You are on page 1of 31

Accepted Manuscript

Employing Microbial Eelectrochemical Technology-driven electro-Fenton ox-


idation for the removal of recalcitrant organics from sanitary landfill leachate

Muhammad Hassan, Narcis Pous, Bing Xie, Jess Colprim, M. Dolors Balaguer,
Sebastia Puig

PII: S0960-8524(17)31136-7
DOI: http://dx.doi.org/10.1016/j.biortech.2017.07.042
Reference: BITE 18462

To appear in: Bioresource Technology

Received Date: 14 May 2017


Revised Date: 3 July 2017
Accepted Date: 6 July 2017

Please cite this article as: Hassan, M., Pous, N., Xie, B., Colprim, J., Balaguer, M.D., Puig, S., Employing Microbial
Eelectrochemical Technology-driven electro-Fenton oxidation for the removal of recalcitrant organics from sanitary
landfill leachate, Bioresource Technology (2017), doi: http://dx.doi.org/10.1016/j.biortech.2017.07.042

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers
we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and
review of the resulting proof before it is published in its final form. Please note that during the production process
errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Employing Microbial Eelectrochemical Technology-driven electro-
Fenton oxidation for the removal of recalcitrant organics from
sanitary landfill leachate

Muhammad Hassana,b, Narcis Pousa, Bing Xieb, Jess Colprima, M. Dolors Balaguera,
Sebastia Puiga*

a
LEQUiA, Institute of the Environment, University of Girona, C/Maria Aurelia
Company, 69, Facultat de Ciencies, E-17003 Girona, Spain
b
Shanghai Key Laboratory for Urban Ecological Process and Eco-Restoration, School
of Ecology & Environmental Science, East China Normal University Shanghai 200241,
China

* Corresponding author, E-mail: sebastia@lequia.udg.cat

Intended for: Bioresource Technology

Type of contribution: Research Article

Total number of References: 38

Number of Figures: 3

Number of Tables: 5

Abstract
1
The feasibility of employing Microbial Electrochemical Technology (MET)-driven

electro-Fenton oxidation was evaluated as a post-treatment of an anammox system

treating sanitary landfill leachate. Two different MET configuration systems were

operated using effluent form partial nitrification-anammox reactor treating leachate. In

spite of the low organic matter biodegradability of the anammoxs effluent (2401562

mg COD L-1; 23757 mg BOD5 L-1), the technology was capable to reach COD

removal rates of 1077-1244 mg L-1 d1 with concomitant renewable electricity

production (43.52.1 Am-3NCC). The operation in continuous mode versus batch mode

reinforced the removal capacity of the technology. The recirculation of acidic catholyte

into anode chamber hindered the anodic efficiency due to pH stress on anodic

electricigens. The obtained results demonstrated that the integrated system is a

potentially applicable process to deal with bio-recalcitrant compounds present in mature

landfill leachate.

Key words: Advanced Oxidation Processes; Anammox; Electricity production;

Hydroxyl radicals; Recalcitrant organics

1. Introduction

Landfill leachate contains wide variety of recalcitrant compounds that hardens

its treatment using conventional techniques. Several biological and physico-chemical


2
processes have been practiced to treat landfill leachate for the last few decades.

Biological processes are effectively employed to remove organic matter and nitrogen

from leachate. However, it is hindered by the presence of recalcitrant compounds

especially in old leachate, and it is difficult to achieve high nitrogen removal with a low

C/N ratio using conventional nitrification/denitrification process, as it requires

additional carbon source which makes the treatment systems complicated and expensive

(Hassan et al., 2016b; Muller et al., 2015). Anaerobic ammonium oxidation (anammox)

process is an alternative to remove nitrogen which does not need external carbon source

and reduces considerably the air supplied with the consequent cost reduction (Shi et al.,

2013). Therefore, it can effectively treat mature landfill leachate but limited for the

organic matter removal (Anfruns et al., 2013). Among the chemical methods, advanced
-
oxidation processes (AOPs), such as use of certain oxidants (O3, H2O2, S2O82 ),

catalysts/electrocatalysts (TiO2, ZnO, Fe2+) and their combination have been reported in

the literature to be used to enhance the biodegradability of mature leachate (Anfruns et

al., 2013; Elmolla and Chaudhuri, 2010; Hassan et al., 2016a; Xie et al., 2013; Zhang et

al., 2006).

The chemical Fenton process has been widely investigated for degradation of

biodegradable and recalcitrant organics. Certain radicals like hydroxyl (OH),

hydroperoxy (OH2) or superoxide (O2) radicals from reaction of H2O2 with Fe2+ and

Fe3+ are generated during Fenton oxidation process in an acidic medium according to

Eqs. 1-3. (Brillas et al. 2009). Superoxide (O2) radical can be formed (Eq. 4) due to

one-electron reduction of oxygen followed by formation of H2O2 (Vinogradov and

Grivennikova, 2005).

Fe2+ + H2O2 Fe3+ + OH + OH- (1)

Fe3+ + H2O2 Fe2+ + HO 2 + H+ (2)

H2O2 + OH H2O + HO2 (3)


3
HO2 H+ + O2 (4)

The main limitations in terms of operational and economic issues include

transportation and storage of H2O2, cost and pH modulation (Feng et al., 2010). As

compared to conventional Fenton oxidation, electro-Fenton process is considered as

more efficient option (Brillas et al., 2009), however the main drawback of EF process is

the formation of final products like Fe (III)-carboxylate complexes that are quite

difficult to degrade even by OH radicals (Brillas and Sirs, 2015). This limitation can

be overcome by photo-EF (Garcia-Segura and Brillas, 2016) but it increases the energy

costs making the process less economical.

Recently, several studies have been furnished, revealing the feasibility of

coupling Microbial Electrochemical Technology (MET) and electro Fenton-based

AOPs to remove refractory organic matter and in situ hydrogen peroxide (H2O2)

production (Feng et al., 2010; Wang et al., 2014; Zhuang et al., 2010). In literature, this

process (MET-driven electro - Fenton oxidation) was also named as a bioelectro-

Fenton (BEF) technology (Feng et al., 2010). In this process, the oxidation of organic

compounds in the bioanode releases electrons, which are transferred to the cathode via

external wire where they are consumed to reduce an electron acceptor, commonly

oxygen. It results in H2O2 synthesis by a two-electron transfer reaction according to Eq.

(5).

-
O2 + 2H+ + 2e H2O2 (5)

In a previous study (Anfruns et al., 2013) the combination of a partial nitiration-

anammox system coupled with two AOP -based technologies (coagulation/flocculation

+ ozonation and photo-Fenton) were assessed in terms of nitrogen and carbon removal

for mature landfill leachate treatment. Higher removal efficiencies with lower doses of

4
reagents were obtained by applying a biological treatment prior to treatment with AOP-

based technologies.

A new configuration based on anammox followed by a BEF was proposed. The

schematic of the integrated system is given in Fig. 1. The purpose of this study was to

evaluate the robustness, reliability and resilience of the BEF, which consisted of anodic

bio-oxidation coupled with cathodic electro-Fenton where H2O2 is produced in situ in

the presence of iron catalysts thereby partially oxidizing the recalcitrant organics

present in the effluent of anammox reactor.

<Figure 1>

2. Materials and Methods

2.1. Landfill leachate

Sanitary landfill leachate was collected from the Oris urban landfill site (Osona,

Catalonia - Spain) and stored in 1000 L outdoor tanks at the University of Girona

facilities. The raw leachate presented a high concentration of nitrogen content and

recalcitrant organic pollutants. The leachate was firstly treated in a partial

nitritation/anammox system installed at the University of Girona (Spain), which was

mostly employed for nitrogen content removal from sanitary landfill leachate. Table 1

presents the mean values ( standard deviation) of the main physico - chemical

characteristics of effluent of the anammox reactor treating landfill leachate. The


-1 -1
leachate contained 2401 562 mg COD L and 237 57 mg BOD5 L , depicting low

biodegradability of the organic matter. The leachate showed a dark brown colour and

high values of UV254 (24.058.42), attributed to the presence of dissolved organic

matter, specifically those that contain aromatic rings or unsaturated bonds (double and

triple) in their molecular structures (e.g humic and fulvic acids) (Baun and Christensen,

5
-1
2004). A low concentration of NH4+-N (76.2554.87 mg L ) was noticed in the treated

leachate because it was overwhelmingly degraded by anammox SBR (Ruscalleda et al.,

2008). The pH was 7.6 1.8 due to the pH control required for the anammox process in

the anammox SBR (Ruscalleda et al., 2008). The high conductivity of 32.04.2 mS cm

1
was as a result of high concentrations of inorganic ions, such as Na+, Cl, Ca2+ and K+

in the samples.

<Table 1>

2.3. Experimental Setup

Two double-chambered rectangular-shaped MET systems (RR-1 and RR-2)

similar to Pous et al. (Pous et al., 2013), were employed. The systems were built using

two methacrylate frames (200 mm 22 mm) separated by cation exchange membrane

(20 20 cm, CMI-7000, Membranes Int., USA). The cathode in reactor 1 (RR-1)

contained stainless steel (SS) wire mesh (18 18 cm, Mersen Iberica, Spain) and SS

rod (250 mm 6 mm) as current collector, whereas anode was furnished with two

layers of granular activated carbon (GAC) + graphite granules (1.5-5 mm diameter,

EnViro-cell, Germany) embedded between SS wire meshes alternatively. Graphite rod

(250 mm 6 mm, Mersen Iberica, Spain) was used as current collector. The cathode

and anode of system 2 (RR-2) consist of GAC coupled with graphite rods, each as

current collectors. The net anodic compartment (NAC) and net cathodic compartment

(NCC) volumes were 600 and 500 mL, respectively. The cathode potential (i.e. working

electrode) was poised at two different potentials i.e. -0.7 and -1.0 V vs Ag/AgCl (RE-

5B, BASI, United Kingdom) by a homemade potentiostat built according to Ref.

(Friedman et al., 2012). Magnetic stirrers placed in the stock solution bottles agitated

the anolyte and catholyte solutions. However in continuous mode operation the anolyte

and catholyte was in a flow mode (i.e. in and out directly). Experiments were performed

6
at room temperature (254 C) and ambient atmospheric pressure. The schematic

representation of the experimental set-up and reaction mechanism of anode and cathode

chamber was shown in Fig. 1.

2.4. Operation of the MET systems

Table 2 shows the various conditions and tests applied in RR-1 and RR-2. Both

systems were initially inoculated with 20 mL of the effluent (as source of electroactive

bacteria) obtained from a MFC reactor previously run for more than 3 months. During

the start-up period (day 1-11), the system was run in batch mode having glucose
-1
substrate (0.8 g L ) and phosphate buffered solution (PBS) described elsewhere

(Fernndez de Dios et al., 2013) as anolyte, and effluent from the anammox reactor

treating landfill leachate henceforward named LL, as catholyte. The proportion of

anolyte was changed to 1:1 ratio of glucose/yeast extract medium and LL, henceforth

called GLL (day12-18) followed by 100% pre treated leachate (LL) as anolyte (day 19-

35), employing only LL as catholyte in both cases. The pH of catholyte was adjusted to

3.0 using 1N HCl and/or NaOH, as literature suggested a pH between 2 and 4 effective

for Fentons reagent and overall organics removal (Zhang et al., 2005). The anolyte was

fed without any pH adjustment (7.61.8).

The batch mode operation (day 1-11) at cathode potential of -0.7 and -0.9 V vs

Ag/AgCl was switched to continuous mode (day 12-27) and finally to recirculation

mode (day 28-35) at -1.0 V poised potential vs Ag/AgCl. In recirculation mode,

catholyte with acidic pH were fed to anode chamber as anolyte in order to enhance the

organic removal rates. The catholyte was furnished with 300 mg L-1 FeSO4 as Fenton

catalyst during the whole experiment for electro-Fenton process, whereas air was

continuously bubbled in the catholyte stock solution bottles before each run. The

purpose of comparison of RR-1 and RR-2 under bath and continuous mode operation

7
was to evaluate the overall efficiency (current density, pollutants removal, coulombic

efficiency etc.) of different electrode materials used in the reactors.

<Table 2>

2.5 Analytical determinations and calculations

The treatments were evaluated by analyzing the following major parameters:

chemical oxygen demand (COD; APHA standard method 5220B), biochemical oxygen

demand (BOD; WTW, Oxi Top), total organic carbon (TOC; Shimadzu TOC-VCSH

analyzer), ammonium (BUCHI B-324 distiller, Titrino 719S Methrohm) and total

Kjeldahl nitrogen (BUCHI B-324 distiller, Titrino 719S Methrohm). Nitrites (NO2-N),

nitrates (NO3-N), and phosphates (PO43-P) and other organic and inorganic ions were

determined by ion chromatography in a Dionex (ICS-2100 LC, APHA standard method

4110B). The pH and conductivity were measured with a pH-meter (pH-meter basic

20+, Crison, Spain) and an EC-meter (EC-meter basic 30+, Crison, Spain), respectively.

All UV-Vis measurements including UV254 were carried out using a spectrophotometer

(CECIL-1000 SERIES, Thermo Scientific). Using the same spectrophotometer, H2O2

content was assessed by photometric measurements at 410 nm (UV410) using a

commercial solution of titanium IV oxysulfate. All samples were measured in duplicate

except TOC.

The anodic coulombic efficiency (CE) in batch and continuous mode were

calculated according to Eqs. (6 and 7).

(for batch mode operations) (Eq 6)

(for continuous mode operations under steady

conditions) (Eq 7)

8
where, F is Faradays constant (96485 C mol1), Va is the anolyte volume (L), Qq is the

influent flow rate (L s1), is the difference of influent COD to effluent COD (mg

L-1) and t is the time interval during which CE is calculated (s).

3. Results and discussion

3.1. Leachate treatment through anodic bio-oxidation

Both MET systems (RR-1 and RR-2) were initially run using glucose substrate

to acclimatize the bioanode in batch mode (test 1). Once stable current production
3
(11.83.7 and 4.73.2 A m NCC in RR-1 and RR-2, respectively) was reached in one

week the influent was changed to introduce the effluent of anammox reactor and

different operation conditions were tested in the anode chambers (test 2). Table 3

summarizes the results of anodic performance at various operating conditions. As a

general trend, the current density was quite higher in RR-1 than RR-2. It might be due

to the electrode material of RR-1 (SS, stainless steel), which has a better conductivity

than material of RR-2 (GAC, granular activated carbon). The SS shape favored better

substrate distribution (Vil-Rovira et al., 2015). Moreover, the SS wire mesh cathode

also provided good conductivity. In RR-1, a maximum current density of 24.43.7 A


3
m NCC was obtained during 11days of operation (CE 26.2%). Interestingly, the current


density rose to 43.5 2.1 A m 3 (CE 29.33.9%) when the system was switched to


continuous mode at a volumetric influent flow rate of 0.5 L d 1 using GLL. This is in

accordance with Puig et al., (2011) where power output increased when the system was

switched to continuous mode using raw leachate. The current density in RR1 dropped
-
to 34.71.3 A m 3NCC (CE 22.44.2%) when 100% leachate was used as substrate. The

leachate having certain recalcitrant organics is difficult to degrade easily by

electrogenic bacteria; and as a consequence the current density was reduced. Similar

trend was observed for RR-2. In batch mode, the current density attained was

9
-
16.53.5Am 3 (CE 4.7%) using GLL. It increased to 26.82.1 A m 3NCC at continuous

-
mode but later fell down sharply and stabilized at 17.41.0 A m 3NCC upon replenishing

with 100% pre-treated leachate in the subsequent period (day 22-35).

<Table 3>

Fig. 2 presents the anolyte COD removal over time and summarizes results of

anodic removal rate at various operating conditions in both MET systems. The COD
- -
removal rate in RR-1 was 279 76 (test 1) and 33040 mg COD L 1 d 1 (test 2)

operating in batch mode from an initial concentration of 1753 180 and 2016 169 mg
-
L 1 (Table 3). In continuous mode, a huge increase of COD removal rate was revealed

- -
achieving an average value of 1244126 mg COD L 1 d 1 with a CE of 29.33.9% using

GLL as carbon source at 2.020.07 g CODL-1d-1 of OLR. When 100% pre-treated

- -
leachate was fed, COD abatement rate declined to 88391 mg COD L 1 d 1 having CE

- -
of 22.35.2%. The COD removal rate further declined to 549265 mg COD L 1 d 1

during the loop recirculation mode i.e. recirculation of catholyte into anode chamber. It

was due to the acidic pH (ca. 4.81.3, Test 5) of anolyte, which is unfavorable for the

anodic microbial community (Fig. 2). In contrast to non-bio electrochemical systems, a

near-neutral pH is required for the bioanode and thus, a decrease of anodic pH would

lead to a severe loss of biological activity (Rago et al., 2015).

<Figure 2>

In RR-2, the current density, CE and organics removal were slightly lower than

RR-1 batch mode with glucose substrate (Figure 2). In the batch mode with GLL, the
- -
COD removal rate was 33845 mg L 1 d 1 (GLL) with CE of 7.4% at poised potential of

-0.9 V vs Ag/AgCl. The low coulombic efficiencies implied that the electron-transfer

10
bacteria were incapable of converting all the available carbon fuel into electricity (He et

al., 2005). In continuous system with GLL substrate, the CE was 10.1 1.3% with 1077
-
60 mg L 1 d 1 COD reduction from an initial concentration of 2016 169 mg COD L-

1 -
. The COD removal declined sharply to 59733 mg L 1.d (9.52.1% CE) using 100%

LL in continuous operation having initial concentration of 2704142 mg COD L-1

(Table 4). The low CEs at the anode might be attributed to several reasons. First, MFCs

fueled with simple substrates such as acetate, glucose, sucrose etc. typically exhibit

higher efficiencies than those fueled with complex substrates (Reimers et al., 2007) like

landfill leachate which usually contains recalcitrant organics. Secondly, oxygen

diffusion from the cathode into the anode chamber especially in continuous mode of

operation cannot be neglected which may pose negative impact on CE (Xu et al., 2011).

<Table 4>

In order to evaluate the capability of the described systems to remove

recalcitrant organic matter, two parameters were considered: TOC and UV254. UV254 is

a quality parameter directly related to the presence of aromatic and unsaturated

compounds. No UV254 concentration was present in both METs when glucose was used

as substrate (test 1) however UV254 removal improved with time in batch (day 8-11) and

continued its increasing removal trend even in continuous mode (day 18 and 27)

followed by a slight decline (Fig. S1). After further slip down on day 29, it enhanced on

subsequent days (ca. day 31-35).

The removal of TOC is also of great importance during the electrochemical

degradation of wastewater containing organic pollutants, because it indicates the extent

of mineralization (Rajkumar et al., 2005). As shown in Table 3, a TOC degradation rate


- -
of 10521 mg L 1 d 1 occurred in RR-1 from an initial concentration of 75953 mg TOC

- -
L 1 in batch with GLL; whereas 10448 mg TOC L 1 d 1 was removed in RR-2. In

11
continuous mode with GLL substrate, the abatement trend declined but stabilized at
- -
32723 mg TOC L 1 d 1 (RR-1) and 20812 (RR-2), which further declined to 28837

- - - -
mg L 1 d 1 (RR-1) and 15148 mg L 1 d 1 (RR-2) upon employing 100% leachate

followed by negligible reduction rate due to loop recirculation on day 29 at initial


- -
concentration of 896157 mg TOC L 1 d 1 due to acidic anolyte pH. Later, the removal

- -
rate gradually increased up to 126 and 156 mg TOC L 1 d 1 in RR-1 and RR-2,

respectively upon acclimation of anodic bacteria to acidic pH (Fig. S2). The high

current density promoted overall direct anodic oxidation of TOC in RR-1. A similar

trend happened in terms of UV254 removal as well, verifying better bioanodic activity,

except day 1-7 (test 1), where no aromatic compounds were present in glucose

substrate.

3.2. Leachate treatment through cathodic bioelectro - Fenton oxidation

The removal of organics in catholyte depends on electrochemically produced

H2O2 concentration and subsequent OH radicals (the reaction mechanism is elaborated

in Fig. 1). However, a higher rate and greater generation of H2O2 could be made

possible at a relatively higher current density. The higher current densities in RR-1 than

RR-2 affected the residual H2O2 yield as well. However, in loop recirculation mode, an

abrupt increment in residual H2O2 occurred, as can be seen in Table 3 (test 5). The high

catholyte effluent pH of 7 in test 5 forced the amount of soluble iron to decrease by

precipitation, resulting higher residual H2O2 concentration (Zhang et al., 2006). The

abrupt accumulation of residual H2O2 concentration in loop recirculation mode hindered

the catholyte COD and TOC removal trend (Fig. 3), indicating a lower organic matter

oxidation in accordance with Beltran de Heredia et al., (2005).

Although RR-1 performed well in terms of current density, coulombic efficiency

and anodic pollutant removal but cathodic pollutant removal was comparatively better

12
in RR-2 (Table 4). The reason might be the high adsorption capability of GAC in RR-2

owing to its high surface area (579.2 m2 g 1), which enhanced the cathodic COD

removal efficiency accordingly. As shown in Table 4, the COD removal in batch mode

was 254 60 and 28973 mg L 1 d 1 in RR-1 and RR-2, respectively. In continuous

-
mode (day 15-27), the removal rate was stable i.e. 926 90 and mg COD L 1 d 1 in RR-

1 while 1110 38 and in RR-2. This trend declined (82014 in RR-1 and 75455 mg
- -
COD L 1 d 1 in RR-2) when the anode chambers were replenished with 100% pre-

treated leachate as fuel, which ultimately affected the cathodic performance. The COD

abatement declined to almost negligible amount during day 29 (loop recirculation of

acidic catholyte into anode) owing to certain pH stress on anodic electricigens, which

tremendously affected the cathodic efficiency (Fig. 3). Similar trend was observed for

cathodic TOC removal (Fig. S3). The pH value of catholyte (pH 3) was closely related

to the reactions responsible for the generation of H2O2, Fe2+ OH and other radicals

according to Eqs (1 - 5), and eventually the efficiency of Fenton reaction.

<Figure 3>

The degradation of catholyte UV254 was most probably due to the oxidation of

aromatic and unsaturated sites by hydroxyl radicals produced (Liu et al., 2004). From an

initial concentration of 24.43.2 mg UV254 L-1, 318% (batch), 3710% (continuous)

and 225% (recirculation) of UV254 was removed in RR-1; whereas, 417% (batch),

519% (continuous) and only 55% (recirculation) was abated in RR-2 (Fig. S4). These

results are evident that MET-driven electro-Fenton has capability to remove recalcitrant

organics from cathode compartment. Further improvements might be possible based on

electrode material selection, provision of appropriate cathodic conditions and reactor

design.

3.3. Dealing with complex substrates in MET systems

13
In this section, we aim to compare the current work with the results reported in

literature about complex substrates treatment in MET systems and Fenton oxidation.

The similarities and/or differences in terms of COD removal and coulombic efficiencies

are because of variations in parameters such as mode of operation, nature and strength

of the wastewaters, poised potentials, size and reactor design etc.

As shown in Table 5, wide varieties of wastewaters have been dealt with MET

systems such as brewery, dairy, swine, domestic, landfill leachate, medicinal herbs

wastewater. This is an emerging process for treating complex pollutants in wastewaters

and power generation. Complex wastewaters contain refractory substances, toxic

pollutants, volatile organic compounds, heavy metals, colour etc. Some wastewaters

like leachate might be considered a good feedstock for MET systems owing to its

relatively high conductivity, buffering capacity and minimal solids but studies

demonstrate that current density, CE, CR are relatively low (Mahmoud et al., 2014),

probably due to a widespread amount of recalcitrant organics as well as different toxic

compounds, like heavy metals.

In our study, a maximum anodic COD removal of 1.24 g L-1 d-1 (65%) and

around 0.9 g L-1 d-1 (45%) was achieved in continuous mode dealing with landfill

leachate. The CE obtained (22-29%) was higher than reported in literature except

Mahmoud et al., (2014) who achieved a maximum 56% but their TCOD removal was

only 31%. Moreover, dealing with high strength landfill leachate, Puig et al., (2011)

abated a maximum 8.5 g COD L-1 d-1, but with lower coulombic efficiency (2%).

More recently, Birjandi et al., (2016) examined simultaneous electricity

production and treatment of medicinal herb wastewater using MFC-driven bioelectro-

Fenton. Owing to high biodegradable wastewater (>0.5), 51-87% COD was degraded at

the rate 0.8-1.2 g COD L-1 d-1 in batch mode. Domestic wastewater led to higher CE

(20%) due to its richness in biodegradable organic compounds, however, landfill

14
leachates exhibited lower CE (< 20%). These studies show that the complex nature of

substrate hinders the CE and organics removal efficiency.

<Table 5>

4. Conclusion

Employing Microbial Electrochemical Technology (MET) - driven electro-

Fenton oxidation led to the treatment of recalcitrant organics of landfill leachate

(effluent of anammox reactor). The system resulted in a maximum COD removal rate of
- -
318-351 mg L 1 d 1 in batch followed by a 1077-1244 mg L-1 d-1 in continuous mode.

The recirculation of acidic catholyte into anode chamber hindered the anodic efficiency

due to pH stress on anodic electricigens. In terms of current densities, continuous mode

operation showed better efficiency than batch mode. These findings provide an efficient

and sustainable approach to enhance degradation of recalcitrant organic pollutants from

landfill leachate.

Supplementary data

Supplementary data for this work can be found in e-version of this paper online.

Acknowledgement

The authors would like to thank the Spanish Ministry (CTQ2014-53718-R) and the

University of Girona (MPCUdG2016/137) for their financial support. LEQUIA has

been recognized as consolidated research group by the Catalan Government (2014-

SGR-1168). Muhammad Hassan wishes to thank East China Normal University,

Shanghai China for financial support through universitys study overseas program

fund (40600-511232-14203/003). The authors also acknowledge Mr. Tiago Vitor and

Dr. Mael Ruscalleda for supplying the anammox effluent used in this study.

15
References

Anfruns, A., Gabarr, J., Gonzalez-Olmos, R., Puig, S., Balaguer, M.D., Colprim, J., 2013. Coupling

anammox and advanced oxidation-based technologies for mature landfill leachate treatment.

Journal of Hazardous Materials 258259, 2734.

Baun, D.L., Christensen, T.H., 2004. Speciation of heavy metals in landfill leachate: a review. Waste

Management & Research 22, 323.

Behera, M., Jana, P.S., More, T.T., Ghangrekar, M.M., 2010. Rice mill wastewater treatment in microbial

fuel cells fabricated using proton exchange membrane and earthen pot at different pH.

Bioelectrochemistry 79, 228233.

Beltran de Heredia, J., Torregrosa, J., Dominguez, J.R., Partido, E., 2005. Degradation of wine distillery

wastewaters by the combination of aerobic biological treatment with chemical oxidation by

Fentons reagent. Water Science and Technology 51, 167174.

Birjandi, N., Younesi, H., Ghoreyshi, A.A., Rahimnejad, M., 2016. Electricity generation through

degradation of organic matters in medicinal herbs wastewater using bio-electro-Fenton system.

Journal of Environmental Management 180, 390400.

Brillas, E., Sires, I., Oturan, M.A., 2009. Electro-fenton process and related electrochemical technologies

based on fentons reaction chemistry. Chemical Reviews 109, 65706631.

Brillas, E., Sirs, I., 2015. Electrochemical removal of pharmaceuticals from water streams: Reactivity

elucidation by mass spectrometry. TrAC Trends in Analytical Chemistry 110.

Elmolla, E.S., Chaudhuri, M., 2010. Comparison of different advanced oxidation processes for treatment

of antibiotic aqueous solution. Desalination 256, 4347.

Feng, C., Li, F., Liu, H., Lang, X., Fan, S., 2010. A dual-chamber microbial fuel cell with conductive

film-modified anode and cathode and its application for the neutral electro-Fenton process.

Electrochimica Acta 55, 20482054.

Fernndez de Dios, M.., del Campo, A.G., Fernndez, F.J., Rodrigo, M., Pazos, M., Sanromn, M..,

16
2013. Bacterial-fungal interactions enhance power generation in microbial fuel cells and drive dye

decolourisation by an ex situ and in situ electro-Fenton process. Bioresource Technology 148, 39

46.

Friedman, E.S., Rosenbaum, M.A., Lee, A.W., Lipson, D.A., Land, B.R., Angenent, L.T., 2012. A cost-

effective and field-ready potentiostat that poises subsurface electrodes to monitor bacterial

respiration. Biosensors and Bioelectronics 32, 309313.

Garcia-Segura, S., Brillas, E., 2016. Combustion of textile monoazo, diazo and triazo dyes by solar

photoelectro-Fenton: Decolorization, kinetics and degradation routes. Applied Catalysis B:

Environmental 181, 681691.

Hassan, M., Wang, X., Wang, F., Wu, D., Hussain, A., Xie, B., 2016a. Coupling ARB-based biological

and photochemical (UV/TiO2 and UV/S2O82) techniques to deal with sanitary landfill leachate.

Waste Management.

Hassan, M., Zhao, Y., Xie, B., 2016b. Employing TiO2 photocatalysis to deal with landfill leachate:

Current status and development. Chemical Engineering Journal 285, 264275.

He, Z., Minteer, S.D., Angenent, L.T., 2005. Electricity generation from artificial wastewater using an

upflow microbial fuel cell. Environmental Science and Technology 39, 52625267.

Kelly, P.T., He, Z., 2014. Understanding the application niche of microbial fuel cells in a cheese

wastewater treatment process. Bioresource Technology 157, 154160.

Kim, K.Y., Yang, W., Evans, P.J., Logan, B.E., 2016. Continuous treatment of high strength wastewaters

using air-cathode microbial fuel cells. Bioresource Technology 221, 96101.

Liu, H., Liu, H., Ramnarayanan, R., Ramnarayanan, R., Logan, B.E., Logan, B.E., 2004. Production of

electricity during wastewater treatment using a single chamber microbial fuel cell. Environmental

science & technology 38, 22815.

Muller, G.T., Giacobbo, A., dos Santos Chiaramonte, E.A., Rodrigues, M.A.S., Meneguzzi, A.,

Bernardes, A.M., 2015. The effect of sanitary landfill leachate aging on the biological treatment and

assessment of photoelectrooxidation as a pre-treatment process. Waste Management 36, 177183.


17
Mahmoud, M., Parameswaran, P., Torres, C.I., Rittmann, B.E., 2014. Fermentation pre-treatment of

landfill leachate for enhanced electron recovery in a microbial electrolysis cell. Bioresource

Technology 151, 151158.

Nidheesh, P.V., Gandhimathi, R., Ramesh, S.T., 2013. Degradation of dyes from aqueous solution by

Fenton processes: A review. Environmental Science and Pollution Research.

Pous, N., Puig, S., Coma, M., Balaguer, M.D., Colprim, J., 2013. Bioremediation of nitrate-polluted

groundwater in a microbial fuel cell. Journal of Chemical Technology and Biotechnology 88, 1690

1696.

Puig, S., Serra, M., Coma, M., Cabr, M., Dolors Balaguer, M., Colprim, J., 2011. Microbial fuel cell

application in landfill leachate treatment. Journal of Hazardous Materials 185, 763767.

Rago, L., Ruiz, Y., Baeza, J.A., Guisasola, A., Corts, P., 2015. Microbial community analysis in a long-

term membrane-less microbial electrolysis cell with hydrogen and methane production.

Bioelectrochemistry 106, 359368.

Rajkumar, D., Palanivelu, K., Balasubramanian, N., 2005. Combined electrochemical degradation and

activated carbon adsorption treatments for wastewater containing mixed phenolic compounds.

Journal of Environmental Engineering and Science 4, 19.

Reimers, C.E., Stecher, H.A., Westall, J.C., Alleau, Y., Howell, K.A., Soule, L., White, H.K., Girguis,

P.R., 2007. Substrate degradation kinetics, microbial diversity, and current efficiency of microbial

fuel cells supplied with marine plankton. Applied and Environmental Microbiology 73, 70297040.

Ren, L., Ahn, Y., Logan, B.E., 2014. A Two-Stage Microbial Fuel Cell and Anaerobic Fluidized Bed

Membrane Bioreactor (MFC-AFMBR) System for E ff ective Domestic Wastewater Treatment.

Ruscalleda, M., Lpez, H., Ganigu, R., Puig, S., Balaguer, M.D., Colprim, J., 2008. Heterotrophic

denitrification on granular anammox SBR treating urban landfill leachate. Water Science and

Technology 58, 17491755.

Shi, Y., Hu, S., Lou, J., Lu, P., Keller, J., Yuan, Z., 2013. Nitrogen removal from wastewater by coupling

anammox and methane-dependent denitrification in a membrane biofilm reactor. Environmental


18
Science and Technology 47, 1157711583.

Vil-Rovira, A., Puig, S., Balaguer, M.D., Colprim, J., 2015. Anode hydrodynamics in

bioelectrochemical systems. RSC Adv. 5, 7899479000.

Vinogradov, a D., Grivennikova, V.G., 2005. Generation of superoxide-radical by the NADH:ubiquinone

oxidoreductase of heart mitochondria. Biochemistry. Biokhimiia 70, 120127.

Wang, X.-Q., Liu, C.-P., Yuan, Y., Li, F., 2014. Arsenite oxidation and removal driven by a bio-electro-

Fenton process under neutral pH conditions. Journal of Hazardous Materials 275, 2009.

Wen, Q., Wu, Y., Cao, D., Zhao, L., Sun, Q., 2009. Electricity generation and modeling of microbial fuel

cell from continuous beer brewery wastewater. Bioresource Technology 100, 41714175.

Xie, B., Lv, Z., Hu, C., Yang, X., Li, X., 2013. Nitrogen removal through different pathways in an aged

refuse bioreactor treating mature landfill leachate. Applied Microbiology and Biotechnology 97,

92259234.

Xu, N., Zhou, S., Yuan, Y., Qin, H., Zheng, Y., Shu, C., 2011. Coupling of anodic biooxidation and

cathodic bioelectro-Fenton for enhanced swine wastewater treatment. Bioresource technology 102,

777783.

Zhang, H., Choi, H.J., Huang, C.-P., 2005. Optimization of Fenton process for the treatment of landfill

leachate. Journal of Hazardous Materials 125, 166174.

Zhang, H., Zhang, D., Zhou, J., 2006. Removal of COD from landfill leachate by electro-Fenton method.

Journal of Hazardous Materials 135, 106111.

Zhuang, L., Zhou, S., Yuan, Y., Liu, M., Wang, Y., 2010. A novel bioelectro-Fenton system for coupling

anodic COD removal with cathodic dye degradation. Chemical Engineering Journal 163, 160163.

19
Table captions
Table 1: Physico-chemical characteristics of the effluent of an anammox process

treating landfill leachate.

Table 2: Applied conditions for RR-1 and RR-2

Table 3: Summarized results of system performance in terms of current density,

coulombic efficiency and residual in situ H2O2 concentration at various operating

conditions.

Table 4: Overall anodic and cathodic performance at various modes of operation in

terms of COD and TOC removal.

Table 5: Comparison of this work with other studies dealing with complex wastewater

substrates

in MET system.

Figure captions
Fig. 1: Scheme of an integrated system for the bioelectrochemical treatment of effluents

from Anammox Reactor (AR)

Fig. 2: Anolyte COD removal over time in RR-1 (A) and RR-2 (B)

Fig. 3: Cathodic COD removal efficiency over time in RR-1 (A) and RR-2 (B).

Tables

Table 1: Physico-chemical characteristics of the effluent of an anammox process


treating landfill leachate. The results are presented as the mean standard deviation (n
= 15).

Parameter Unit Concentration


pH - 7.6 1.8
Conductivity mS cm-1 32.0 4.2
ORP mV 332 172
20
COD mg L-1 2401 562
BOD5 mg L-1 237 57
UV254 - 24.1 8.5
TOC mg L-1 569 299
IC mg L-1 56 5
NH4-N mg L-1 77 55
NO3-N mg L-1 188 50
NO2-N mg L-1 2.8 0.7
SO4 S mg L-1 541 181
PO4 P mg L-1 5.5 4.9
Cl- mg L-1 10403 3771
Br- mg L-1 16.3 6.4
CH3COO- mg L-1 6.1 3.3
Ca2+ mg L-1 520 278
Mg2+ mg L-1 81 22
K+ mg L-1 563 205
Na+ mg L-1 5200 1630
ORP: Oxidation-reduction potential; IC: Inorganic carbon

Table 2: Applied conditions for RR-1 andRR-2.

Reactor Test Operation Anolyte Catholyte E cathode Flow Operational HRT


mode (V vs rate time (d) (h)
Ag/AgCl) (L d-1)
RR-1 1 Batch GL LL -0.7 - 0-7 855
RR-1 2 Batch GLL LL -0.9 - 8 -11 75
RR-1 3 Continuous GLL LL -1.0 0.5 12-18 24
RR-1 4 Continuous LL LL -1.0 0.5 19-28 24
RR-1 5 Recirculation LL LL -1.0 0.5 29-35 24

21
(acidic
pH)
RR-2 1 Batch GL LL -0.7 - 0-11 855
RR-2 2 Batch GLL LL -0.9 - 75
RR-2 3 Continuous GLL LL -1.0 0.5 12-18 24
RR-2 4 Continuous LL LL -1.0 0.5 19-28 24
RR-2 5 Recirculation LL LL -1.0 0.5 29-35 24
(acidic
pH)
GL: Glucose; GLL: Glucose + effluent from the anammox reactor treating landfill
leachate (1:1); LL: Effluent from the anammox reactor treating landfill leachate

Table 3: Summarized results of system performance in terms of current density,


coulombic efficiency and residual in situ H2O2 concentration at various operating
conditions.

CODi CODf Initial pH Final pH Residua j (A.m-


Test CE (%)
(mg L-1) (mg L-1) l H2O2 3)
Anode Cathod Anode Cathod (mg/L)
RR- e e
1 4.71. 96.64. 13.15. 14.15.
1 1702126 730127
7.70.2 2.70.2 7 5.82.7 4 3 8

22
2016 6.60. 25.87. 26.24.
2 63092 1066
169 7.80.3 3.60.4 9 5.62.5 1 6

2016 5.93. 43.52. 29.33.


3 169 826100 7.50.4 3.40.3 4 5.44.1 13014 2 9

176232 7.760.0 5.62. 34.61. 22.44.


4 2704142 9 1 3.00.6 8 4.81.9 10816 4 2

2667 222319 5.01. 24.12.


5 234 5 4.81.9 3.30.6 1 7.41.2 21449 8 3116

RR-
2

6.20. 73.83.
1 1702126 386126
7.70.2 2.70.2 7 5.20.7 4 6.16.0 2.61.7

2016 6.80. 17.48.


2 59839
169 7.80.4 3.60.3 7 6.22.0 793 7 4.72.0

2016 5.80. 68.76. 26.82. 10.11.


3 169 880104 7.50.4 3.10.5 2 5.44.1 5 1 3

224918 7.760.0 6.90. 43.47. 18.32.


4 2704142 5 1 3.00.3 3 4.90.9 2 6 9.52.1

249711 5.61. 35011 14.40. 11.35.


5 2997433 7 4.90.9 4.01.3 4 7.40.9 4 8 6

Table 4: Overall anodic and cathodic performance at various modes of operation in


terms of COD and TOC emoval. The poised potential was -1.0 V vs Ag/Ag Cl except batch
(-0.9 V vs Ag/Ag Cl).

Anodic removal rate (mg L-1d) Cathodic removal rate (mg L-1d)
Parameters Batch (GLL) Continuous (GLL) Continuous (LL) Batch (LL) Continuous (LL)
RR-1
COD 31816 1244 126 88391 25460 86374
TOC 10521 32723 28837 3810 18349
RR-2
23
COD 35118 1077 60 597 33 28973 897200
TOC 10953 20822 15148 6718 30382
GLL: Glucose+effluent from the anammox reactor treating landfill leachate
(1:1); LL: Effluent from the anammox reactor treating landfill leachate

Table 5: Comparison of this work with other studies dealing with complex wastewater
substrates in MET systems.

MET system Wastewater type Operation Influent COD COD removal CE (%) References
mode (g L-1)
(%) (g L-1 d-1)
MET-driven electro- Effluent of anammox Continuous 2.7040.142 35 - 65 0.88 -1.24 22-29 This study
Fenton (BEF) reactor treating LFL
Air cathode MFC Brewery WW Fed-batch 1.501 20.7 1.06a 2.58 (Wen et al.,
2009)
Dual chamber MFC Swine WW Batch 1.652 39 - 46.5 2.5 4-6.5 (Xu et al.,
2011)
Air-cathode MFC LFL Continuous 3.480.48 37 8.5 2 (Puig et al.,
2011)

24
Two stage MFC- Domestic WW Fed-batch 0.210.01 92 0.55 a 18 (Ren et al.,
AFMBR 2014)
a
MFC Rice mill WW Fed-batch 1.1 87 0.09 4.1-5.9 (Behera et
al., 2010)
a
Tubular MFC Cheese whey Batch 11.350.42 599 0.56 < 20 (Kelly and
He, 2014)
a
Single chamber MFC Domestic WW Batch 0.22 80 0.35 20 (Liu et al.,
2004)
a
MFC Swine WW Continuous 7.5 22 - 59 2.4-6.3 17-23 (Kim et al.,
2016)
Air-cathode MFC Medicinal herbs WW Batch 6183309 51-78 0.8-1.2a 0.15-1.2 (Birjandi et
(BEF) al., 2016)
a
: values are calculated based on available data; AFMBR: Anaerobic fluidized bed membrane bioreactor; CE: Coulombic efficiency;
BEF: Bioelectro-Fenton; LFL: landfill leachate; WW: Wastewater.

Figures

25
Figure 1: Scheme of an integrated system for the bioelectrochemical treatment of
effluents from Anammox Reactor (AR): the AR effluent is further processed at the
anode and cathode of Microbial Electrochemical Technology-driven electro-Fenton
(BEF) system simultaneously.

Removal rate
A Batch Removal ( %)
1600 (GLL) Cont. (GLL) 100
Removal rate (mg L-1 d-1)

Batch (GL)

Removal efficiency (%)


1400
Cont. (LL) 80
1200
Loop (LL)
1000 60
800
600 40
400
20
200
0 0
4 7 11 15 18 22 25 27 29 31 35
Time (d)

26
Removal rate
B Removal ( %)
Batch
1400 100
Batch (GL) Cont. (GLL)
Removal rate (mg L-1 d-1)

Removal efficiency (%)


1200
80
1000 Loop (LL)
Cont. LL
800 60

600 40
400
20
200
0 0
4 7 11 15 18 22 25 27 29 31 35
Time (d)

Figure 2: Anolyte COD removal over time in RR-1 (A) and RR-2 (B).

GLL: Glucose + Effluent from the anammox reactor treating landfill leachate; LL:
Effluent from the anammox reactor treating landfill leachate

27
COD removal rate COD removal (%)
A
1200 Cont. LL 100

COD removal rate (mg L-1 d-1)


1000 80

COD removal (%)


800
Batch LL 60
600 Loop LL
40
400

200 20

0 0
4 7 11 15 18 22 25 27 29 31 35
Time (d)

COD removal rate COD removal (%)


B
1400 100
Cont. LL
COD removal rate (mg L-1 d-1)

1200
80

COD removal (%)


1000
Batch LL 60
800
Loop LL
600 40
400
20
200
0 0
4 7 11 15 18 22 25 27 29 31 35
Time (d)

Figure 3: Cathodic COD removal efficiency over time in RR-1 (A) and RR-2 (B). Error
bars represent standard deviations of replicate samples (n = 2). LL: Effluent from the
anammox reactor treating landfill leachate

28
Highlights

MET-driven electro-Fenton process was evaluated to treat landfill leachate.


COD removal of 1077-1244 mg L-1 d1 with electricity production was obtained
Recirculation of acidic catholyte into anode chamber hindered the anodic efficiency
Higher current density was observed in continuous mode operation.

29
Graphical abstract