Role of macrophyte species in constructed wetland-microbial fuel cell for simultaneous wastewater treatment and bioenergy generation

Journal Pre-proofs Role of macrophyte species in constructed wetland-microbial fuel cell for simultaneous wastewater treatment and bioenergy generation Yan Yang, Yaqian Zhao, Cheng Tang, Lei Xu, David Morgan, Ranbin Liu PII: DOI: Reference:

S1385-8947(19)33123-7 https://doi.org/10.1016/j.cej.2019.123708 CEJ 123708

To appear in:

Chemical Engineering Journal

Received Date: Revised Date: Accepted Date:

12 October 2019 30 November 2019 3 December 2019

Please cite this article as: Y. Yang, Y. Zhao, C. Tang, L. Xu, D. Morgan, R. Liu, Role of macrophyte species in constructed wetland-microbial fuel cell for simultaneous wastewater treatment and bioenergy generation, Chemical Engineering Journal (2019), doi: https://doi.org/10.1016/j.cej.2019.123708

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Role of macrophyte species in constructed wetland-microbial fuel cell for simultaneous wastewater treatment and bioenergy generation

Yan Yanga,b, Yaqian Zhaoa,c*, Cheng Tanga, Lei Xua, David Morgana, Ranbin Liua a

UCD Dooge Centre for Water Resources Research, School of Civil Engineering,

Newstead Building, University College Dublin, Belfield, Dublin 4, Ireland b Department

of Environmental Engineering, Anhui Jianzhu University, Hefei 230601, Anhui, P.R. China

c State

Key Laboratory of Eco-Hydraulics in Northwest Arid Region, Xi’an University of Technology, Xi’an 710048, P.R. China

_____________________________ *Corresponding author: Yaqian Zhao e-mail: [email protected]; telephone, +86-17782876871

1

Abstract The aim of this study was to determine the role of plants on pollutant removal and bioelectricity production in the treatment of municipal wastewater with constructed wetland matrix incorporating microbial fuel cells (CW-MFCs) compared to traditional CWs. Multi-anode unplanted and planted CW-MFCs (Iris pseudacorus, Hyacinth pink, and Phragmites australis) were established in fed-batch mode. CW-MFC modules with established vegetation had high treatment efficiencies with COD, NO3--N, NH4+-N, and PO43--P removal of 46.9-51.6%, 94.8-97.4%, 43.2-71.5%, and 96.0-97.6%, respectively, compared to 36.6%, 89.9%, 43.0%, 97.1% in the unplanted wetland module, respectively. More efficient pollutant removal and higher power production were correlated with higher plant growth. The highest maximum power density achieved was 25.14 mW/m2 in the multi-anode CW-MFC planted with Iris pseudacorus at highest plant height (1,635 cm). The CW-MFC planted with Iris pseudacorus enhanced NH4+-N removal by 66.2% and significantly contributed to bioelectricity generation by 97.5% compared to the unplanted CW-MFC. The results highlight the significant role of growing plants in the CW-MFC matrix in strengthening the bioenergy output compared with enhancement in wastewater treatment in CW-MFCs. Future studies should focus on improvement in cathode potential over a long-term operation and minimize the negative role of withered plants on the planted CW-MFCs.

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Keywords: Microbial fuel cell; Constructed wetland; Wetland plants; Pollutant removal; Bioenergy production

3

1. Introduction Constructed wetlands (CWs) have been acknowledged to have aesthetic, recreational and ecological functions for wastewater treatment and have been increasingly applied worldwide in recent years. Wetland plant is an indicating component of traditional CWs to distinguish CWs from biofilters or lagoons. The main roles of plants in CWs include absorbing nutrients, excreting oxygen into the rhizosphere, providing a surface for bacterial attachment and supporting microbial community biodiversity, as well as preventing the substrate clogging [1]. However, the plant contribution for the removal of nitrogen (N) and phosphorus (P) from wastewater in CWs is the focus of significant debate [2-5]. The consensus is that plant uptake is negligible with less than 10% of the total removed nutrients harvested from plants [3]. CW coupled with microbial fuel cell (CW-MFC) is a novel, promising, and scalable technology which has emerged in recent years for harvesting bioelectricity while treating conventional and emerging contaminants in wastewater [6-8]. Researchers have consistently stated that plants play a crucial role in bioelectricity enhancement by increasing bacteria biodiversity (especially electroactive bacteria) in CW-MFCs [9, 10]. The maximum power density in planted CW-MFCs was found to be significantly higher than unplanted CW-MFCs. For example, the maximum power density of CW-MFCs planted with Ipomoea aquatic was 12.42 mW/m2 while unplanted was 5.13 mW/m2 [11]; CW-MFCs planted with Typha latifolia was 13.4 mW/m2 while the unplanted was 5.39 mW/m2 [12]; CW-MFC planted with Canna indica was 8.91 mW/m2 while the unplanted was 1.84 mW/m2 [9]; Additionally, 4

CW-MFC planted with Elodea nuttallii was high as 41.46 mW/m3 while unplanted CW-MFC was low as 0.17 mW/m3 [13]. Furthermore, planted CW-MFCs enhance the removal efficiencies of organic matter, nitrogen (N) and phosphorus (P) compared to unplanted CW-MFCs. The removal efficiencies of COD and total P in a CW-MFC planted with Typha angustifolia were 85.4±16.3% and 97.05±4.4%, respectively, which were higher than that of 75.81±17.1% for COD and 71.77% for total P in an unplanted CW-MFC system [12]. The NH4+-N removal rate of CW-MFC system with submerged plants (Hydrilla verticillata) was 31.25% higher than that of an unplanted CW-MFC system [14]. It seems that the role of plants in wastewater treatment becomes more significant in CW-MFC (resulted from electroactive bacteria) than that in traditional CWs (i.e., CW-MFCs under open-circuit). Indeed, wetland plant species may demonstrate a vast difference in power generation and pollutant removal [12, 15] because of the concentration of diverse oxygen and dissolved organic carbon produced by various wetland plants. Although a few studies have investigated and compared a few plant species in their studies [10, 12], they did not address the comparison and effects of popular and common species (e.g., Phragmites australis) on treatment performance and bioelectricity production in the CW-MFC systems. The understanding of the role of plants (in different species) in CW-MFC systems for wastewater treatment and bioelectricity production compared to conventional CWs (open-circuit condition) is still lacking. The main objectives of this study were: 1) to investigate the role of wetland macrophytes (i.e., common plant species) in wastewater treatment in CW-MFCs 5

(closed-circuit) and conventional CWs (open-circuit condition); and 2) to examine and compare wastewater treatment and bioelectricity production in planted and unplanted wetland CW-MFCs. To achieve the objectives, multi-anode alum sludge-based CW-MFCs planted with three different macrophytes (i.e., Iris pseudacorus, Hyacinth pink, and Phragmites australis, respectively) were investigated with an unplanted CW-MFC as control under open- and closed-circuit for comparative purpose in this study.

2. Materials and methods 2.1 Wetland Plants Iris pseudacorus and Phragmites australis were obtained from the Grand Canal, while Hyacinth pink was obtained from a garden center, all in Dublin city, Ireland. The three macrophyte species with each weighing 95±5 g were propagated for 2 weeks in a culture solution, which contained Miracle-Gro Liquid All Purpose dissolved in tap water. Before transplanted to CW-MFC with a density of one rhizome per unit, the wetland plants were rinsed five times using tap water. Their roots were measured with lengths of 17.67±9.29 cm, 8.67±4.04 cm, and 17.67±4.50 cm for Iris pseudacorus, Hyacinth pink, and Phragmites australis, respectively. Iris pseudacorus had one stem with an average length of 28.5±1.29 cm. Hyacinth pink also had one stem of 10±0.5 cm in length, and two flowers with an average length of 12.75±0.35 cm. Phragmites

6

australis had two stems with length of stem 1 of 41.5±4.94 cm and stem 2 of 15±2.82 cm (Fig. 1).

a

d

e

f

C

b

c

A2 A1

Fig. 1 Schematic diagram of the CW-MFC configuration (a), photograph of the CW-MFC systems (b), electrode structures (c), Iris pseudacorus (d), Hyacinth pink (e), and Phragmites australis (f)

2.2 Multi-anode CW-MFC configurations and electrode structure 2.2.1 Set-up of multi-anode CW-MFC systems Four identical microcosm-scale CW-MFCs with internal diameter of 15 cm and height of 32 cm were constructed (Fig. 1). Gravel with average diameter of 5 mm was added from the bottom up to 3 cm height of the CW-MFC as a supporting layer. Dewatered alum sludges (DAS) collected from a water treatment plant in Dublin with 7

a particle size ranging from 4 to 14 mm, and a porosity of 45% were added into each CW-MFC as the main wetland substrate. The advantage of the DAS as wetland substrate lies in its good P adsorption capacity [16]. Graphite gravel (4-10 mm) was used as electrodes, which was pretreated by soaking it in 1 M NaOH and 1 M HCl, respectively, to eliminate possible oil stain and metal ion contamination. Stainless steel mesh (SSM, thickness of 1 mm, 5 Mesh, 9.5 cm×8.5 cm×3 cm) filled with graphite gravel was used as the anode. Stainless steel mesh (SSM, Diameterout, 13 cm; Diameterin, 5 cm) filled with graphite gravel was used as the cathode. The surface areas of each anode and the cathode were 161 cm2 and 226 cm2, respectively. Before setting up the CW-MFCs, the anode compartments were inoculated with anaerobic digester sludge sourced from Ringsend Wastewater Treatment Plant, Dublin, and the cathode compartments were inoculated for 2 days with activated sludge sourced from Malahide Wastewater Treatment Plant, Dublin. Anodes and cathodes were connected by insulated copper wire through an external circuit with a resistor of 10 kΩ initially and then 983 Ω for the main test period. MFCs were embedded in the CWs in a two anodes-one cathode configuration. Anode 1 (A1) and anode 2 (A2) were installed at 10 cm and 20 cm, while the cathode (C) was placed at 30 cm from the bottom of the CW-MFC system (Fig. 1). One unplanted CW-MFC system served as a control (R1), and the remaining three CW-MFCs were planted with different macrophytes: Iris pseudacorus (R2), Hyacinth pink (R3), and Phragmites australis (R4), respectively. The plants were strategically placed on the top of the second anode (A2) in each system. 8

2.2.2 Operation of the multi-anode CW-MFC system The effects of plant species on pollutant removal and bioelectricity generation performance were assessed in the four CW-MFC systems. After start-up, the CW-MFCs were operated for 94 days under fed-bach mode with 14 Cycles of different hydraulic retention times (HRTs) (Table 1). CW-MFCs were operated with zero energy consumption (without pumping systems, aeration and/or external power supply). Synthetic wastewater was prepared using: CH3COONa, 256.41 mg/L; NH4Cl, 76.43 mg/L; NaNO3, 30.36; KH2PO4, 14.24 mg/L; CaCl2, 14.7 mg/L; MgCl2, 20.3 mg/L and trace element solution, 10 mL/L [17]. The influent COD of 210.4±60.9 mg/L, NH4+-N of 19.7±1.6 mg/L, and NO3--N of 4.78±1.5 mg/L were chosen based on the fact that the concentration of total nitrogen (TN) in domestic wastewater is reported to vary between 20 and 35 mg/L while 70% to 82% of TN is NH4+-N [18]. The synthetic wastewater was fed onto the surface of each CW-MFC in each batch/cycle. All the systems were operated in lab conditions with room temperature of around 20 °C. The daily water loss due to evapotranspiration and sampling in the CW-MFCs was about 0.84±0.95%, 5.23±0.72%, 1.18±1.19%, 2.62±0.12% for systems R1-R4, respectively. Obviously, higher water loss was observed in the planted CW-MFC systems than the unplanted system. The evaporated water was refilled daily by the fresh synthetic wastewater.

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Table 1 Operational cycles for the CW-MFCs (OC: open-circuit; CC: closed-circuit) Cycle 1 2 3 4 5 6 7 8 9 10 11 12 13 14

HRT (d) 5 5 6 7 6 11 8 5 11 6 6 6 6 6

Circuit Open Open Closed Closed Closed Closed Closed Closed Closed Closed Open Open Open Open

Resistance (KΩ)

Conditions OC-10 KΩ OC-10 KΩ CC-10 KΩ CC-10 KΩ CC-1 KΩ Kinetic experiment;

10 10 1 1 1 1 1 1

Hyacinth pink was dying

CC-1 KΩ CC-1 KΩ Hyacinth pink completely

dead

CC-1 KΩ CC-1 KΩ CC-1 KΩ OC-1 KΩ OC-1 KΩ OC-1 KΩ OC-1 KΩ

2.3 Sample collection and analysis 2.3.1 Water quality determination The water samples were collected at the start and the end of each cycle in order to evaluate treatment performance of each CW-MFC. To study the kinetics of pollutant removal, water samples were also collected at different time intervals, and the CW-MFCs were refilled by the fresh synthetic wastewater. COD, NH4+-N, NO2--N, NO3--N, and reactive PO43--P (RP) in the samples were determined using a spectrophotometer (DR/2800, Hach) according to their standard operating procedures; pH was measured using a pH meter (Orion 720 A, Thermo). PO43--P test was modified using the sample as control rather than deionized water. This is because light 10

yellow color in the liquid sampled was observed due to the release of natural organic matters (mainly humic substance) from the DAS [19]. 2.3.2 Electrochemical measurements The electrical signals produced during each cycle were monitored. Voltage and electrode potential were recorded using multimeter over Cycles 1-6 and by data acquisition system over Cycles 7-14. The electrochemical performance of CW-MFC was evaluated by polarization and power density curves obtained at the end of Cycle 7 and Cycle 9. Power densities (P = U2/RA, mW/m2) were determined through basic electrical calculations, where U is the voltage (V), R is the resistance (Ω) and A is the surface area of anodes (m2). To obtain the polarization curve, external resistance was varied over a range from 20 to 21,800 Ω and the steady-state voltage across the resistors was measured. The electrode potentials were determined against a saturated Ag/AgCl electrode (Mettler Toledo, +0.197 V vs Standard Hydrogen Electrode). The coulombic efficiency (CE) reflecting the efficiency of electron generated from organic matter for electrical power was determined by Eq. (1) [6]. 𝑀×𝐼

𝐶𝐸 = 𝐹 × 𝑉 × 𝑏 × ∆𝐶𝑂𝐷

(1)

Where, CE (%) is coulombic efficiency, M is the molecular mass of oxygen (g O2/mol O2), which is 32. I (A) is current, F (C/mol) is Faraday’s constant, which is 94,685. q (L) is the liquid volume in the CW-MFC, b is the number of electrons donated by one

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mole O2 (mol e−/mol O2), which is 4, and △COD (g/L) is the decrease of COD in the beginning and the end of the Cycles. 2.3.3 Plant growth measurements Plant growth was measured by counting the number of stems and leaves and measuring their length from top of the cathode to tip. Stem and leaf length were summed up for total length [20]. The enhanced removal efficiency/bioelectricity production by plants was calculated by Eq. (2): Enhancement (%) =

𝑃𝑙𝑎𝑛𝑡𝑒𝑑 ― 𝑈𝑛𝑝𝑙𝑎𝑛𝑡𝑒𝑑 𝑈𝑛𝑝𝑙𝑎𝑛𝑡𝑒𝑑

(2)

× 100

2.4 COD reduction kinetic analysis and statistical analysis In this study, the kinetic study of COD, NH4+-N, NO2--N, NO3--N, PO43--P were carried out over Cycle 5. COD removal kinetics was regressed using the first-order equation as follows [21]: Ln

𝐶𝑡 𝐶𝑜

(3)

= kt

Where, k is the first-order rate constant (h-1), Co is the influent COD concertation, and 𝐶𝑡

Ct is COD concentration at certain time. Through the linear regression between Ln 𝐶𝑜 and the operating time, the values of k under various conditions could be obtained.

In order to analyze the performance of each CW-MFC, statistical tests were 12

carried out with SPSS Statistics 23 of the statistical software package and a statistical confidence of p < 0.05. The statistical relations between the concentrations of COD, NH4+-N, NO3--N, and TP in unplanted and planted CW-MFCs under open- and closed- circuit were determined with a one-way ANOVA test.

3. Results and discussion 3.1 Plant monitoring and evaluation Plant growth was monitored at the end of each cycle throughout the experimental period (Fig. 2). After their transplantation into the CW-MFC systems, Iris pseudacorus, Hyacinth pink, and Phragmites australis all showed healthy growth. New stems of Iris pseudacorus (Stem 2), and Phragmites australis (Stem 3) were even observed at the end of Cycle 1 (Fig. 2a and 2c). The growth trend showed that the plants were acclimatizing and reproducing well in the experimental environment with synthetic wastewater. During the 88-day operation, Iris pseudacorus and Phragmites australis showed positive growth rates in terms of height, number of stems and number of leaves. Iris pseudacorus produced the highest biomass (Stem 1 grew from 28.5 ± 1.29 cm to 96.64 ± 23.17 cm, and Stem 2 grew from 0 cm to 62.42 ± 24.43 cm) than those of Phragmites australis and Hyacinth pink. The stem number of Phragmites australis increased from three (Cycles 1-5) to five (Cycles 6-9), to seven (Cycles 10) and then it decreased to five (Cycles 11-14) again. Hyacinth pink grew over Cycles 1-5, but started to wither away over Cycles 5-7 due to its short growth period, and was dead from Cycle 7 (Fig. 2b). Overall, the total plant length 13

showed a trend of: Iris pseudacorus (from 199 to 1635 cm) > Phragmites australis (from 380 to 1088 cm) > Hyacinth pink (from 75 to 141 cm) (Fig. 2d). More biomass production in the CW-MFCs could assimilate more organic matter and nutrients and reduce the internal resistance of system, resulting in higher bioelectricity production [22]. Therefore, it is reasonable to infer that: i) CW-MFC planted with Iris pseudacorus would have the best wastewater treatment performance and highest bioelectricity production; and ii) the wastewater treatment performance and voltage production would decline in the CW-MFC planted with Hyacinth pink when it started to wither.

Stem length (cm)

c

Stem 1-leave number Stem 2-leaf number

14

b

12 10

80

8

60

6

40

4

20

2

0 0 Start 1 2 3 4 5 6 7 8 9 10 11 12 13 14 No. of Cycles 70 12 11 60 10 9 50 8 7 40 6 30 5 4 20 3 2 10 1 0 0 Start 1 2 3 4 5 6 7 8 9 10 11 12 13 14 No. of Cycles

30

Stem 1-leaf length Flower length

25

No. of leaves Stem length (cm)

100

d

No. of leaves Stem length (cm)

Stem length (cm)

120

Stem 1-leaf length Stem 2-leaf length

Stem 1-leaf number Flower number -length

5

20

4

15

3

10

2

5

1

0 0 Start 1 2 3 4 5 6 7 8 9 10 11 12 13 14 No. of Cycles 1800 1600 1400

Iris Hyacinth Phra.

1200 1000 800 600 400 200 0

Start 1 2 3 4 5 6 7 8 9 10 11 12 13 14 No. of Cycles

Stem 1-leaf1-leaf number Stem 2-leaf number Stem Stem 3-leaf1-leaf number 2-leaf length/number Stem length Stem 3-leaf length/number Stem length/number Stem4-leaf number Stem 5-leaf number Stem Stem 6-leaf 2-leaf number length Stem 7-leaf number Stem 3-leaf lengthStem 5-leaf length/number Stem 4-leaf length/number Stem 4-leaf length Stem 6-leaf length/numberStem 5-leaf lengthStem 7-leaf length/number Stem 6-leaf length Stem 7-leaf length

14

6

No. of leaves/flowers

a 140

Fig. 2 Plant monitoring in CW-MFC modules over the experimental period (a: Iris pseudacorus, b: Hyacinth pink, c: Phragmites australis, and d: total plant length)

3.2 Plant role in pollutant removal in CW-MFCs under open- and closedcircuits All the DAS-based CW-MFCs (R1-R4) were self-sustaining pH systems with influent pH of 7.34±0.11 at the beginning of each cycle and 7.27±0.26, 7.27±0.26, 7.12±0.27, and 7.23±0.22 in R1-R4, respectively, at the end of each cycle. The pH balancing phenomenon in the studied CW-MFCs was attributed to DAS’s ability of pH neutralization [16].

3.2.1 PO43--P removal Efficient PO43--P removal with 96-97% was observed in both planted and unplanted CW-MFCs under open- and closed-circuit conditions (Fig. 3). Stable high removal performance of P with no significant differences under planted/unplanted (p=0.18>0.05) or open- and closed-circuit conditions (p=0.47>0.05) demonstrated that the P removal was mainly depending on the adsorption of alum sludge rather than plant uptake or MFC impact. The high removal efficiency of P in all CW-MFCs is attributed to the high adsorption capacity of alum sludge of 3.5 g/kg [23, 24]. In previous CW-MFC studies of using conventional substrates, the P removal was reported to be 71-97% with coarse sand as substrate [12] while in many studies P 15

removals were not reported [9, 13]. In the later stage of this study, slightly decreased P removal performance was observed in the CW-MFC planted with Hyacinth pink over Cycles 9-14, probably because of the P release from Hyacinth pink decomposition.

Removal efficiency (%)

100

Average CC-1 KOhm

OC-10 KOhm OC-1 KOhm

CC-10 KOhm

80 60 40 20 0

Unplanted

Iris

Hya.

Phra.

Fig. 3 PO43--P removal efficiency in the unplanted and planted CW-MFCs

3.2.2 N removal Iris pseudacorus significantly improved the removal rates of NH4+-N with 71.9±14.8% in R2 (NH4+-N reduced from 19.7±1.6 mg/L to 5.63 mg/L), followed by Phragmites australis (reduced to 11.35 mg/L) and Hyacinth pink (reduced to 13.12 mg/L), in comparison of that in unplanted systems with 43.0±5.4% (reduced to 11.24 mg/L). The CW-MFC planted with Iris pseudacorus demonstrated the significantly best NH4+-N removal performance (p<0.05, Fig. 4a), corresponding to the highest plant height/biomass of Iris pseudacorus among all the plants (Fig. 2a). The higher NH4+-N removal in the planted CW-MFCs may be achieved by: 1) uptake of plants (the uptake 16

rate of Iris pseudacorus is 0.15±0.01 mg NH4+-N/(g dry-root∙h) [25]); 2) better growing environment for nitrifying bacteria (e.g., Nitrosomonas, Nitrobacter) which can oxidize ammonia to nitrate in the aerobic microsites adjacent to roots and rhizomes where the release of O2 from Iris pseudacorus’s root has been estimated as 0.34 mg/h∙plant [26]. More importantly, by inspecting the CW-MFCs under open- and closed-circuit conditions, there were no significant differences in NH4+-N removal (p=0.54>0.05) except for CW-MFC planted with Iris pseudacorus and the CW-MFC planted with Hyacinth under CC-1 KΩ and OC-1 KΩ, indicating that MFC did not play a significant role in NH4+-N removal. The low concentration of NH4+-N over OC 1 KΩ in CW-MFC planted with Iris was probably because of the high plant growth, while the high NH4+-N concentration over OC-1 KΩ in R3 was owing to the NH4+-N release from Hyacinth decomposition. In addition, efficient NO3--N removal was detected in the unplanted CW-MFC (89.9%) and planted CW-MFCs (96.1%, 93.0%, and 94.8% for Iris pseudacorus, Hyacinth pink, and Phragmites australis, respectively) (Fig. 4b). NO3--N removal follows the same order as plant biomass with Iris pseudacorus > Phragmites australis > Hyacinth pink > unplanted without significant difference (p=0.095>0.05). NO3--N removal due to the sorption of plants was estimated to be around 3-6% [27] by subtracting NO3--N removal efficiency in the unplanted CW-MFCs (89.9%) from the planted CW-MFCs (93.0-96.1%) under open- and closed- circuits. This phenomenon demonstrated that plant uptake for NO3--N removal was similar in both CW-MFC (closed-circuit) and conventional CW (open-circuit) (p=0.67>0.05). 17

Favorably, no significant NO2−–N (≤0.05 mg/L) was detected at the end of each cycle (data not shown) in all the CW-MFCs.

Average OC-10 KOhm CC-10 KOhm CC-1 KOhm OC-1 KOhm

80 60 40 20 0

Unplanted

Iris

Hya.

100

NO3--N Removal Efficiency (%)

a

NH4+-N Removal Efficiency (%)

100

Phra.

b

80 60 40 20 0

Unplanted

Iris

Hya.

Fig. 4 Concentrations of NH 4 + -N (a) and NO 3 - -N (b) in the unplanted and planted CW-MFCs

3.2.3 COD removal Over the experimental period, Iris pseudacorus had the highest COD removal with an average of 51.6±6.0%, followed by Phragmites australis of 46.9±9.4% compared to 36.0±5.0% in the unplanted CW-MFC (Fig. 5a). Planted CW-MFCs had higher removal efficiencies with significant differences between Iris pseudacorus and Hyacinth pink (p=0.005<0.05) & between Hyacinth pink and Phragmites australis (p=0.013<0.05) than the unplanted system, and the order of removal efficiency was the same as plant growth. This was because plants provide more specific surface area for microorganisms associated with organic matter degradation [12]. In addition, there was no significant differences on COD removal under open- and closed-circuit 18

Phra.

conditions in planted/unplanted CW-MFCs (p=0.07>0.05), demonstrating that the presence of an electric current did not significantly impact the removal efficiencies of organic matter. This result differs from other studies which showed a significantly enhanced pollutant removal under closed-circuit compared to open-circuit [28, 29]. The difference may be explained by lower COD concentration used in this study (i.e., 210.4±60.9 mg/L) than other studies (215-823 mg/L) [28, 29]. The low COD was mostly and easily degraded by heterotrophic electrochemically inactive bacteria, and thus intensely competitive for electrochemically active bacteria to utilize remaining COD [30]. The COD reduction kinetics in the closed-circuit CW-MFCs was found to follow the first-order kinetics with high coefficients of determination (R2 > 0.9) (Fig. 5b). The kinetic rate constants were 0.0683/h for Iris pseudacorus, 0.0549/h for Hyacinth pink, 0.0543/h for Phragmites australis, and 0.0318/h for unplanted CW-MFC, respectively. It is worth noting that the degradation rates of COD were around 2 times higher in the planted CW-MFCs than the unplanted system. Plants with higher growth rates own higher degradation rates. The higher COD degradation rates suggest that plants have a significant impact on COD reduction rate in CW-MFCs, which might be attributed to direct reduction by heterotrophic and electroactive microorganisms in root area and plant uptake in the system [9, 10].

19

a

b 0.4

50 0 -50

-100 -150

-Ln(Ct/Co)

COD Removal Efficiency (%)

100

Average OC-10 KOhm CC-10 KOhm CC-1 KOhm OC-1 KOhm

Unplanted

Iris

Unplanted Iris Hya. Phra.

0.3

y=0.0683x+0.1658 R2=0.9316 y=0.0549x+0.0771 R2=0.9527

y=0.0543x+0.0757 R2=0.919

0.2

y=0.0318x+0.0988 R2=0.9268

0.1

Hya.

0.0

Phra.

0

1

2

3 Time (h)

4

Fig. 5 COD removal efficiencies (a) and its reduction kinetics (b) in the unplanted and planted CW-MFCs

3.3 Plant role in bioenergy generation in multi-anode CW-MFCs 3.3.1 Voltage generation The bioenergy production could be classified into two stages based on the alive/dead phases of Hyacinth pink. When Hyacinth pink was alive and the CW-MFCs were connected with 10 KΩ resistance (i.e. Cycles 3-4), the average bioelectricity generation of the four CW-MFCs followed the same order of plant growth with Iris pseudacorus > Phragmites australis > Hyacinth pink > unplanted (129±74 mV for A1-C and 131±75 mV for A2-C in R1, 280±143 mV for A1-C and 282±145 mV for A2-C in R2, 236±109 mV for A1-C and 201±144 mV for A2-C in R3, 201±144 mV for A1-C and 205±147 mV for A2-C in R4) (Fig. 6a).

20

5

When Hyacinth pink was completely dead and the CW-MFCs were connected with 983 Ω resistance (from Cycle 7), the average bioelectricity generation of the four CW-MFCs was in the order of Iris pseudacorus > Phragmites australis > unplanted > Hyacinth pink (115±37 mV for A1-C and 132±42 mV for A2-C in R1, 182±39 mV for A1-C and 194±41 mV for A2-C in R2, 87±36 mV for A1-C and 94± 40 mV for A2-C in R3, 172±40 mV for A1-C and 183±42 mV for A2-C in R4). The voltages of CW-MFCs planted with Iris pseudacorus and Phragmites australis were higher than that of unplanted CW-MFC, corresponding with our hypothesis that the macrophye Iris pseudacorus and Phragmites australis played a significant role in the enhancement of electricity production and a higher growth biomass of plants related to a higher enhancement. Notably, the average voltage of dying Hyacinth pink CW-MFC was 26.4% lower than that of unplanted CW-MFC (Since Cycle 7). This negative role of Hyacinth pink in bioelectrical performance is totally different compared to its beneficial role at its alive time in CW-MFCs (Cycles 3-4). This phenomenon suggested that the live plant plays a positive role in bioelectricity production, while the dead plant harms the CW-MFC by releasing organic matter, nutrients and lowering the voltage production.

21

500

a

Unplanted A1-C Iris A1-C Hya.A1-C Phra.A1-C

Unplanted A1-C Iris A1-C Hya.A1-C Phra.A1-C

b

300 Voltage (mV)

Voltage (mV)

400

350

Unplanted A2-C Iris A2-C Hya.A2-C Phra. A2-C

300 200

250

Unplanted A2-C Iris A2-C Hya.A2-C Phra. A2-C

200 150 100

100

50 0

0

20

40

60 80 100 Time (h)

120

140

0

0

20

40

60 80 100 Time (h)

120

140

Fig. 6 Typical voltage production in the CW-MFCs over Cycles 3-4 (a) and Cycles 7-10 (b)

3.3.2 Bioelectricity production The maximum power density of R1, R2, R3, and R4 was obtained at A2-C, which is in turn as 7.60, 13.27, 4.86, and 11.87 mW/m2, respectively (Fig. 7a and Table 2). The total maximum power density of R1, R2, R3, and R4 was 12.92, 25.14, 8.74, and 21.70 mW/m2, respectively. The maximum current density at A2-C of R1, R2, R3, and R4 was 74.3, 80.4, 71.2, and 86.6 mA/m2, respectively. It has been reported that N removal can be promoted by the accelerated transfer of electrons under micro-electric field in CW and can be inhibited when the current density is greater than 290 mA/m2 [9, 31]. Therefore, the current density of 74.3–86.6 mA/m2 detected in this study might be favorable for N removal. This is supported by the efficient NO3--N removal with 89-96% in all CW-MFCs under closed-circuit compared to 22

open-circuit (Fig. 4b). The average CE of the R1, R2, R3, and R4 was 8.35±0.05%, 8.05±0.03%, 9.05±0.08% and 9.74±0.20%, respectively. The low CE was also obtained in similar configurations by other researchers [12, 13]. More significantly, lower internal resistances derived from the maximum value of polarization curve were observed in the planted CW-MFCs (326-508 Ω) than unplanted CW-MFC (508 Ω). Interestingly, internal resistance in R1 and R4 showed a great decrease (Table 2) with the path distance between the cathode and anode electrodes decreased from 20 cm (i.e., A1-C) to 10 cm (i.e., A2-C). The reduced ohmic resistance due to small electrode spacing [32, 33] resulted in an increased power output (6.8% for R1 and 14.9-26.8% for R4). However, the internal resistance did not reduce with the decreased electrode distance in R2 and R3. This may be explained by the uniform distribution of Iris pseudacorus’s roots in R2 and dead plant roots of Hyacinth pink in R3 [34].

3.3.3 Electrode performance Electrode potentials versus the current density were examined to explore the anode and cathode performance (Fig. 7b). In terms of anodic potential in all CW-MFCs, the values presented a similar changing trend along with the increased current density, which means that the electrons provided by the anode are not the restriction. The cathodic potential showed the tendency of Iris pseudacorus > Phragmites australis > unplanted > Hyacinth pink, corresponding with the power density as the current 23

density in Fig. 7a. Furthermore, the anode potential remained at -437±18 mV while the differences of cathode potentials in the planted (-284±72 mV) and unplanted CW-MFC (-310 mV) under closed-circuit condition led to the voltage differences in CW-MFCs (data not shown). The voltage difference resulting from cathode potential suggested that the bio-cathode is the restricting factor for CW-MFC performance.

16

a

V R1 P R1

500

V R2 P R2

V R3 P R3

Voltage (mV)

12 400

10

300

8 6

200

4

100 0

0

200

V R4 P R4 14

b

R1 C R2 C R3 C R4 C

100 Power density (mW/m2) Voltage (mV)

600

0 -100 -200 -300

2

-400

0 10 20 30 40 50 60 70 80 90 100 Current Density (mA/m2)

-500

0

10 20 30 40 50 60 70 80 90 100 Current Density (mA/m2)

Fig. 7 Electrical performance: polarization curve & power density (a); electrode potential changes of A2-C in CW-MFCs over Cycles 7-10 in CW-MFCs (b)

Table 2 Bioelectricity performance of CW-MFCs

CW-MFC

R1 (unplanted) R2 (Iris) R3 (Hyacinth) R4 (Phragmites)

Maximum power density (mW/m2)

Internal resistance (Ω)

Maximum current density (mA/m2)

Coulombic efficiency (%)

Total

A1-C

A2-C

A1-C A2-C A1-C

A2-C

A1-C A2-C

12.92 25.14 8.74 21.70

5.32 11.87 3.88 9.83

7.60 13.27 4.86 11.87

508 326 326 508

74.30 80.49 71.20 86.68

5.57 8.70 5.92 7.66

24

R1 A R2 A R3 A R4 A

326 326 326 326

49.53 77.39 52.63 68.11

8.35 9.05 8.01 9.74

3.4 Plant role in wastewater treatment and bioelectricity production in CW-MFCs As presented in Section 3.2, plant contribution to the removal of COD, NH4+-N, NO3--N, and PO43--P was similar in CW-MFCs (closed-circuit) and conventional CWs (open-circuit). Regarding the plant role in power generation, Table 3 compares the voltage and power density in lab-scale CW-MFCs using external resistance of 1 KΩ in this study and other studies in the literature. A much higher voltage of 1.01±0.14 V in CW-MFC planted with Typha angustifolia was observed [12]. This could be attributed to utilization of high conductive magnesium as a cathode material. A significant high power density of 3714.08 mW/m2 was achieved using high conductive titanium mesh as the electrode material [35]. In this study, the produced voltage and power are comparable with other studies even if the cathode potential was negative over the experiment period. This may be explained by the multiple-anode structure adopted in this study as an alternative effective strategy to harvest energy. Nevertheless, all the studies have led to a consistent conclusion that plant growth plays a significant role in power production in CW-MFCs. There are two recognized pathways. On the one hand, plants produce rhizodeposits (i.e. carbohydrates) by photosynthetic activity, while the bacteria convert these rhizodeposits into green electricity via the fuel cell. For example, the average reported release rates of the dissolved organic carbon of Iris Pseudacorus and Phragmites australis are 12.2±0.7 and 9.0±0.9 µg/(g dry-root matter∙h), respectively [25]. On the other hand, plants 25

could release oxygen into cathode. Oxygen release rates of 1.0 mg/h·plant for Phragmites australis and 0.34 mg/h·plant for Iris pseudacorus have been observed [26], while no oxygen was released from water Hyacinth [36]. If rhizodeposition and photosynthesis of plants are dominant, it is expected that a lower anode potential was observed at A2 closer to the rhizosphere, but it was not the case in the current study. Therefore, it is reasonable to conclude that root release of oxygen from plants plays a more important role than the released organic matter.

26

Table 3 Comparison of power production in different CW-MFCs (GAC: Granular activated carbon; CFF: Carbon fiber felt) CW-MFC Size

Plant

Substrate

(cm, D× h)

HRT (d)

Mode

Anode

Cathode

Average

Internal

Power

voltage

resistance

density

(mV)

(Ω)

(mW/m2

References )

30×50

Ipomoea aquatica

Gravel

2

Continuous

GAC

GAC

500-700

156

12.42

[15]

18×75

Elodea nuttallii

Gravel

1

Continuous

GAC

GAC

302 ± 74

300

6.37

[13]

15×52

Canna indica

Quartz sand

2

Fed-batch

CFF

CFF

231 ± 53

8.39

[9]

416±50

21.53

Typha orientalis 16×52

Juncus effuses

Quartz sand

2

Fed-batch

CFF

CFF

Scirpus validus 15×30 45×45×40 (l×w×h)

Arundo donax

Quartz sand

Typha angustifolia

Sand

Phragmites australis

4

Intermittent

Graphite felt

Graphite felt

Intermittent

Graphite

Magnesium

sand,

GAC 3

Continuous

haycite

by

enclosed a

cylinder

titanium mesh

Titanium mesh (single layer)

Iris pseudacorus 15×32

Phragmites australis

Around 800

345±42

Quartz 20×55

182 ± 29

DAS

5

Fed-batch

Graphite

Graphite

Hyacinth (Dead)

27

6.40

[10]

14.12 399

790-1340

17.41

[34]

18.1

[12]

[35]

265.77±12.66

373

3714.08

377

326

25.14

356

326

21.70

182

326

This study

1

The contribution of plants to wastewater treatment efficiency and bioelectricity

2

production in this study and other studies in published CW-MFC systems is presented

3

in Table 4. The live planted CW-MFC enhanced the treatment efficiencies of COD,

4

NH4+-N, NO3--N, and PO43--P in the range of 2.93-43.29%, 0.67-66.17%,

5

-12.70-29.23%, and -1.13-35.15%, respectively. Compared with its role in pollutant

6

removal, it is clear that live plants play a much more significant role in bioelectricity

7

production with the range of 49-235%. However, the dead plants like Acorus calamus

8

[34] and Hyacinth pink in this study have a negative impact in power density. The

9

reason could be the fact that the biodegradation of exudates in the wetland had

10

consumed part of oxygen distributed in the aquatic environment, leading to limited

11

electron donors in the cathode. In addition, the decomposing bacteria of the plants

12

would compete with current-producing bacteria (such as Geobacter sulfurreducens

13

and Betaproteobacteria), limiting voltage production [34]. There is no doubt that the

14

negative impact of dead plants is a challenge for scaling up CW-MFC application

15

when plants experience non-growing and withering seasons.

16 17

Table 4 Role of emergent macrophyte on pollutant removal and power

18

production in CW-MFCs

19

Plant

Enhanced pollutant removal (%) COD NH4+-N NO3--N P

Enhanced power density References (%)

Ipomoea aquatica

2.93

142

48.79

-

28

[15]

Canna indica Scirpus validus Arundo donax Acorus calamus (Dead) Hydrilla verticillata Typha angustifolia Hyacinth pink (Alive) Hyacinth pink (Dead)

8.9

-

29.23

-

384

[9]

5.8

23.9

7.2

-

150

[10]

-

-

-

-

49.18

[34]

-80.63

[34]

66.22

[14]

235.8

[12]

31.25 12.65

11.35

-12.70

35.15

35.49

2.48

8.26

-1.13

-205.55

-43.51

-0.83

-5.56

-32.32

This study

Iris

43.29

66.17

6.60

0

97.52

This study

Phragmites australis

28.38

0.67

5.41

0.92

68.02

This study

This study

1 2

4. Conclusion

3

This study has demonstrated that the plant contribution (Iris pseudacorus, Hyacinth

4

pink, and Phragmites australis) to the pollutant removal (COD, NH4+-N, NO3--N, and

5

PO43--P) was similar in CW-MFCs (closed-circuit) and conventional CWs

6

(open-circuit). CW-MFC planted with Iris pseudacorus improved the removal

7

efficiencies of COD, NH4+-N, NO3--N, and power density by 43.29%, 66.17%, 6.60%,

8

and 97.52% compared with the unplanted CW-MFC over the study period (i.e. 94

9

days). Plant role in power production in CW-MFCs is more significant compared to

10

its role in wastewater treatment. Moreover, efficient P removal with 96-97% governed

11

by adsorption of alum sludge was achieved in all the CW-MFCs. Further work is

12

desirable regarding the plant role over a long-term operation and improving cathode

13

potential in planted CW-MFC systems. 29

1 2

Acknowledgements

3

This work was supported by Irish Research Council, Republic of Ireland

4

(GOIPD/2017/1367), Natural Science Foundation of Anhui Province, China (No.

5

1808085QE144), and Natural Science Foundation of China (41472047, 41702043,

6

and 41772038).

7

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13 14

Graphic abstract

15

36

Power density/Removal rate

90 60 30 0 -30

Total power density (mW/m2)

-60

COD (%) NH4+-N (%)

pollutant removal by 0.6-66%

NO3--N (%)

-90 -120

power by 68-97% Live plants enhanced

3-

PO4 -P (%)

Unplanted

Iris

1,600

Hya.-alive Hya.-dead

Phra.

CW-MFCs

Plant growth (cm)

1,400 1,200 1,000 800 600 400 200 0 Unplanted

Iris

Hyacinth

Phragmites

1 2 3 4

Highlights

5

6 7



Plant uptake of pollutants was similar in CW-MFCs under open- and close-circuit. 37

1



unplanted CW-MFC.

2 3





8

Dead Hya. harms the CW-MFC by releasing pollutants and lowering power production.

6 7

Iris improved removal of COD, N, and power density by 43, 66, and 97% in the CW-MFC.

4 5

Live plants enhanced the power output by 68-97% compared with



Phragmites improved COD removal and power density by 28.38% and 68.02%.

9 10

38