Anda di halaman 1dari 12

Environmental

Science
Water Research & Technology
View Article Online
PERSPECTIVE View Journal

Bioelectrochemical systems for nitrogen removal


and recovery from wastewater
Cite this: DOI: 10.1039/c4ew00066h
M. Rodrguez Arredondo,ab P. Kuntke,*a A. W. Jeremiasse,c T. H. J. A. Sleutels,a
C. J. N. Buismanab and A. ter Heijneb
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

Removal of nitrogen compounds from wastewater is essential to prevent pollution of receiving water
bodies (i.e. eutrophication). Conventional nitrogen removal technologies are energy intensive, representing
one of the major costs in wastewater treatment plants. For that reason, innovations in nitrogen removal
from wastewater focus on the reduction of energy use. Bioelectrochemical systems (BESs) have gained
attention as an alternative to treat wastewater while recovering energy and/or chemicals. The combination
of electrodes and microorganisms has led to several methods to remove or recover nitrogen from
wastewater via oxidation reactions, reduction reactions and/or transport across an ion exchange
membrane. In this study, we give an overview of nitrogen removal and recovery mechanisms in BESs
based on state-of-the-art research. Moreover, we show an economic and energy analysis of ammonium
recovery in BESs and compare it with existing nitrogen removal technologies. We present an estimation of
the conditions needed to achieve maximum nitrogen recovery in both a microbial fuel cell (MFC) and a
Received 8th October 2014, microbial electrolysis cell (MEC). This analysis allows for a better understanding of the limitations and key
Accepted 16th October 2014
factors to take into account for the design and operation of MFCs and MECs. Finally, we address the main
challenges to overcome in order to scale up and put the technology in practice. Overall, the revenues
DOI: 10.1039/c4ew00066h
from removal and recovery of nitrogen, together with the production of electricity in an MFC or hydrogen
rsc.li/es-water in an MEC, make ammonium recovery in BESs a promising concept.

Water impact
Nitrogen is an essential element for life. It is applied in reactive form (NH 3 or NO 3 ) as a fertilizer on soils for growth of agricultural crops. The
accumulation of reactive nitrogen in the environment causes environmental problems such as eutrophication and acidification. To decrease the
accumulation of nitrogen in the environment, it needs to be removed from wastewaters before discharge into receiving water bodies. Classically, this is
done using a combined aerobic and anaerobic treatment process in wastewater treatment plants (WWTPs). This process requires energy for aeration, which
can constitute up to 60% of the total energy consumption of a WWTP, while nitrogen is lost. This review gives an overview of the innovative nitrogen
removal and recovery technologies based on bioelectrochemical systems (BESs). We show that BESs enable energy-efficient nitrogen removal and even
recovery of useful nitrogen (ammonia) from wastewaters.

nine planetary boundaries proposed thresholds for a safe


1 Introduction operation space of humanity have been breached, namely
climate change, biodiversity loss and nitrogen cycle.3
Population growth has dramatically accelerated,1 fueled by Nitrogen is one of the elements essential for life. Most of
developments during and following the industrial revolution. the nitrogen is present in the atmosphere as inert N 2 gas,
As of 2012, over 7 billion people live on earth. 2 As a result, where it represents approximately 78% of the present gases. In
the impact of human activities on the environment has its inert form, nitrogen is not available to most living organ-
reached a critical point, not just for humanity.3 Three out of isms and needs to be converted to more reactive forms like
nitrate NO3), nitrite (NO2), ammonium (NH4+), and ammo-
a
Wetsus, Centre of Excellence for Sustainable Water Technology, Oostergoweg 7, nia (NH3). Natural nitrogen fixation of inert N2 to reactive NH3
8911 MA Leeuwarden, The Netherlands. E-mail: philipp.kuntke@wetsus.nl;
is carried out by some prokaryotes (e.g. Azotobacter, Clostridium,
Fax: +31 (0)58 284 30 01; Tel: +31 (0)58 284 30 00
b
Sub-Department of Environmental Technology, Wageningen University,
cyanobacteria, Rhizobium) using the nitrogenase enzyme.4 This
Bornse Weilanden 9, P.O. Box 17, 6700 AA Wageningen, The Netherlands conversion is essential to provide the more reactive forms of
c
MAGNETO Special Anodes B.V., Calandstraat 109, 3125 BA, Schiedam, The Netherlands nitrogen, as a nutrient for other living organisms.

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology

Nowadays, humanity severely interferes with the natural


nitrogen cycle to provide fertilizers for agriculture. Large
amounts (120160 Mt per year) of inert N 2 are transformed
into NH 3 via the HaberBosch process,3,5 a value exceeding
the total amount of N 2 fixed annually via natural terrestrial
processes.3 While this conversion of N 2 into reactive NH 3 is
essential for fertilizer production and to increase food pro-
duction, a large part of this newly produced nitrogen even-
tually ends up in the environment,6 where it accumulates
and leads to pollution of waterways, soils and atmosphere
(acidification). One of the strategies to mitigate the effects of
nitrogen on the environment is, amongst others, removal of
nitrogen from domestic wastewater. In the current practice of
wastewater treatment, alternating aerobic and anaerobic
Fig. 1 The nitrogen cycle in fertilizer production and wastewater
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

treatments are required to remove the dissolved nitrogen and


treatment processes.
to convert it to inert N 2 gas. The disadvantage of aerobic
treatment is the considerable amount of energy required for
aeration. Innovations in nitrogen removal from wastewater produced ammonia (~80 Mt N per year) is used as a fertilizer
therefore focus on the reduction of energy use. in agriculture to enhance food production.3,5 Part of the
Bioelectrochemical systems (BESs) offer clean and CO2 neu- ammonium is taken up by the crops, but another part ends
tral recovery of energy from wastewaters. The core of BESs is up in the environment, where they increase the risk of eutro-
electrochemically active microorganisms, which can exchange phication of receiving water bodies, and adds to the pollution
electrons between electrodes and organic substances to con- of the atmosphere.
vert chemical energy into electrical energy or the other way Because of these adverse effects on the environment, reac-
around.712 This variety of conversions has led to research in tive nitrogen compounds in wastewater were considered as
many areas: from wastewater treatment for electricity produc- pollutants, and the importance of removing or recovering
tion, and the production of chemicals, to conversion of elec- nitrogen compounds from wastewater was recognized.17 In
tricity into methane or organic compounds. Alternatively, BESs wastewater, nitrogen is mostly present in the form of ammo-
have been proposed as a new treatment technology to remove nium, and removal of ammonium in wastewater treatment
nitrogen from wastewaters while producing electricity.13,14 Dif- plants mainly occurs via a two-step process.18 During the first
ferent types of nitrogen-based reactions have been reported step, nitrification under aerobic conditions, ammonia is oxi-
both at the anode and at the cathode. Recently, some of these dized to nitrite by Nitrosomonas, and subsequently, nitrite is
reactions have been addressed in a study on nutrient removal oxidized to nitrate by Nitrobacter according to (reaction (2),
and recovery in BESs by Kelly and He (2014).15 Fig. 1):
The objective of our study is to give an overview of the I : NH 4 1.5O 2 NO 2 H 2O 2H
state-of-the-art research on nitrogen removal or recovery in II : NO 2 1/ 2O 2 NO3 (2)
BESs and to compare these new processes to existing nitro-
Overall : NH 4 2O 2 NO3 H 2O 2H
gen removal technologies. Our economic analysis, that builds
on the previous work by Sleutels et al. (2012),16 shows that So for each mole of ammonium, 2 moles of oxygen are
ammonium recovery from urine is a promising concept for required for full oxidation to NO 3 . During the second step,
economical application of BESs, mainly because of the high denitrification under anoxic conditions, nitrate is reduced to
revenues generated from removal and recovery of nitrogen. N2 gas, for example, by Paracoccus denitrificans, according to
(reaction (3), Fig. 1):
2 The influence of humans on the
nitrogen cycle: biological, chemical, 2NO3 + COD N2 + CO2 + 2OH + H2O (3)
and physical processes
The produced N 2 gas is released (or recycled) to the
The HaberBosch process is the primary human-driven atmosphere.
industrial conversion process of inert N2 to NH3. In this con- The disadvantage of the conventional nitrification/
version, nitrogen gas reacts with hydrogen gas (H2) according denitrification reaction is that it requires considerable
to (reaction (1), Fig. 1): amounts of energy, because the wastewater needs to be
aerated to supply oxygen for the conversion of ammonium to
N2 + 3H2 2NH3 (1) nitrate, and a supply of electrons for denitrification in the
form of COD (e.g. methanol) is required. The advantage of
The H2 required for the HaberBosch process is produced nitrification/denitrification is that nitrogen can be removed
via steam reforming of natural gas. Most of the industrially at low concentrations.

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014
View Article Online

Environmental Science: Water Research & Technology Perspective

Anammox (anaerobic ammonium oxidation) has been pro- Depending on the cathode reaction, BESs can be divided
posed as a more energy-efficient alternative to the conven- in two types: galvanic and electrolytic cells. In galvanic cells,
tional nitrification and denitrification process. Anammox electricity is produced by coupling the anodic oxidation to
relies on the biological conversion of ammonium and nitrite the reduction of a suitable electron acceptor (i.e. O 2, Fe 3+,
to N2 gas by specialized bacteria (planctomycete-like).19 First, and Cu2+).2426 These systems are called microbial fuel cells
part of the ammonium needs to be partially oxidized to (MFCs). In electrolytic cells, electricity is needed to drive the
nitrite in a pretreatment step. Therefore, Anammox is com- reduction reaction at the cathode. In a so-called microbial
bined with, for example, the SHARON (Single reactor system electrolysis cell (MEC), the anodic oxidation is coupled to
for High-rate Ammonium Removal Over Nitrite)20,21 process. reduction of protons to hydrogen gas.8,2729
SHARON is a biological process in which ammonium is oxi- The cathodic reactions of an MFC (oxygen reduction reac-
dized to nitrite (instead of a complete oxidation to nitrate). tion, ORR) and an MEC (hydrogen evolution reaction, HER)
The oxidation to nitrite is possible due to the specific growth under neutral to alkaline pH conditions are given in reac-
rates of nitrite-oxidizing bacteria, ammonium-oxidizing bac- tions (6) and (7), respectively.
teria and the applied loading rate of the reactor. Another
2H2O + O2 + 4e 4OH
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

approach is the so-called CANON (Completely Autotrophic (6)


Nitrogen removal Over Nitrite) process, where the aerobic
and anaerobic ammonium oxidizers symbiotically coexist. In 2H2O + 2e H2 + 2OH (7)
the CANON process, it is possible to perform aerobic and
anaerobic ammonium oxidation simultaneously. Therefore, BESs are seen as a potential sustainable solution to treat
ammonium-oxidizing and Anammox bacteria cooperate.22 wastewaters while at the same time producing energy and/or
The overall Anammox process can be described by (reaction (4), chemicals. Anode and cathode chambers are often separated
Fig. 1): by an ion exchange membrane to prevent mixing of the oxi-
dation and reduction products. 8,9 The ion exchange mem-
I : NH 4 1.5O 2 NO 2 H 2O 2H brane allows for anions and/or cations to be transported to
(4)
II : NH 4 NO 2 N 2 2H 2O maintain electron neutrality of the electrochemical system.
BESs allow for energetically and chemically efficient
Because only half of the ammonium needs to be oxidized ammonium recovery from wastewater. The organic matter in
to nitrite and no addition of COD is required, the energy wastewater is oxidized at the anode by bacteria, while ammo-
input for the SHARON/Anammox process is considerably nium (present in the wastewater) is transported over a cation
lower than the energy input for conventional nitrification/ ion exchange membrane (CEM) to the cathode chamber,
denitrification.19,21 where the high catholyte pH allows for recovery in the form
A recent study23 reports a new process for the removal of of ammonia. Therefore, no addition of caustics is required
nitrogen from wastewater: Coupled Aerobicanoxic Nitrous compared to other ammonia recovery technologies. In this
Decomposition Operation (CANDO). CANDO consists of three way, BESs can create a shortcut in the nitrogen cycle by
steps: (1) partial nitrification of NH4+ to NO2 (by the SHARON removing NH 3 from the wastewater, not by reduction to N 2
process), (2) partial anoxic reduction of NO2 to N2O and (3) but by direct recovery in the form of NH3 (Fig. 1).
decomposition or combustion of N2O to nitrogen, oxygen and Ammonium recovery using an electrochemical cell (EC)
energy.23 Even though pilot-scale studies are needed, this was investigated by Desloover et al. (2012).30 Ammonium
process has the potential to lower oxygen demand and sludge recovery from anaerobic digestate was investigated using an
production, as well as recover energy from nitrogen. electrolysis cell, in which ammonium transported over a
Recently, bioelectrochemical systems (BESs) have been CEM was stripped from the catholyte by the produced hydro-
investigated as an alternative to the conventional wastewater gen. The current and thus the rate of ammonium transport
treatment processes, such as organic matter and nitrogen in such an abiotic system are not limited by the biological
removal. A BES is an electrochemical cell which uses microor- catalyzed anode reaction. Furthermore, the common limita-
ganisms to catalyse one or more reactions taking place on tion of high internal resistance in MFCs by the cathodic reac-
the electrodes. At the anode, anaerobic microorganisms can tion (ORR), which is the result of the prevalent conditions
oxidize biodegradable organic matter to carbon dioxide, pro- found in MFCs (temperature, pH and oxygen concentration),
tons and electrons, which is often represented by the oxida- is not found in such an EC. As a result, the reported ammo-
tion of acetate: nium transport rates (120 gN m2 d1) are significantly higher
than those reported in MFCs, whereas the ammonium trans-
CH3COO + 4H2O 2HCO3 + 9H+ + 8e (5) port accounted for approximately 40% of the overall charge
transport over the membrane, similar to results found in
As the electrode can act as an electron acceptor, the pro- BESs.13,14 Desloover et al. (2012) reported an energy demand
duced electrons are transferred by the microorganisms to the of 5 kW h kg N 1 (or 18 kJ g N 1) for ammonium recovery by
anode, which is connected over an external circuit to the an EC,30 which is lower than the reported energy demand of
cathode where a reduction reaction takes place. 9 kW h kg N 1 (or 32.4 kJ g N 1) for conventional ammonia

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology

stripping.31 However, they did not take into account the be formed first, for example, via biological oxidation of
energy used for stripping and absorption. Finally, similar to ammonium by aeration (2b). Alternatively, ammonium can
the BES approach, no caustic is necessary to increase the pH be converted into N 2 via Anammox, which is, in principle,
at the cathode. independent of the cathode. The third mechanism that has
been suggested occurs at the anode, where ammonium is
directly converted into nitrogen gas by microorganisms (3),
3 Bioelectrochemical systems for but clear evidence is still lacking. The fourth mechanism is
ammonium removal and recovery incorporation of ammonium in biomass during microbial
growth in the anode (4) or in the cathode compartment.
As an alternative to conventional nitrogen removal processes, Concerning the direct oxidation of ammonium to nitrogen
bioelectrochemical systems offer new advantages. Several gas at the anode (3), a study reports that ammonium is
nitrogen-based reactions in BESs, both at the anode and at involved in electricity generation either directly as the anodic
the cathode, have been reported so far. In this section, we fuel or indirectly as substrates for nitrifiers to produce
will give an overview of the reported ammonia removal and organic compounds for heterotrophs.36 On the contrary, it
recovery mechanisms in BESs (Fig. 2). The first mechanism
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

was reported in the study of Kim et al. (2008) that ammonia


of ammonium removal/recovery is based on active and pas- removal, instead of being biologically oxidized at the anode
sive transport through the ion exchange membrane, com- to nitrogen gas, was mainly due to physicochemical factors,
bined with acid/base equilibrium (1). NH4+ concentrations in such as diffusion through the membrane and volatilization
wastewater are considerable: in urine >4 g L 1 (ref. 3234) of ammonia due to pH increase at the cathode.37 Zang et al.
and in domestic wastewater 0.04 g L1 (ref. 18 and 35). Con- (2012) also reported that direct ammonia oxidation in the
sequently, especially in highly concentrated wastewaters, anode was not a source of electricity.38 Cyclic voltammetry
NH 4 + is the main ion transported through the membrane, tests did not detect redox couples, nitrite and nitrate were
either passively in its non-charged NH 3 form (1a) or actively not found and nitrifying or Anammox bacteria were not iden-
in its charged NH 4 + form (1b). In the catholyte, it can leave tified in the anode compartment.38 In conclusion, the occur-
the system in the form of ammonia as the chemical equilib- rence of direct oxidation of ammonium to nitrogen gas so far
rium shifts from ammonium to ammonia because of the ele- lacks solid proof.
vated pH in the cathode (1c). The second mechanism is Table 1 gives an overview of the reported mechanisms for
reduction (denitrification) of nitrate to inert N2 gas by micro- the removal and recovery of ammonium via routes 1 and 2
organisms at the cathode (2a). In this case, nitrate needs to and their performance.

3.1 Diffusion and migration of NH3 and NH4+


In a BES equipped with a CEM, ammonium (and other
cations) can be transported from the anode to the cathode
chamber by two processes: migration and diffusion. Transport
by migration is induced by the electric field across the ion
exchange membrane. Diffusional transport is induced by a
concentration gradient across the ion exchange membrane. As
a result of the production of hydroxyl ions in the ORR and
HER, and the insufficient H+ and OH transport over the CEM,
the pH increases in the cathode chamber.4648 Therefore, ionic
ammonium is transformed into volatile ammonia, which can
be removed from the cathode compartment by NH3 stripping
with a suitable gas stream. Hence, one of the advantages of
using BES for nitrogen recovery is that no additional caustics
Fig. 2 Overview of the ammonia removal mechanisms in an MFC. This need to be added to increase the pH of the solution.13
figure is representative of BES in general. Ammonium can be Kim et al. (2008) studied ammonia loss from swine waste-
transported through the membrane (1) either passively via diffusion of
water in both single- and two-chamber MFCs.37 An air
ammonia (1a) or actively via migration in the form of ammonium (1b).
Ammonia can leave the system by evaporating into its gaseous form as
cathode was used in the single-chamber MFC, while both
a result of the elevated pH in the cathode (1c). At the cathode aerated phosphate buffer and ferricyanide were tested as
chamber, it can be (biologically) oxidized by oxygen and denitrified by catholyte in the two-chamber MFC. An ammonia removal of
microorganisms at the cathode (2a) or in solution (2b) the dashed 60% was reached in 5 days in the single-chamber MFC
lines show processes that are independent of the electrodes. At the
(cathode exposed to air), while 68% was accomplished in
anode, it has been suggested that ammonia can be directly nitrified/
denitrified to nitrogen gas by microorganisms; however, solid proof is
13 days when using ferricyanide as a catholyte in the two-
still lacking (3). Finally, ammonium can be incorporated in biomass for chamber MFC. The authors concluded that the main mecha-
growth (4), either in the anode or in the cathode chamber. nism for this ammonia removal was ammonium transport

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014
View Article Online

Environmental Science: Water Research & Technology Perspective

Table 1 Performance of the reported mechanisms for the removal and recovery of nitrogen in BESs

Type of N concentration Current density


Reactor type wastewater Removal mechanism influent (mgN L1) Removal efficiency/rate (A m2) Ref.
Single-chamber MFC Swine Ammonia removal 188 6 60% 0.5 mAe 37
wastewater
Dual-chamber MFC Swine Ammonia removal 219 2 68% 0.5 mAe 37
wastewater
Dual-chamber MFC Swine Ammonia removal 219 2 89% 0.3 mAe 37
wastewater
Dual-chamber MFC Urine Ammonia removal 4050 3.3 gN m2 d1 0.5 13
Dual-chamber MFC Urine Ammonia removal 4050 9.7 gN m2 d1 2.7 33
Dual-chamber MEC Urine Ammonia removal 700 162.18 gN m2 d1 14.7 39
Dual-chamber MFC Synthetic Nitrate reduction 2615 146 gN m3 d1 a 35 A m3 a 40
Dual-chamber MFC Synthetic Nitrification coupled to 88 67.4% and 410 gN m3 NCC d1 b 133 A m3 b 41
nitrate reduction
Dual-chamber MFC Synthetic Simultaneous nitrification 41 94.1% TN c and 104 gN m3 39.7 A m3 d 42
and denitrification TCV d1 d
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

Dual-cathode MFC Synthetic Nitrification and 3090 6790% TN c and 140 gTN m3 d1 c 43 A m3 f 43
denitrification
Single-chamber MFC Synthetic Simultaneous nitrification 100 96.8% 3.6 44
and denitrification
Dual-chamber Synthetic Ammonia removal 3000 2.94 gN m2 d1 3.6 45
MFC/MEC
Dual-chamber Synthetic Ammonia removal 3000 8.5 gN m2 d1 3.6 45
MFC/MEC
Dual-chamber Synthetic Urea removal 4000 37.8 gN m2 d1 5 45
MFC/MEC
a
Based on cathodic volume. b NCC: net cathodic compartment. c TN: total nitrogen. d TCV: total compartment volume. Both cathode and anode
have the same volume. e Insufficient data to determine current density. f Based on anodic volume.

(migration and diffusion) to the cathode with subsequent investigated the feasibility of ammonium recovery in a two-
ammonia volatilization. chamber MFC with a CEM using a sacrificial potassium ferri-
Exploiting this ammonia loss mechanism, future work of cyanide cathode system.14 The authors showed that ammo-
research groups focused on ammonia as a suitable proton nium concentrations up to 4 g N L 1 did not affect the
shuttle for pH control in BESs and ammonium recovery by performance of the MFC and that total ammonium transport
NH 3 stripping from the cathode.13,14,49 Cord-Ruwisch et al. from anode to cathode accounted for up to 50% of the charge
(2011) investigated the feasibility of more sustainable pH transport. Following up on this proof of principle, Kuntke
control in MFCs by proton shuttling from anode to cathode et al. (2012) demonstrated and evaluated the feasibility of
via ammonia addition to the anode chamber.49 Their results using a two-chamber MFC with a gas diffusion cathode.13
showed that ammonium accounts for 90% of the ionic flux Here, the volatile ammonia was removed from the cathode
in the BES and that ammonia recovered from the cathode chamber by the gas stream used for aeration and subse-
could be recycled to the anode. Further investigation by quently collected in a gas wash bottle containing an acid
Cheng et al. (2013) demonstrated the feasibility of such (boric acid). They reported an ammonium recovery rate of
ammonium recycle for anolyte pH control in an MEC also 3.3 gN m2 d1 from urine with an energy yield of 3.46 kJ gN1
demonstrating a possible pathway for ammonia recovery at a current density of 0.5 A m2. Later results presented by
from wastewater.50 Kuntke et al. (2013) showed an ammonium recovery rate of
In domestic wastewater, most of the nitrogen (75%) origi- 9.7 gN m2 d1 from urine with an energy yield of 10 kJ gN1
nates from urine.51 This nitrogen is excreted by humans in at a current density of 2.6 A m2 (ref. 33). Following the stud-
the form of urea NH2)2CO),32 which is hydrolyzed to ammo- ies of Cheng et al. (2013)50 and Desloover et al. (2012),30
nia and carbamate by the enzyme urease.52,53 Kuntke et al. (2014) investigated simultaneous ammonium
recovery and hydrogen production from urine in an MEC.39
urease
NH 2 2 CO H 2O NH 2COOH NH3 (8) They achieved a stable ammonium removal rate of
162.2 g N m 2 d 1 at a current density of 14.7 A m 2, while a
Subsequently, carbamate decomposition leads to the for- maximum removal rate of 173.3 gN m2 d1 at a current den-
mation of ammonia and carbon dioxide: sity of 23.1 A m2 was reported.39
The consumed COD also represents a certain amount of
NH2COOH + H2O NH3 + H2CO3 (9)
energy. In this respect, it is interesting to compare the COD
Ammonium recovery from urine in an MFC was first consumption for different nitrogen removal and recovery pro-
reported by Kuntke et al. (2011), where the authors cesses. Using an MFC or an MEC, for each kg of N recovered,

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology

0.57 kg of COD is required, assuming that each mole of COD formation by using a diethylamine-functionalized polymer
corresponds to 4 moles of electrons, that the COD is (DEA) as a catalyst binder instead of the conventional Nafion-
converted into electricity at 100% coulombic efficiency, that type binder and went through an enrichment period of
all cation transport occurs through NH4+, and that all NH4+ is 75 days. The MFC with the DEA binder had an ammonia
recovered at the cathode. For nitrification/denitrification, the- removal efficiency of up to 97%, while that with the Nafion
oretically, 2.86 kg COD is required for removal of 1 kg of N.54 binder (which also went through the pre-enrichment) had an
On the other hand, nitrification and Anammox require no ammonia removal efficiency of 91%. The maximum total
COD at all. nitrogen efficiencies were between 75% and 95%, but nitrate
concentrations of up to 30 mg L1 were detected in the MFC
effluent. Furthermore, the enrichment process improved the
3.2 Nitrification/denitrification at the cathode maximum power densities of the MFCs regardless of the cata-
The second part of Table 1 summarizes the performance of lyst binder, while without the enrichment, power production
systems that studied denitrification at the biocathode. was about 25% lower.
Clauwaert et al. (2007) showed that complete denitrification
4 Ammonia recovery from urine
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

could be performed by microorganisms in the cathode of an


MFC.40 Acetate was used as the electron donor in the biologi- in an MFC and an MEC
cal anode, while nitrate was used as the electron acceptor in
the biological cathode. Electricity production was thus Kuntke et al. (2013) proposed a full treatment concept for
coupled to the reduction of nitrate to nitrogen gas by urine, in which ammonium is recovered using a BES33
denitrifying microorganisms. Nitrate was removed at a rate of (Fig. 3).
146 gN m3 d1. The treatment concept includes phosphate recovery via
Virdis et al. (2008) coupled the anodic oxidation of organic struvite (also known as MAP, MgNH4PO46H2O) precipitation
matter and cathodic nitrate reduction in an MFC to an exter- as a pre-treatment step followed by a BES to recover energy
nal nitrification reactor enabling the removal of ammonium and ammonia simultaneously. Notably, the recovered ammo-
from wastewater by nitrification and denitrification while nia can be used either as a fertilizer or as an energy source,
producing electricity. During their experiments, organics for example, in a fuel cell.55 In the proposed scheme, caustics
present in the anode influent containing ammonium were can be obtained as a by-product. The BES could be either an
oxidized to produce electricity. The anode effluent containing MFC for electricity production or an MEC, in which case
ammonia was fed to an external biofilm reactor for nitrifica- hydrogen would be produced instead of electricity. The
tion followed by denitrification at the cathode.41 The authors advantage of using an MEC is that a voltage is applied, which
reported a removal rate of 0.41 kg N per m 3 of net cathode helps overcome the internal resistances of the system, and
compartment per day and a removal efficiency of 67.4%. higher current densities can be achieved compared to an
Virdis et al. (2010) also used nitrate as an electron accep- MFC. On the other hand, the advantage of an MFC is its elec-
tor at the cathode of an MFC.42 The system accomplished tricity production, as applying a voltage in an MEC means an
simultaneous nitrification and denitrification by optimising additional energy input.
the oxygen supply in the aerated cathode chamber. The In this section, we present an analysis of the potential
anode effluent was directed to the cathode through a loop energy recovery from urine, in the form of electricity or
connection to mitigate the pH increase in the cathode. Low hydrogen, and ammonia, using a BES under different con-
levels of nitrate and ammonium in the effluent were accom- ditions. Urine, collected by separation toilets and water-free
plished (1 and 2 mgN L1, respectively). The highest nitrogen urinals, has a COD and an ammonia concentration of
removal efficiency obtained in this system was 94%. 101.6 gCOD L1 and 8.10.4 gN L1, respectively.34 In this
Zhang and He (2012) also achieved high ammonia and case, to resemble the treatment concept shown in Fig. 3, a
total nitrogen removal efficiencies (96% and between 67% urine supernatant after struvite precipitation with COD and
and 90%, respectively) by testing a tubular dual-cathode
MFC, in which both anion and cation exchange membranes
were used.43 The design allowed for an anoxic inner cathode
in which bioelectrochemical denitrification could take place
and an aerobic outer cathode for the nitrification process,
which shared the same anode. A final nitrate concentration
of 3 mgN L1 was achieved in this system.
Finally, higher ammonia removal efficiencies compared to
the previous system were reached without the extra energy
input of aeration by Yan et al. (2012).44 The MFC consisted of
a single chamber with an air cathode which was pre-enriched
with a nitrifying biofilm. The cathode was especially prepared Fig. 3 Proposed full treatment concept for urine, in which ammonium
with partial positive charges to promote the nitrifying biofilm is recovered using a BES.

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014
View Article Online

Environmental Science: Water Research & Technology Perspective

NH 4-N concentrations of 4 g L1 was used as a model, corre- In BESs, the produced charge (related to current) is equal
sponding to earlier reported concentrations.13 The typical pH to the amount of ions that are transported through the mem-
difference observed in previous experiments performed in brane. The transport efficiency (N) represents the percent-
two-chamber BESs with urine is 6 (pH 7 in the anode and age of ammonium that is transported through the membrane
13 in the cathode). This pH gradient means that a higher compared to the total amount of ions transported. Thus, at a
applied voltage would be required in an MEC and a higher transport efficiency of 100%, all the transported charge
energy loss would be experienced in an MFC.16 The effect of through the system is in the form of ammonium. The overall
this gradient, which can be considered as an additional ammonium flux increases with increasing current density
internal resistance, was included in the calculations. and increasing ammonium transport efficiency. From the
Furthermore, in this calculation, it was assumed that there combination of Fig. 4A and B, the total amount of ammo-
is no energy input for the MFC, and the energy outputs nium that is transported from the anode compartment to the
come from electricity production and ammonia recovery. cathode compartment can be related to ammonium transport
For MECs, the energy input consists of electricity or external efficiency, coulombic efficiency, and COD loading rate. Here,
power supply, and the energy outputs are hydrogen produc- it is assumed that 100% of the ammonia which is removed is
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

tion and ammonia recovery. To calculate the theoretical also recovered. Clearly, to maximize the ammonium recovery,
energy output, the lower heating values (LHV) for both hydro- the BES needs to be operated at high coulombic efficiency
gen and ammonia were used: 10 817 J L 1 for hydrogen56 and high loading rate (to achieve a high current density), in
and 18 577 J g 1 for ammonia (adapted from Hacker combination with high ammonium transport efficiency.
et al. (2003) (ref. 57)). For comparison, the values for both These aspects will be further discussed in section 6.
MFC and MEC are presented in units of kJ per gram of Reported values (Table 2) for MFCs and MECs for urine
nitrogen recovered. The potential NH 4-N removal depends treatment are well in line with Fig. 4A. In MFC mode, the
on both the coulombic efficiency of the system and the COD loading rate was 286 gCOD m2 d1, but not all COD was
ammonium transport efficiency across the membrane. removed, while in the calculation for Fig. 4, it is assumed
Therefore, the amount of removed ammonium from the that all COD is removed. Therefore, we compare the perfor-
anode compartment can be calculated based on assump- mance of the BES treating urine (Table 2) with Fig. 4 based
tions for coulombic efficiency, loading rate and transport on COD removal rate. At 181 gCOD m2 d1 and 10% coulom-
efficiency as will be described below. bic efficiency, indeed the expected current from Fig. 4A is
Fig. 4A shows the theoretical current density (contour below 5 A m2 (measured value of 2.6 A m2). In MEC mode,
lines) as a function of the coulombic efficiency and the COD at a COD removal rate of 171 g COD m 2 d 1 and 96% cou-
loading rate. The coulombic efficiency represents the amount lombic efficiency, the expected current is between 20 and
of degraded COD that ends up in electricity, where one mole 25 A m2, matching well with the measured value. Now, the
of COD corresponds with 4 moles of electrons, while the current can be linked with the N removal rate (Table 2) to
loading rate is the amount of COD that is added to the sys- determine the N transport efficiency. For the MFC, the N
tem per time unit. This figure shows that current density transport efficiency derived from Fig. 4 is 30%, a value also
increases with increasing loading rate and increasing cou- reported in this study; for the MEC, it is 60%.
lombic efficiency. In addition, the same current density can Fig. 5A shows the energy yield for a scaled-up MEC
be achieved by combining a high loading rate and a low cou- treating urine for ammonia recovery, using the concept
lombic efficiency or vice versa. proposed by Kuntke et al. (2013).33 All calculations were

Fig. 4 (A) Current density (A m 2) as a function of coulombic efficiency (%) and loading rate (g d 1) and (B) ammonium flux from anode to
cathode (g d1) as a function of transport efficiency (%) and current density (A m2).

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology

Table 2 Examples of current densities, coulombic efficiencies, COD show that achieving a low internal resistance in these sys-
loading and removal rates, internal resistances, and power outputs
tems is crucial to actually recover energy from urine,
achieved in BES treating urine
because low internal resistance leads to both high current
Microbial Microbial density and low power consumption.
fuel cell electrolysis cell The results of the analysis for an MFC are not shown here
Current density (A m2) 2.6 0.1 23.1 1.15 but are comparable. The main difference is that the current
COD loading rate (gCOD m2 d1) 285.7 7.1 466.6 14.0 range that can be achieved in the MFC is much smaller
COD removal rate (gCOD m2 d1) 180.9 5.8 171.0 16.9
(3.5 A m2) compared to the MEC. In an MFC, the cell voltage
Coulombic efficiency (%) 10.4 0.5 95.6 3.1
N removal rate (gN m2 d1) 10 173.34 18.07 is limited by the internal resistance. This internal resistance
Internal resistance (m m2) 95 43 2.2 causes the cell voltage to decrease to short circuit conditions
References 33 39 (0 V, reached at 3.5 A m 2 in our analysis). Currents higher
than short circuit cannot be achieved in MFC mode, which
means that to achieve higher current densities, the MFC
performed for current densities from 0.5 to 25 A m 2 would operate as an MEC. Here, the applied voltage acts as a
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

(normalized by the membrane surface area) and for high driving force for the reactions to proceed at a high rate, and
(200 m m 2) and low (25 m m 2) internal resistances. thus, current densities higher than 3.5 A m 2 can be
Negative values for energy recovery represent actual energy achieved. Although MFCs do not rely on the input of electri-
recovery. Fig. 5A shows that systems with low internal resis- cal energy to drive the reactions (applied voltage), this addi-
tance (25 m m 2) can be used in the full current range to tional applied energy in MECs is recovered in the form of
recover energy from urine. At high internal resistance hydrogen. The recovered energy in the form of nitrogen is
though (200 m m 2), operating in the low current density the same for both systems as it is directly correlated to the
range (up to 13 A m 2) is required to recover energy from produced current. As a result, the energy balance for both
the system. The reason for this is that at high internal resis- MFC and MEC, at low current densities (<3.5 A m 2), is
tance, the power input required to overcome the internal similar.
resistance to achieve a certain current density increases In the comparison shown above, the energy required for
much faster than the recovery of energy in the form of pumping and stripping is not taken into account, because at
hydrogen and ammonium. This can be seen in more detail this early stage of development no realistic estimations can
in Fig. 5B. Here, the effect of the different contributions to be made in terms of flow rates required in scaled-up systems.
the total energy balance for a system with 200 m m 2 inter- Of course, these processes will negatively affect the energy
nal resistance is shown. The input of electrical energy recovery from urine.
increases linearly with increasing internal resistance, as
more energy is required to overcome the internal resistance at
higher current density. The output energy (kJ gN1 recovered) 5 Economic analysis for ammonia
in the form of H 2 and NH 3 in Fig. 5B is independent of recovery from urine in an MFC
current density because it is normalized by the nitrogen and an MEC
recovered. The nitrogen recovered is directly related to the
current density through the transport efficiency of ammo- Sleutels et al. (2012) have shown an approach to determine
nium. Overall, energy can only be recovered at high internal the maximum internal resistance at which point it is still eco-
resistance when the electrical energy input is limited, and nomically feasible to apply MFCs and MECs for the removal
thus current density is lower than 13 A m 2. These results of COD from wastewater.16 In this analysis, the costs (both

Fig. 5 (A) Energy recovery in an MEC as a function of current density for high (200 m m2) and low (25 m m2) internal resistances. The energy
recovery for an MFC is not shown since it is comparable to the MEC. (B) A more detailed overview of the energy input (electrical) and output
(hydrogen and ammonia) for the MEC with an internal resistance of 200 m m2 as a function of current density.

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014
View Article Online

Environmental Science: Water Research & Technology Perspective

operational and capital) and benefits of both systems for the Only at 25 m m 2, the revenues become higher than the
treatment of COD in wastewaters were estimated. Here, we costs at current densities that have been achieved in MFCs so
extend the analysis for the case that ammonium is recovered far (510 A m 2). Like Sleutels et al. (2012) reported before,
in an MFC or an MEC. The economic value of the treatment hardly any MFCs so far have reached such a low internal
of urine, products and by-products is presented in Table 3. resistance.16
Similar to the example of COD removal, the value for ammo- When the recovery of ammonia is taken into account,
nia removal mainly originates from the fact that no addi- much higher internal resistances can be allowed for both sys-
tional treatment is required. tems at which the process is still economic, mainly because
As an indication for feasibility of simultaneous ammo- of the savings for wastewater treatment that are reflected in
nium recovery and wastewater treatment in MFCs and MECs, the value of ammonia per kg of N removed. This means that,
costs and benefits have been calculated for current densities for example, distances between electrodes can be allowed to
in the range of 0 to 50 A m 2. The results for the economic be higher to still achieve higher revenue than cost, making
comparison for the removal of ammonia are shown in Fig. 6A scale-up of the systems easier. When ammonium recovery is
for MFCs and in Fig. 6B for MECs. To study the effect of taken into account, the costs become relatively low compared
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

internal resistance, the analysis was done at both 25 and to the revenue for both the MFC and the MEC. It should be
200 m m2. noted however that, when locally produced, the production of
The solid lines in Fig. 6 represent the costs for the MFC electricity compared to hydrogen is probably more attractive.
and MEC consisting of both capital and operational costs. These calculations show that the removal of ammonia in
The dotted lines represent the revenues at high and low inter- BESs gives a significant economic value in addition to the
nal resistances and with and without N recovery. When reve- production of electricity in an MFC or hydrogen in an MEC,
nues are higher than costs, the system becomes profitable. which leads to less stringent design criteria (e.g. in terms of
Clearly, when ammonium recovery is included in the eco- internal resistance), and an easier road towards practical
nomic analysis in addition to COD removal, the revenues application. Kuntke et al. (2014) reported an internal resis-
increase for both MFC and MEC at both internal resistances tance of 43 m m 2 (Table 2) for urine treatment using an
(Fig. 6A and B) compared to the situation without ammo- MEC with platinum-coated titanium electrodes. The chal-
nium recovery. Both systems become profitable at almost all lenge now is to reach similar internal resistances with less
current densities, even at higher internal resistance. expensive materials.
The capital costs for both MFCs and MECs are similar,
since these systems have the same configuration and are
constructed from the same materials. However, the capital 6 Challenges in bioelectrochemical
costs decrease with increasing current density when systems for nitrogen recovery
expressed in kg CODr 1, because the rate of COD removal
increases at higher current densities. In contrast with the In the previous sections, we have shown and compared the
capital costs, the operational costs are different for MECs different processes for nitrogen removal and recovery in
and MFCs. For MFCs, the operational costs are independent BESs. Although our analysis shows a promising prospect for
of current densities, while for MECs, the electrical energy application of ammonium recovery via membrane transport
input and thus the operational costs need to be increased to in an MFC or an MEC, there are still several challenges to
achieve a higher rate of hydrogen production. Therefore, the overcome before the technology can be applied in practice.
total costs for MECs have a minimum value, determined by Most importantly, we need to optimize the ammonium
the current density and the internal resistance, and the total recovery and therefore the ammonium transport across the
costs for MFCs decrease with increasing current density. For membrane. At present, the reported values for the ammo-
the MFC, low internal resistances are required to make pro- nium removal efficiency from urine, e.g. the fraction of
duction of electricity from wastewater economically attractive. ammonium that is removed from urine, are around 30%. The

Table 3 Overview of the parameters used in the economic evaluation of MECs and MFCs as a treatment concept for wastewater

Parameter Unit References


1
Electricity 0.06 kW h 58
Hydrogen 0.35 m3 59
Capital and operational costs 0.05 per kg COD removed Calculated from ref. 60
COD removal 0.35 per kg COD removed 61
Ammonia removal efficiency 30 % Based on ref. 13
Ammonia removal 1.63 per kg of N removed 62
pH difference between anode and cathode 6 Estimated from ref. 63
Applied voltage 1 V
Interest rate 6 %

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology


Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

Fig. 6 Comparison of the costs and revenues of ammonia recovery in an MFC (A) and in an MEC (B). The costs and revenues are shown at
different internal resistances of the system and with and without the recovery of ammonia.

removal of ammonium from the anode waste stream is we assume that all the COD is converted into electrons and
dependent on several factors, most importantly (i) the con- that ammonium is the single transported cation. Further
centration of ammonium in the wastewater, (ii) the removal experiments are needed to study which COD removal effi-
of ammonium from the catholyte/cathode head space by ciency, coulombic efficiency, and nitrogen recovery can be
stripping, (iii) the current density, (iv) the catholyte pH, achieved in a BES.
(v) the type of membrane, and (vi) the equilibria of other ions While all current nitrogen removal technologies require
at the anode and cathode. Many of these factors are interre- energy for the removal of nitrogen gas mainly through aera-
lated, e.g. the current density determines the catholyte pH63 tion, BESs, though not applied in practice yet, are a promis-
and is in turn dependent on the type of membrane and the ing technology for energy-efficient ammonia recovery. The
ions present in solution.48 These interactions should be stud- main reason for the low-energy requirement for MFCs and
ied in more detail to clarify how the removal efficiency and MECs, or even energy recovery, is the fact that no oxygen is
ammonium recovery can be improved. It has been shown required to oxidize the ammonium to nitrate or nitrite. Instead,
that removing the ammonium/ammonia batch-wise from the the movement of electrons from anode to cathode drives the
catholyte by replenishing the catholyte results in higher transport and recovery of ammonium at the cathode.
ammonium removal rates.39 In a continuous setup, removal The next step is to bring BESs in general, and also specifi-
of ammonium can be achieved by stripping, where the solu- cally for the application of nitrogen recovery, to a larger scale.
ble ammonia evaporates to gaseous ammonia by contact with A recent review article summarizes all the work performed
a N 2 or H 2 gas stream and subsequently absorbed in until now on scaling-up of MFCs.65 Their major observations
sulphuric acid, as has been done in the electrochemical are that in terms of design, both tubular and flat-plate sys-
ammonium recovery process.30 Up until now, such a system tems still suffer from too high internal resistance. The main
has not been tested and the performance of a BES connected causes for these high internal resistances are that the
to a stripper, and the maximum achievable ammonia recov- electrode spacing is too high, electrode materials have lim-
ery, needs to be determined. Another approach to understand ited conductivity, and contact between electrodes and current
the processes that determine ammonium transport is model- collectors is often not optimal. They point out that separa-
ling. Dykstra et al. (2014) derived a one-dimensional steady- tors, like membranes, are crucial to obtain high treatment
state model of the urine MEC used by Kuntke et al. (2014).64 efficiency, although separators also increase the total internal
The model includes the transport of ions through the mem- resistance. Janicek et al. (2014) stress that waste streams with
brane and allowed us to identify one of the main limiting fac- high organic concentrations are likely to generate higher per-
tors of the system, which is the inert gas flow along the formance,65 although the drawback is that COD removal is
cathode. It was concluded that a higher N2 flow or a decrease generally lower, and as a result, treatment efficiencies are
in pressure in the cathode chamber was needed to increase limited, when a single system is used. They conclude that
ammonia recovery. Modelling the system gave valuable pilot studies are essential to demonstrate the practical feasi-
insight and understanding of its performance. In urine, COD bility of BESs.
concentrations are approximately 10 g L 1, and ammonium In 2013, Wetsus has set up a pilot BES at the water board
concentrations are approximately 9 g L 1. Because ideally of Frysln located in Leeuwarden, The Netherlands in cooper-
0.57 kg of COD is required for the removal of 1 kg N, urine ation with partners from industry. The objective of this pilot
contains sufficient COD to recover all the ammonium, and experiment is to purify urine by removing the COD and
no additional carbon source is required. In this ideal case, ammonium and recover energy in the form of hydrogen, in

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014
View Article Online

Environmental Science: Water Research & Technology Perspective

addition to ammonia gas. This installation consists of 4 flat- 11 K. J. J. Steinbusch, H. V. M. Hamelers, J. D. Schaap,
plate cells that are stacked in parallel with a total surface C. Kampman and C. J. N. Buisman, Environ. Sci. Technol.,
area of 0.16 m2. With this pilot, we will demonstrate the fea- 2009, 44, 513517.
sibility of on-site treatment of urine and conversion into 12 M. C. A. A. Van Eerten-Jansen, A. Ter Heijne,
ammonium and hydrogen gas. T. I. M. Grootscholten, K. J. J. Steinbusch,
T. H. J. A. Sleutels, H. V. M. Hamelers and C. J. N. Buisman,
Acknowledgements ACS Sustainable Chem. Eng., 2013, 1, 10691069.
13 P. Kuntke, K. M. miech, H. Bruning, G. Zeeman, M. Saakes,
This work was performed in the cooperation framework of T. H. J. A. Sleutels, H. V. M. Hamelers and C. J. N. Buisman,
Wetsus, Centre of Excellence for Sustainable Water Technol- Water Res., 2012, 46, 26272636.
ogy (www.wetsus.nl). Wetsus is co-funded by the Dutch Minis- 14 P. Kuntke, M. Geleji, H. Bruning, G. Zeeman,
try of Economic Affairs and Ministry of Infrastructure and H. V. M. Hamelers and C. J. N. Buisman, Bioresour. Technol.,
Environment, the European Union Regional Development 2011, 102, 43764382.
Fund, the Province of Frysln, and the Northern Netherlands 15 P. T. Kelly and Z. He, Bioresour. Technol., 2014, 153, 351360.
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

Provinces. The authors would like to thank the participants of 16 T. H. J. A. Sleutels, A. Ter Heijne, C. J. N. Buisman and
the research theme Resource Recovery for the fruitful dis- H. V. M. Hamelers, ChemSusChem, 2012, 5, 10121019.
cussions and their financial support. This research has 17 J. L. Barnard, Elimination of eutrophication through resource
received funding from the European Union's Seventh recovery, in Proceedings of International Conference on
Programme for research, technological development and Nutrient Recovery from Wastewater Streams, ed. D. Mavinic,
demonstration under grant agreement no. 308535. K. Ashley and F. Koch, IWA publishing, London, 2009,
pp. 122.
References 18 G. Tchobanoglous, F. L. Burton and H. D. Stensel,
Wastewater engineering: treatment and reuse, McGraw-Hill,
1 US Bureau Census, World Population, http://www.census. New York, 4th edn, International Edition, 2004.
gov/population/international/data/worldpop/table_ 19 M. S. M. Jetten, I. Cirpus, B. Kartal, L. van Niftrik,
population.php (accessed May 2014). K. T. van de Pas-Schoonen, O. Sliekers, S. Haaijer,
2 UN, World population projected to reach 9.6 billion by 2050 W. van der Star, M. Schmid, J. van de Vossenberg,
with most growth in developing regions, especially Africa I. Schmidt, H. Harhangi, M. van Loosdrecht, J. G. Kuenen,
says UN, http://esa.un.org/unpd/wpp/Documentation/pdf/ H. O. den Camp and M. Strous, Biochem. Soc. Trans., 2005,
WPP2012_Press_Release.pdf (accessed May 2014). 33, 119123.
3 J. Rockstrom, W. Steffen, K. Noone, A. Persson, F. S. Chapin, 20 L. G. J. M. Dongen, M. S. M. Jetten, M. C. M. van Loosdrecht
E. F. Lambin, T. M. Lenton, M. Scheffer, C. Folke, and K. Kujawa-Roeleveld, The combined Sharon/Anammox
H. J. Schellnhuber, B. Nykvist, C. A. de Wit, T. Hughes, process: a sustainable method for N-removal from sludge
S. van der Leeuw, H. Rodhe, S. Sorlin, P. K. Snyder, water, IWA Publishing, London, 2001.
R. Costanza, U. Svedin, M. Falkenmark, L. Karlberg, 21 U. van Dongen, M. S. M. Jetten and M. C. M. van Loosdrecht,
R. W. Corell, V. J. Fabry, J. Hansen, B. Walker, D. Liverman, Water Sci. Technol., 2001, 44, 153160.
K. Richardson, P. Crutzen and J. A. Foley, Nature, 2009, 461, 22 M. S. M. Jetten, M. Wagner, J. Fuerst, M. van Loosdrecht,
472475. G. Kuenen and M. Strous, Curr. Opin. Biotechnol., 2001, 12,
4 M. T. Madigan, J. M. Martinko and J. Parker, Brock biology 283288.
of microorganisms, Prentice Hall, Upper Saddle River, NJ, 23 Y. D. Scherson, G. F. Wells, S.-G. Woo, J. Lee, J. Park,
9th edn, 2000. B. J. Cantwell and C. S. Criddle, Energy Environ. Sci., 2013, 6,
5 M. Kitano, Y. Inoue, Y. Yamazaki, F. Hayashi, S. Kanbara, 241248.
S. Matsuishi, T. Yokoyama, S. W. Kim, M. Hara and 24 A. ter Heijne, H. V. M. Hamelers, V. de Wilde,
H. Hosono, Nat. Chem., 2012, 4, 934940. R. A. Rozendal and C. J. N. Buisman, Environ. Sci. Technol.,
6 A. M. Leach, J. N. Galloway, A. Bleeker, J. Willem Erisman, 2006, 40, 52005205.
R. Kohn and J. Kitzes, Environ. Dev., 2012, 1, 4066. 25 A. Ter Heijne, F. Liu, R. van der Weijden, J. Weijma,
7 S. Cheng, D. Xing, D. F. Call and B. E. Logan, Environ. Sci. C. J. N. Buisman and H. V. M. Hamelers, Environ. Sci.
Technol., 2009, 43, 39533958. Technol., 2010, 44, 43764381.
8 B. E. Logan, D. Call, S. Cheng, H. V. M. Hamelers, 26 F. Zhao, F. Harnisch, U. Schrder, F. Scholz, P. Bogdanoff
T. H. J. A. Sleutels, A. W. Jeremiasse and R. A. Rozendal, and I. Herrmann, Environ. Sci. Technol., 2006, 40,
Environ. Sci. Technol., 2008, 42, 86308640. 51935199.
9 B. E. Logan, B. Hamelers, R. A. Rozendal, U. Schrder, 27 H. V. M. Hamelers, A. Ter Heijne, T. H. J. A. Sleutels,
J. Keller, S. Freguia, P. Aelterman, W. Verstraete and A. W. Jeremiasse, D. P. B. T. B. Strik and C. J. N. Buisman,
K. Rabaey, Environ. Sci. Technol., 2006, 40, 51815192. Appl. Microbiol. Biotechnol., 2010, 85, 16731685.
10 R. A. Rozendal, E. Leone, J. Keller and K. Rabaey, 28 H. Liu, S. Grot and B. E. Logan, Environ. Sci. Technol., 2005,
Electrochem. Commun., 2009, 11, 17521755. 39, 43174320.

This journal is The Royal Society of Chemistry 2014 Environ. Sci.: Water Res. Technol.
View Article Online

Perspective Environmental Science: Water Research & Technology

29 R. A. Rozendal, H. V. M. Hamelers, G. J. W. Euverink, 49 R. Cord-Ruwisch, Y. Law and K. Y. Cheng, Bioresour.


S. J. Metz and C. J. N. Buisman, Int. J. Hydrogen Energy, Technol., 2011, 102, 96919696.
2006, 31, 16321640. 50 K. Y. Cheng, A. H. Kaksonen and R. Cord-Ruwisch,
30 J. Desloover, A. Abate Woldeyohannis, W. Verstraete, Bioresour. Technol., 2013, 143, 2531.
N. Boon and K. Rabaey, Environ. Sci. Technol., 2012, 46, 51 T. A. Larsen and W. Gujer, Water Sci. Technol., 1996, 34,
1220912216. 8794.
31 M. Maurer, P. Schwegler and T. A. Larsen, Water Sci. 52 H. L. T. Mobley and R. P. Hausinger, Microbiol. Rev.,
Technol., 2003, 48, 3746. 1989, 53, 85108.
32 K. Diem and C. Lentner, Scientific tables, Ciba-Geigy 53 K. M. Udert, T. A. Larsen, M. Biebow and W. Gujer, Water
Limited, Basle, 7th edn, 1970. Res., 2003, 37, 25712582.
33 P. Kuntke, Ph.D. Thesis, Wageningen University, 2013. 54 E. Volcke, K. Villez, S. Van Hulle, M. van Loosdrecht and
34 M. Maurer, W. Pronk and T. A. Larsen, Water Res., 2006, 40, P. Vanrolleghem, Afvalwaterwetenschap, 2004, 3, 297318.
31513166. 55 A. Fuerte, R. X. Valenzuela, M. J. Escudero and L. Daza,
35 J. Wilsenach and M. van Loosdrecht, Separate urine J. Power Sources, 2009, 192, 170174.
Published on 05 November 2014. Downloaded on 18/12/2014 20:48:13.

collection and treatment; option for sustainable wastewater 56 U.S. Department of Energy, Hydrogen Analysis Resource
systems and mineral recovery, 2002. Center, http://hydrogen.pnl.gov/cocoon/morf/hydrogen/site_
36 Z. He, J. Kan, Y. Wang, Y. Huang, F. Mansfeld and specific/fuel_heating_calculator?canprint=false (accessed
K. H. Nealson, Environ. Sci. Technol., 2009, 43, 33913397. May 2014).
37 J. R. Kim, Y. Zuo, J. M. Regan and B. E. Logan, Biotechnol. 57 V. Hacker and K. Kordesch, in Handbook of fuel cells-
Bioeng., 2008, 99, 11201127. Fundamentals, technology and applications, ed. W. Vielstich,
38 G.-L. Zang, G.-P. Sheng, W.-W. Li, Z.-H. Tong, R. J. Zeng, C. Shi A. Lamm and H. A. Gasteiger, John Wiley & Sons,
and H.-Q. Yu, Phys. Chem. Chem. Phys., 2012, 14, 1978. Chichester, 2003, vol. 3, pp. 121127.
39 P. Kuntke, T. H. J. A. Sleutels, M. Saakes and C. J. N. Buisman, 58 Centraal Bureau voor de Statistiek, Aardgas en elektriciteit,
Int. J. Hydrogen Energy, 2014, 39, 47714778. gemiddelde prijzen van eindverbruikers, http://statline.cbs.
40 P. Clauwaert, K. Rabaey, P. Aelterman, L. De Schamphelaire, nl/StatWeb/publication/?VW=T&DM=SLNL&PA=81309NED&D1=
T. H. Pham, P. Boeckx, N. Boon and W. Verstraete, Environ. 1,3,5,8,11,15&D2=0&D3=l&D4=0-3,5-8,10-13,15-18,20-23,l&HD=
Sci. Technol., 2007, 41, 33543360. 120813-1059&HDR=T&STB=G2,G1,G3 (accessed May 2014).
41 B. Virdis, K. L. Rabaey, Z. Yuan and J. Keller, Water Res., 59 International Energy Agency, Hydrogen Production &
2008, 42, 30133024. Distribution, http://www.iea.org/techno/essentials5.pdf
42 B. Virdis, K. Rabaey, R. A. Rozendal, Z. Yuan and J. Keller, (accessed June 2014).
Water Res., 2010, 44, 29702980. 60 J. W. Post, Ph.D. Thesis, Wageningen University, 2009.
43 F. Zhang and Z. He, Process Biochem., 2012, 47, 21462151. 61 S. Aiyuk, I. Forrez, D. K. Lieven, A. van Haandel and
44 H. Yan, T. Saito and J. M. Regan, Water Res., 2012, 46, W. Verstraete, Bioresour. Technol., 2006, 97, 22252241.
22152224. 62 S. J. Kang, K. Olmstead, K. Takacs and J. Collins, Municipal
45 S. Haddadi, E. Elbeshbishy and H.-S. Lee, Bioresour. Nutrient Removal Technologies Reference Document, U.S.
Technol., 2013, 142, 562569. Environmental Protection Agency, 2008.
46 R. A. Rozendal, H. V. M. Hamelers and C. J. N. Buisman, 63 T. H. J. A. Sleutels, A. Ter Heijne, C. J. N. Buisman and
Environ. Sci. Technol., 2006, 40, 52065211. H. V. M. Hamelers, Int. J. Hydrogen Energy, 2013, 38,
47 R. A. Rozendal, T. H. J. A. Sleutels, H. V. M. Hamelers and 72017208.
C. J. N. Buisman, Water Sci. Technol., 2008, 57, 17571762. 64 J. E. Dykstra, P. M. Biesheuvel, H. Bruning and A. Ter Heijne,
48 T. H. J. A. Sleutels, H. V. M. Hamelers, R. A. Rozendal and Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys., 2014, 90.
C. J. N. Buisman, Int. J. Hydrogen Energy, 2009, 34, 36123620. 65 A. Janicek, Y. Fan and H. Liu, Biofuels, 2014, 5, 7992.

Environ. Sci.: Water Res. Technol. This journal is The Royal Society of Chemistry 2014

Anda mungkin juga menyukai