electric current intensity (I) and hydraulic retention time (HRT), which were investigated [32, 39, 49, 51]. Results showed when the electric current increased the reduction of nitrate improved. Results show that low and high electric current because of inadequate hydrogen production and excessive hydroxyl generation respectively has low reduction. Also, the efficiency of system was reduced in the low and high HRT because at low (6h) and high (48h) HRT the required reaction time for microorganisms was not achieved, but increased the rate of flushing unfavorable hydroxyl anions out of the cathode sector .
6. Implementation of BERs
The bio-electrochemical reactor process may have a potential for the removal or detoxification of other substances in water and wastewater. Therefore, some investigations have been carried out on remove various contaminants using BERs, such as simultaneous removal of nitrate and pesticide , copper ion  or ammonium nitrogen [61, 62]. Some researchers applied sulfur limestone autotrophic denitrification (SLAD) systems for nitrate removal. In this system, limestone is used to adjust the pH, and sulfur use as electron donor. During the reaction 7.54 mg/L sulfate to 1mg-N/L removed nitrate will be produced, which can raise the hardness due to produced Ca2+ by the limestone. To improve SLAD researchers combined bioelectrochemical and sulfur autotrophic denitrification (CBSAD). In this novel system, the limestone to pH adjustment is not necessary. Therefore, for preventing hardness in effluent, the produced H+ by sulfur denitrification consume in the bio-electrochemical reactor. In addition, the produced CO2 on anode complement this system as inorganic carbon source and pH buffer [32, 49]. Sakakibara and Nakayama  used a novel multielectrode system for bio-electrochemical denitrification of water contain15-20 mg NO-3-N/L. In this reactor, 8 pieces of titanium were located in reactor as cathode, and the anodes were two pieces from Pt-coated. To prevent leakage of O2 into cathode part, water-permeable plastic foam was placed between anode and cathode. Results showed suitable denitrification performance with multielectrode system compared to previous BERs because of large effective surface area of electrode, the charge transfer mechanism by dissociative electrolyte, and formation of highly reducing (or oxidizing). In another research, Prosnansky et al.  investigated a multicathode biofilm-electrode reactor combined with
microfiltration (MF) for treatment of nitrate-contaminated water. The reactor is composed of two compartments (multi-cathode BER and membrane compartments). The BER was divided two part with a porous sponge-foam rubber to impede inter O2 bubbles to cathode zone and mixing with H2. In the BER section cathodes was arranged by 5 porous GAC electrodes, and the anode was designed by platinum-coated titanium that surface area of cathode and anode were 750 and 150 cm2, respectively. Results confirmed this novel system could perform denitrification with high rates at low hydraulic retention time (20 minutes). Furthermore, the efficiency of denitrification rate improved 3–60 times in comparison with previous studies. Also, the cathodic current density decreased because of enlarged surface area of cathodes by multi-GAC electrode system. Watanaba,T et al.  applied a bio-electrochemical reactor (working volume =5 L, axial center anode carbon rod 16mm diameter, surrounded cathode with 12 carbon rods and 8mm diameter) to treat acidic wastewater containing copper ions and a high concentration of nitrate. The distance between the anode and cathode was about 50mm. Achievements showed an effective removal of copper ions and nitrate, when an electric current was applied and acetate was added as an external electron donor. Ghafari et al.  studied an up-flow bioelectrochemical reactor to denitrification of polluted water with biocarrier (GAC) and stainless steel plate as cathode zone. The achieved results for two operating parameters (HRT= 6–36 h) and electric current (I= 0 to 20 mA) were examined on contaminated water containing 20mg NO3--N/L. The nitrate completely reduced in electric current range (10–16mA) as well as HRT 13.5–30 h. The removal of nitrate in I=0 was minimum but the nitrate removal was improved by increase of electric current (up to 14mA).
Based on this review, nitrate contamination has been a worldwide environmental challenge for many years. Water contamination is a major universal concern because continuous consumption of water containing high nitrate levels can cause many diseases such as methemoglobinemia. Therefore, nitrate removal from wastewater has been the focus of numerous studies, in the aim to achieve acceptable nitrate concentration. Up to now, researchers have applied different kinds of methods for nitrate removal from water and wastewater, but results show that denitrification of contaminated water and wastewater by conventional abiotic methods are not adequate due to many reasons discussed in this paper. Even biological denitrification which is looked upon for denitrification is not functional for high concentration of nitrogen components.
Table 2. Performance of denitrification in BERs % Nitrogen removal 95 - 100 100 99.80
Type of reactor
NO3--N mgL-1 20.9 – 22.0 20 30
CBSADb UBERc 3DBERd BERe
Groundwater Contaminated water Groundwater Synthetic wastewater Municipal sewage Drinking water Synthetic groundwater Ground water Groundwater Feed solution ( groundwater) groundwater Contaminated groundwater
Stainless steel Stainless steel Activated carbon fiber Graphite felt Stainless steel Cylindrical stainless steel GAC with platinum Stainless Metal Carbon material Stainless Stainless
Carbon rod Stainless steel mesh Beta-lead dioxide Dimensionally stable anode (DSA) Graphite Carbon rod Pt-coated titanium coated
CO2 NaHCO3 CO2
30 - 1200 0–20 8-32
4.2 - 2.1 6–36 8 1-7 (4) 6 1.9–5 0.33-6 (2.88) 10 2-6 10–13 10 10–50
  
N/A 20-120 2-20
20 to 492 TN=37.2– 68 30 15-40 (25) 24
98 75 90 - 100
  
CBSAD BER-MF BER +Absorber BER
Amorphous carbon Pt-coated Carbon material Amorphous carbon Amorphous carbon
CO2 NaHCO3 NaHCO3 CO2 CO2
0–10 80-960 0-100 2-10 1–10
>95 80 98 100 N/A
    
13.8–20.8 20 20 20–24
BER BER BER
a Units used for HRT (h) . b Combined bio-electrochemical and sulfur autotrophic denitrification system (CBSAD) C Upflow bio-electrochemical reactor (UBER) d Three-dimensional bio-electrochemical reactor(3DBER) e Bio-electrochemical reactor (BER)
The trend has thus been for researchers to focus on further development of biological denitrification by creating better correlations between the nitrate and microorganisms. The bio-electrochemical system is new method, which meets this objective. The efficiency of bio-electro chemical system is affected by many parameters such as electrode specifications, pH, carbon source, HRT, and current intensity that were discussed in this review. Notwithstanding all of the mentioned prior investigation, there remain many unclear aspects, which calls for further development and improvement of efficiency of BERs since although the use of this kind of denitrification system became known two decade ago and there is insufficient information about performance of system and the effects of operational variations and configuration of reactor. There is definitely room for further research, particularly on the aspect of reactor configuration and electrodes material. Furthermore, in the case of sewage treatment applying BERs, the applicable hydraulic retention times, pH, carbon source, and current intensity are still a subject of argument.
The authors thank Universiti Malaya for financial support of this project.
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