Accepted Manuscript

Tertiary Wastewater Treatment in Membrane Photobioreactor using Microal-

gae: Comparison of Forward Osmosis & Microfiltration

Prashant Praveen, Jonathan Yun Ping Heng, Kai-Chee Loh

PII: S0960-8524(16)31391-8
DOI: http://dx.doi.org/10.1016/j.biortech.2016.09.124
Reference: BITE 17147

To appear in: Bioresource Technology

Received Date: 11 August 2016

Revised Date: 27 September 2016
Accepted Date: 29 September 2016

Please cite this article as: Praveen, P., Yun Ping Heng, J., Loh, K-C., Tertiary Wastewater Treatment in Membrane
Photobioreactor using Microalgae: Comparison of Forward Osmosis & Microfiltration, Bioresource Technology
(2016), doi: http://dx.doi.org/10.1016/j.biortech.2016.09.124

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 Tertiary Wastewater Treatment in Membrane
Photobioreactor using Microalgae: Comparison of
Forward Osmosis & Microfiltration

Prashant Praveen, Jonathan Yun Ping Heng, Kai-Chee Loh*

Department of Chemical and Biomolecular Engineering

National University of Singapore

4 Engineering Drive 4, Singapore 117585

*Corresponding author:
Associate Professor, Department of Chemical and Biomolecular Engineering,
National University of Singapore, 4 Engineering Drive 4, Singapore 117585.
Email: chelohkc@nus.edu.sg; Tel.: +65 6516 2174; Fax: +65 6779 1936

1
Abstract

Discharge of wastewater with high nitrogen and phosphorus content is a major cause of

eutrophication. In this study, a microfiltration-based membrane photobioreactor (MPBR) and

forward osmosis-based osmotic membrane photobioreactor (OMPBR) have been operated

with Chlorella vulgaris for continuous tertiary wastewater treatment. Both the bioreactors

exhibited good biomass accumulation (over 2 g/L), although the OMPBR achieved better

nutrients removal due to high rejection properties of the membranes. At 2 days HRT, the

OMPBR achieved nitrogen and phosphorus removal efficiencies of 86-99% and 100%,

respectively, whereas the corresponding values in the MPBR were 48-97% and 46%,

respectively. Based on the energy input, the total operating costs for OMPBR were 32-45 %

higher than that of the MPBR, and filtration cost for OMPBR was 3.5-4.5 folds higher than

that of the MPBR. These results indicate that the integration of membrane filtration with

photobioreactors is promising in microalgae-based tertiary wastewater treatment.

Keywords: Forward osmosis; Membrane bioreactor; Microalgae; Photobioreactor;

Wastewater treatment

2
1 Introduction

Membrane bioreactors (MBR) function through a combination of biological remediation and

membrane separation. These bioreactors offer the advantages of small footprint, high biomass

retention, large loading rates, process flexibility and enhanced effluent quality (Judd, 2008).

MBRs are typically associated with the activated sludge process, and these have commercial

uses in the treatment of both municipal and industrial wastewater (Huang & Lee, 2015).

Recently, MBRs have also found application in nitrogen (N) and phosphorus (P) removal

from tertiary wastewater using autotrophic microalgae (Choi, 2015; Marbelia et al., 2014).

Conventional MBRs have been based on pressure-driven membrane separation techniques,

such as microfiltration (MF) or ultrafiltration (UF). In the past decade however, filtration

based on forward osmosis (FO) has also been investigated as an economical and sustainable

alternative to conventional filtration (Huang & Lee, 2015). FO is akin to natural osmosis,

wherein a draw solution (DS) with high osmotic pressure is used to drive water transport

through semi-permeable membranes (Chekli et al., 2016). FO-based osmotic membrane

bioreactors (OMBR) have the advantages of high solute rejection, low energy costs and

reduced membrane fouling, which have been amply demonstrated in biological wastewater

treatment, as well as in nutrients recovery from wastewater (Achilli et al., 2009; Praveen &

Loh, 2016b; Qiu et al., 2015).

Due to the absence of hydraulic pressure, FO is deemed to be more economical than the

corresponding conventional filtration processes (McGinnis & Elimelech, 2007; Zhao et al.,

2012). However, some recent studies have challenged this notion by demonstrating that FO

can be highly energy intensive if the high cost of DS recycle is added to the cost of filtration

(McGovern & Lienhard, 2014; Semiat, 2008). Furthermore, while the effects of external

concentration polarization (ECP) and salt accumulation on FO performance have been

3
investigated in detail (Luo et al., 2015; Qiu & Ting, 2013), the influence of these factors on

the energy input to the OMBR has not been examined. ECP mitigation requires increase in

DS flow rate, whereas salt accumulation demands high rate of DS supply, and both of these

factors may increase the operating costs (Praveen et al., 2015). As a result, there is ambiguity

on the claims pertaining to the energy efficiency of FO-based processes, and OMBRs may

not be more economical to operate than conventional MBRs. In order to better understand the

energy requirements and efficiency of OMBRs, as compared to conventional MBRs, a

detailed and systematic comparison of these bioreactors is needed. In this research, we have

undertaken such a comparative study between MBRs based on MF and FO filtration in

tertiary wastewater treatment, using microalgae under continuously illuminated conditions.

Tertiary wastewater with high N and P concentrations is a common cause for eutrophication

in natural water bodies (Sulzacova et al., 2015). Although many physical, chemical and

biological methods are being used in tertiary wastewater treatment, the use of microalgae is

advantageous for many reasons (Beuckels et al., 2015; Fernandez et al., 2012): high growth

rates, high N and P uptake rates, generation of microalgal biomass, and greenhouse gas

abatement. Furthermore, photobioreactor inspired by MBRs may provide an alternative to

conventional high rate algae ponds which exhibit low efficiency due to poor light penetration,

low biomass concentration and high bioreactor footprint (Wang et al., 2012). Such high-

retention photobioreactors may also be advantageous over conventional closed

photobioreactors, as the former can be operated in continuous mode at low hydraulic

retention time (HRT), without risk of biomass washout (Marbelia et al., 2014).

The objective of this research was to design and operate a membrane photobioreactor

(MPBR) and an osmotic membrane photobioreactor (OMPBR). The bioreactors were

operated under identical conditions. The energy input to the MPBR and OMPBR were

4
estimated and the bioreactors were compared based on biomass accumulation, nutrients

removal kinetics, efficiency and energy demand. Chlorella vulgaris was used as the model

organism due to its high growth rate, large N and P demand and excellent tolerance to

contaminants in wastewater (Ruiz-Marin et al., 2010).

2 Materials and Methods

2.1 Microorganisms, Culture Conditions, and Chemicals

All the chemicals used in this research were of analytical grade and purchased either from

Sigma-Aldrich (St. Louis, United States) or Merck (Darmstadt, Germany).

Chlorella vulgaris ATCC 13482 used throughout this study was cultivated in Bold’s Basal

Medium (BBM) supplemented with 5% CO2 enriched air at 0.2 gas volumes per reactor

volume per minute (VVM), and provided with 2000 lux light intensity. All media, pipette

tips, and Erlenmeyer flasks fitted with cotton plugs were autoclaved before use.

2.2 OMPBR
2.2.1 Experimental Setup

Fig. 1 shows a schematic of the OMPBR setup. The bioreactor tank (20 cm length x 12.5 cm

width x 22 cm height) had an effective volume of 5.5 L. A plate-and-frame membrane

module was prepared using commercial thin film composite (TFC) FO membranes (HTI,

USA) and the module was immersed in the bioreactor tank for osmotic filtration. Two pieces

of membranes (15 cm length x 12 cm width) were used in the module, resulting in an

effective filtration area of 0.036 m2. The membrane module was designed in such a way that

the active layer faced the wastewater and the support layer faced the DS. A continuous stream

of humidified 5% CO2-enriched air was sparged in the OMPBR at a rate of 0.4 VVM to

provide inorganic carbon to the microalgae. The OMPBR was illuminated from all four sides

and the top using fluorescent lights of 1500-2000 lux intensity. A 2 L reservoir designed with

5
an overflow outlet at 1.5 L provided the DS. The beaker was stirred on a magnetic stirrer and

the DS was recirculated in the membrane module using a peristaltic pump (Masterflex, USA).

DS concentration in the reservoir was maintained constant using a feedback control system

(eChem, Singapore) based on conductivity measurements; dilution of the DS was

compensated through pumping of concentrated DS stock solution into the reservoir. Overflow

from the DS reservoir was collected as OMPBR effluent. The wastewater feed tank was

placed on a weighing balance (Sartorius, Germany) and connected to a PC for periodic

weight monitoring to compute the permeate flux.

For MPBR operation, the setup in Fig. 1 was modified to remove the DS reservoir and the

feedback control. The FO membranes in the membrane module were replaced with PVDF

MF membranes (Newton & Stokes, Singapore), and the effluent was filtered through the

membranes through suction, using a peristaltic pump (Masterflex, USA).

2.2.2 Operation

Synthetic wastewater was used for the bioreactor operation. The wastewater contained: 4

mg/L NH4+-N, 0.35 mg/L NO3--N and 1.8 mg/L PO43--P (Arbib et al., 2014). Other

micronutrients were added to the synthetic wastewater, based on BBM composition, to

prevent nutrient limitation on microalgae growth. The bioreactors were operated at HRTs

varying from 1-2 days with complete biomass retention. Only 10 mL liquid was removed

daily to monitor suspended biomass and nutrients concentrations. The bioreactor pH was

regularly monitored and maintained within 7-7.5. Although microalgae growth in tertiary

wastewater can be affected by medium composition, pH, temperature and light exposure (Shi

et al., 2014), these factors would not have elicited different response in the MPBR and the

OMPBR. Consequently, only the effects of HRTs on the bioreactor performance were

studied.

6
2.3 Analytical Methods

Microalgal biomass density was determined by measuring the optical density (OD) of the

aqueous medium at 540 nm using an ultraviolet-visible spectrophotometer (Shimadzu,

Japan). The OD was used to compute the biomass concentration by the formula: dry cell

weight (mg/L) = 542*OD540 (Praveen & Loh, 2015). The concentrations of NH4 +-N, NO3--N

and PO43--P were measured using phenate method, spectrophotometric method and ascorbic

acid method of standard methods handbook, respectively (APHA et al., 2012). The energy

usage for the equipment was monitored using an Ecoplug energy meter (Solargy, Singapore).

The overall removal efficiency and the average removal rate were calculated based on the

concentration difference between the wastewater and the effluent at steady state as: Removal

efficiency = (1 – Conc. in effluent/Conc. in wastewater) x 100; Removal rate = (Conc. in

wastewater - Conc. in effluent)/HRT. Since the MPBR and OMPBR were operated in

continuous mode, the operation was not repeated for reproducibility. Instead, the

uncertainties associated with the measurement of steady state values were estimated and

expressed in terms of standard deviation. In most of the measurements, the statistical

variations were below 5%.

3 Results and Discussion

3.1 Nutrients Removal in MPBR

Fig. 2 shows the changes in nutrients concentrations over 43 days of MPBR operation. At 2

days HRT, the concentrations of NH4+-N, NO3--N and PO43--P decreased rapidly due to

assimilation by the microalgae, and stabilized after 5-8 days at 0.11 mg/L, 0.19 mg/L and

0.98 mg/L, respectively. The corresponding removal efficiencies were 97%, 46% and 51%,

whereas the average removal rates were 1.94 mg/L-day, 0.08 mg/L-day and 0.41 mg/L-day,

respectively. The removal efficiency of NH4 +-N was higher as compared to the other

7
nutrients, which indicated that it could be the limiting nutrient (Praveen & Loh, 2016a). On

the other hand, relatively low removal efficiency for NO3--N could be attributed to the

favorable uptake of NH4+-N over NO3--N by the microalgae (Di Termini et al., 2011). Effects

of increased nutrients loading rate was next investigated through a decrease in the HRT.

When the HRT was decreased to 1.5 days, the effluent NH4+-N concentration increased to a

maximum of 0.45 mg/L on day 18, before decreasing and stabilizing at 0.24 mg/L. The

overall removal efficiency was 94%, at a removal rate of 2.51 mg/L-day. In comparison, the

change in HRT affected NO3--N removal adversely and its concentration in the effluent

increased monotonically and stabilized at 0.25 mg/L, with a poor removal efficiency of 29%

and a removal rate of 0.06 mg/L-day. Similar changes were observed for PO43--P, for which

the effluent concentration increased to 1.11 mg/L, corresponding to removal efficiency and

removal rate of 38% and 0.46 mg/L-day, respectively. While the changes in NO3--N could be

attributed to a relatively higher accumulation of NH4 +-N in the MPBR, the decrease in PO43--

P removal indicated that the N/P ratio in the MPBR was not ideal (Di Termini et al., 2011).

Despite being the limiting substrate and under operating conditions characterized by a

relatively poor N/P ratio, NH4+-N was not completely exhausted in the MPBR. The MPBR

performance was not affected by nutrients concentrations alone, but there could have been

other factors influencing nutrients uptake by the microalgae. Since the microalgae

concentration was high at this stage, it was possible that light intensity could be a limitation

(Gao et al., 2015).

Similar trends in nutrients removal were obtained in the third and the last stage of MPBR

operation at an HRT of 1 day. After a temporary spike, NH4 +-N concentration stabilized at

0.65 mg/L, with a removal efficiency of 84%, and a removal rate of 3.35 mg/L-day. The

concentration of NO3--N in the MPBR effluent increased to 0.3 mg/L, with a removal

8
efficiency and removal rate of 14% and 0.05 mg/L-day, respectively. The changes in PO43--P

followed a similar trend and PO43--P concentration increased to 1.29 mg/L, which translated

to a low removal efficiency of 28% and removal rate of 0.51 mg/L-day. Although the

increase in nutrients loading rates in the MPBR enhanced the removal rates of NH4 +-N and

PO43--P, the increase was not proportional to the loading rates. These trends are typical during

continuous bioreactor operations, as the contact time between the microorganisms and the

nutrients was lowered at high loading rates. Moreover, several parameters such as light

intensity, microalgae activity and N/P ratio might change in the MPBR with changes in HRT,

which might also affect nutrients removal (Marbelia et al., 2014).

During MPBR operation, even though the removal efficiencies for the nutrients decreased at

lower HRTs, the removal rates for NH4+-N and PO43--P remained high at the high loading

rates. These could be attributed to the higher nutrients availability and increasing biomass

concentration in the bioreactor. For NO3--N, on the other hand, both removal efficiency and

removal rates decreased with decreasing HRTs. This discrepancy in NO3--N removal

augments the hypothesis that the microalgae exhibited poor NO3--N uptake in the presence of

NH4 +-N. These results are consistent with other MPBRs where NO3--N removal was

significantly lower than that of NH4 +-N (Singh & Thomas, 2012).

3.2 Nutrients Removal in OMPBR

Fig. 3 shows the changes in nutrients concentrations over 51 days of OMPBR operation. Due

to the low pore size and high rejection properties of the FO membranes, two different

concentrations profiles developed, on either side of the membranes, for each of the nutrients.

At 2 days HRT, NH4+-N concentration in the OMPBR (Fig. 3a) decreased gradually from 4

mg/L and stabilized at 0.15 mg/L after 12 days. NH4+-N concentration in the effluent

increased to reach a maximum of 0.82 mg/L on day 2, which then decreased gradually to

9
stabilize at 0.03 mg/L after 12 days. The average removal rate and removal efficiency were

computed as 1.94 mg/L-day and 99%, respectively. Contrary to NH4+-N, NO3--N

concentration in the OMPBR (Fig. 3b) remained stable at about 0.3 mg/L during the first 10

days of operation, whereas its concentration in effluent stabilized at 0.04 mg/L after 12 days.

The average removal rate and removal efficiency were computed as 0.15 mg/L-day and 87%,

respectively. PO43--P removal in the OMPBR was nearly complete, and its concentration in

the effluent remained below 0.02 mg/L throughout the operation, resulting in the average

removal rate and the removal efficiency of 0.9 mg/L-day and close to 100%, respectively.

PO43--P concentration in the OMPBR (Fig. 3c) increased slowly to reach 2 mg/L after 12

days, but it gradually decreased thereafter to 1.54 mg/L at the end of the first stage of

operation on day 16.

During municipal wastewater treatment in OMBRs, a high accumulation of nutrients in the

OMBR in the first few days of operation is typical (Achilli et al., 2009; Praveen & Loh,

2016b). This accumulation is attributed to the low pore size of the active layer of the FO

membranes, which imparts the membranes high solute rejection properties. The accumulation

trend is reversed after a few weeks of operation, when there is large biomass accumulation in

the bioreactor. However, no such accumulation has been observed during the OMPBR

operation, even though the concentration profiles developed on either side of the FO

membranes were widely different and nutrients rejection by the membranes was excellent.

While NO3--N and PO43--P concentrations in the OMPBR remained flat during the first few

days of operation, there was no accumulation of NH4 +-N and its concentration in the OMPBR

decreased monotonically until it matched the concentration in the effluent. Two conclusions

can be drawn from these results: (1) the loading rates of the nutrients at 2 days HRT was not

very high, and these could be matched by the nutrients uptake rate exhibited by the

microalgae, and; (2) microalgal uptake rate was highest for NH4+-N, which indicated that

10
NH4 +-N was the limiting nutrient for microalgae growth and metabolism (Gao et al., 2015).

While these results are consistent with the findings obtained during the MPBR operation,

these also highlight the role of membranes in nutrients removal in the OMPBR, especially in

the removal of PO43--P. Since the removal efficiency for PO43--P was the highest even though

it was not the limiting nutrient and the wastewater had low N/P ratio, the removal of PO43--P

was mainly through membrane rejection. Such high rejection efficiency of PO43--P has been

reported in literature, and it has also been used to design novel OMBR configurations for

PO43--P recovery from wastewater (Qiu et al., 2015).

When nutrients concentrations in the effluent had stabilized after 16 days of OMPBR

operation at 2 days HRT, the HRT was reduced to 1.5 days and the corresponding nutrients

loading rates was increased. Under the new operating conditions, there was an immediate

increase in nutrients accumulation in the bioreactor. NH4+-N concentration increased to a

maximum of 0.94 mg/L on day 20, whereas the concentration in the effluent increased to a

maximum of 0.19 mg/L in the same period. However, these spikes were temporary and

NH4 +-N levels in the OMPBR and in the effluent soon decreased, and stabilized at 0.44 mg/L

and 0.07 mg/L, respectively, on day 34. The removal efficiency and average removal rate

were determined as 98% and 2.62 mg/L-day, respectively. Contrary to NH4+-N, NO3--N

concentrations on both sides of the FO membranes continued to rise and stabilized at higher

levels on days 27-28. On day 34, NO3--N concentrations in the OMPBR and in the effluent

were 0.62 mg/L and 0.17 mg/L, respectively, with a removal efficiency of 63% and a

removal rate of 0.15 mg/L-h. PO43--P concentration in the OMPBR was also affected by the

decreased HRT. PO43--P concentration increased monotonically up to day 28 and stabilized at

3.7 mg/L, which was nearly double the concentration in the feed wastewater. On the other

hand, PO43--P concentration in the effluent remained unchanged throughout the operating

11
period. The consequent removal efficiency was close to 100% and the average removal rate

was 1.2 mg/L-day.

During the second stage of OMPBR operation (1.5 days HRT), the nutrients loading rates

were 25% higher and a spike in nutrients concentration in both the OMPBR and effluent

streams were expected. The increase in concentrations were expected to be temporary though,

as the increase in biomass concentration and the consequent increase in the nutrients uptake

rate could reverse the accumulation trends. While such a trend was observed in NH4+-N

removal, NO3--N and PO43--P concentrations in the OMPBR increased monotonically

throughout this operating period. The effluent PO43--P concentration remained undetectable

despite PO43--P accumulation in the OMPBR because of FO-based filtration rather than

biological assimilation. It was also observed that the removal rates for NH4 +-N and PO43--P

increased at higher loading rates, but there was no appreciable changes in the removal rate of

NO3--N and it remained at 0.15 mg/L-day. This again indicated the preferential uptake of

NH4 +-N over NO3--N by the microalgae, as was observed during MPBR operation.

Having achieved stable concentration profiles, nutrients loading rate to the OMPBR was

increased further on day 35 by adjusting the HRT to 1 day. Under this operating condition,

the concentrations of the nutrients adjusted quickly in the OMPBR. NH4+-N concentration in

the bioreactor increased to a maximum of 4.5 mg/L and then decreased to stabilize at 3.5

mg/L. On the other hand, NO3--N and PO43--P concentrations in the bioreactor increased

monotonically, and stabilized at 1.41 mg/L and 8.36 mg/L, respectively. After 51 days of

operation, NH4+-N level in the effluent had stabilized to 0.31 mg/L, with a removal efficiency

of 92% and a removal rate of 3.7 mg/L-day, whereas NO3--N concentration in the effluent

was 0.24 mg/L with corresponding removal efficiency and rate of 31% and 0.11 mg/L-day,

respectively. On the contrary, despite the large increase in the loading rate and high PO43--P

12
accumulation in the OMPBR, PO43--P concentration in the effluent remained below the

detection limits, again resulting in close to 100% removal, whereas the removal rate

increased proportionately to the loading rate to 1.8 mg/L-day.

At 1 day HRT, some deterioration in OMPBR performance was observed. Although the

NH4 +-N and PO43--P removal were still excellent, there was substantial increase in their

accumulation in the OMPBR, notwithstanding the presence of a large and growing amount of

biomass in the bioreactor. Even NH4+-N, which was the limiting nutrient, exhibited

temporary accumulation in the bioreactor. Therefore, it was possible that there were changes

in the metabolic activity of the microorganisms during OMPBR operation. Nevertheless, the

effluent concentrations for the nutrients were below the discharge limit under all the

operating conditions (Boelee et al., 2012; Ji et al., 2013). Moreover, effluent quality in the

OMPBR was better than that observed in the MPBR, which demonstrated the advantages of

integrating microalgal bioremediation with FO-based membrane filtration.

Changes in the activity and diversity of the microorganisms with time are common

phenomena in OMBRs during municipal wastewater treatment using activated sludge. These

changes have been attributed to the gradual increase in the salinity of the OMBR, due to salt

rejection by the FO membranes and reverse DS permeation through the FO membranes

(Huang & Lee, 2015; Qiu & Ting, 2013). Fig. S1 shows salinity profiles of the OMPBR over

time. It can be seen that salinity increased gradually and monotonically throughout the

operating period, and the conductivity of the OMPBR was 30 mS after 51 days of operation.

In contrast, the optimal growth medium (BBM) for microalgae had a conductivity of only

about 3 mS. Since freshwater microalgae, such as C. vulgaris, do not have high salt tolerance

(Shen et al., 2015), it was likely that the lower microalgae activity (hence relatively low

nutrients removal) during the last stage of OMPBR operation (1 day HRT) was a

13
consequence of the high salt levels in the bioreactor. It can also be seen from Fig. S1, that the

contribution of accumulated nutrients in the OMPBR to the overall salinity was insignificant.

It can therefore be concluded that the change in the salinity of the OMPBR was driven mainly

by reverse diffusion of DS through the FO membranes.

Salt accumulation is considered one of the biggest challenges to the sustainability of OMBRs.

Not only is the presence of high salt concentrations in the bioreactors harmful for biomass

growth and metabolism, salinity increase in the bioreactor also necessitates an increase in the

DS concentration to maintain the HRT (Huang & Lee, 2015). This would enhance the risk of

concentration polarization, consequently accelerating salt accumulation in the bioreactor, as

well as increase operating costs since it would be necessary to increase the DS strength to

maintain the constant HRT. Literature has indicated that the best strategy to alleviate this

challenge would be to improve membrane design for better salt rejection (Phillip et al., 2010),

and innovative engineering design of the bioreactors (Luo et al., 2015).

3.3 MPBR & OMPBR Comparison

3.3.1 Cell Growth & Biomass Accumulation

Fig. 4 shows the changes in the suspended microalgal biomass concentration in the MPBR

and the OMPBR. In both bioreactors, biomass concentration profiles followed similar trends.

During the first 14-17 days of operation, the biomass concentration in suspension increased

monotonically and reached a maximum of 228 mg/L in the MPBR and 278 mg/L in the

OMPBR. The increase in biomass concentration was characterized by the dark green color of

the microalgal suspension. Although further increase in biomass concentration was expected

in the bioreactors, it did not happen. On the contrary, there was a gradual decline in the

suspended biomass concentration in the bioreactors and the intensity of the greenish

suspension faded gradually. After 35 days of operation, suspended microalgae concentration

14
in both the bioreactors had stabilized at 10-20 mg/L, and the microalgae suspension looked

almost clear.

The reason for this change in the color of the cell suspension was mainly due to the gradual

sedimentation of the microalgal biomass to the bottom of the bioreactor tank due to the lack

of any mechanical mixing. Although attempts were made to improve mixing at the bottom of

the tank using a magnetic stirrer, the rectangular design of the bioreactor tank prevented

efficient mixing and the biomass settled mainly in the un-mixed areas. In addition, C.

vulgaris also exhibited a high tendency to attach to the acrylic surfaces of the bioreactors and

a visible amount of attached biomass was observed on the surfaces after 3 weeks of operation

in both bioreactor setups. Furthermore, the microalgae also exhibited a high tendency to self-

aggregate, which accelerated the rate of sedimentation. The biomass aggregation and

attachment were most visible when microalgae concentration had reached a relatively high

concentration in the bioreactors. The process of biomass attachment and sedimentation were

independent of the nutrients loading rates. It was also apparent that most of the biomass

produced during the later stages of operation remained in attached or aggregated form, and

played a major role in nutrients removal. Since the biomass attached to the walls of the

bioreactor tank were better illuminated as compared to those at the bottom surface, it was

likely that the contribution of the attached biomass in the bioremediation was much higher

than those settled at the bottom.

Since the suspended microalgae concentration was representative of the actual biomass

concentration in the MPBR/OMPBR only in the first 3 weeks of operation, the biomass from

the MPBR and OMPBR were collected at the end of the operation to estimate the actual

amount of biomass in the bioreactors. The collected biomass included the settled and

suspended biomass, as well as the biomass attached to the surfaces, although not all the

attached biomass could be completely recovered. The measurements were performed using

15
both absorbance, as well as dry cell weight estimation. It was found that the total biomass

accumulated in the OMPBR was well over 2 g/L. These results indicate the potential of the

OMPBR in accumulating very high concentration of microalgal biomass, which is consistent

with other studies reporting microalgae cultivation in MBRs (Choi, 2015; Gao et al., 2015;

Praveen & Loh, 2016a).

The high rate of biomass attachment to the surfaces and the high tendency to aggregate can

be explained based on high production and accumulation of extracellular polymeric

substances (EPS) by microalgae in the bioreactor, or changes in the zeta potential of the

microalgae (Gerde et al., 2014; Wang et al., 2014). The zeta potential of the microalgae had

decreased by nearly four times during the operating period, whereas there was significant

increase in EPS concentration in the bioreactors.

3.3.2 Removal Rate & Efficiency

Fig. 5 summarizes the removal efficiencies of the nutrients in the MPBR and the OMPBR at

different HRTs. It is obvious that the removal of all the three nutrients was higher in the

OMPBR. While the removal efficiencies for NH4+-N and NO3--N in the two bioreactors

differed by 2-8% and 17-41%, respectively, the difference was 49-72% for PO43--P, under

different operating conditions. Some extent of performance deterioration was observed for

both the bioreactors when these were operated at lower HRTs, but the OMPBR effluent

quality remained better than that of the MPBR.

The differences between the removal efficiencies of the MPBR and the OMPBR were also

reflected in the corresponding removal rates, as shown in Fig. 6. Once again, the removal

rates in the OMPBR were better for all the three nutrients under all the different operating

conditions. While the difference in the average removal rates between the OMPBR and the

MPBR for NH4+-N was only about 10%, for NO3--N, it was 46-60% and 54-72% for PO43--P.

16
The removal rates, in general, increased at lower HRTs, and PO43--P removal rate in the

OMPBR increased proportionately with the loading rates under different HRTs, resulting in

significant differences between the performances of the two bioreactors. It was also observed

that unlike NH4 +-N and PO43--P, NO3--N removal rates in both the bioreactors decreased

when the HRTs were lowered. This anomaly in the removal trend could again be due to the

increased accumulation of NH4+-N in the OMPBR, which was the preferred N-source for the

microalgae.

Since MPBR and OMPBR operations were carried out under identical conditions, and using

equivalent amounts of microalgae inoculum, it is reasonable to assume that the difference in

the removal efficiencies was not due to microbial metabolism; the difference between the

performances of the MPBR and OMPBR were due to the differences in the filtration

performance of MF and FO.

Table 1 shows comparison of the performance of the MPBR and the OMPBR with

membrane-based photobioreactors previously reported in literature. Biomass accumulation

and nutrients removal trends and the removal efficiencies in the MPBR were consistent with

the other studies. On the other hand, the nutrients removal kinetics in the OMPBR was

different from those reported in literature, and the removal efficiency was comparatively

better. A relatively higher biomass accumulation was observed in this study, which could be

attributed to a lower HRT and complete biomass retention maintained during the operation.

3.3.3 Filtration and Salt Accumulation

Fig. S2 (supplementary data) shows the changes in the permeate flux and the HRT during the

MPBR and the OMPBR operation. In the MPBR, the flux remained relatively constant during

the 43 days of operation without adjustment in the hydraulic pressure. Although SEM images

of the MF membranes at the end of operation indicated significant microalgae attachment on

17
the membranes (images not shown), the biofouling potential of the microalgae was typically

lower than that of bacteria and activated sludge (Bilad et al., 2014). Besides, the permeate

flux of 3.18-6.37 LMH was relatively low for MF, and the extent of biofouling might not

have been significant to affect the relatively low flux. Compared to MPBR, the variation in

the permeate flux was higher in the OMPBR, which could have been caused by: biofouling,

salt accumulation and concentration polarization (Zhao et al., 2012). Since microbial growth

and other characteristics in the MPBR and OMPBR were similar, and the bioreactors were

operated under identical operating conditions, it was unlikely that the membrane biofouling

would have been more severe in the OMPBR, especially in the absence of any hydraulic

pressure in FO-based filtration. On the other hand, the increase in the salinity of the OMPBR

(Fig. 5) resulted in changes in the net osmotic pressure gradient across the FO membranes,

which could have resulted in a decrease in the permeate flux. Although the strength of the DS

was increased over time to neutralize the effects of the increased salinity in the OMPBR,

these changes were not instantaneous and might be responsible for the variations.

Furthermore, during long-term operation of the FO-based processes, the accumulation of salts

inside the membranes, also known as internal concentration polarization (ICP) might also

decrease the effective osmotic pressure gradient and lower the permeate flux (Praveen et al.,

2015). This could be further aggravated when high strength saline solutions were present on

both sides of the membranes, as observed during the last stage of OMPBR operation at 1 day

HRT.

3.3.4 Energy Input

It has been reported that one of the advantages of FO is the low energy requirement of the

process, as compared to other pressure driven filtration processes such as MF (McGinnis &

Elimelech, 2007). However, based on the laboratory-scale bioreactors setup used in this

study, it is obvious that the OMPBR setup was more complex and needed more equipment as

18
compared to that of the MPBR. Although the permeate flux was independent of the DS flow

rate in the OMPBR, the DS had to be circulated above a minimum flow rate (>50 rpm) to

prevent the adverse effects of ECP on the flux. Moreover, the increase in the salinity of the

OMPBR during the operation required gradual increase in DS strength, which would

contribute to an increase in the operating costs. On the contrary, the setup for the MPBR was

relatively simple, and the operating conditions were very straightforward. It was also

observed that there was no significant increase in the transmembrane pressure (TMP) during

the operation.

In order to investigate and compare the energy efficiency of the MPBR and OMPBR further,

the energy input to the two bioreactors were measured using an energy meter and the results

are summarized in Table 2. It can be seen that the energy input to the OMPBR was higher

due to the costs of operating the extra pump, magnetic stirrer and the feedback control

system. It should be noted that the cost of gas sparging was not taken into account (since gas

sparging costs were the same for both the bioreactors).

The fundamental difference between the MPBR and OMPBR was in the way the effluent was

drawn from the bioreactor tanks. During OMPBR operation, the peristaltic pump used to

recirculate DS in the membrane module was operated above 50 rpm, using 3.1 mm internal

diameter (ID) silicone tubing, to prevent the occurrence of ECP (data not shown). The pump

speed remained constant throughout the operating period as the DS flow rates did not

influence the HRT. However, the OMPBR setup also included a second peristaltic pump

which was used to add concentrated DS stock solution in the DS reservoir to maintain a

constant DS concentration in the reservoir. The second peristaltic pump was activated every

time the salinity of the DS reservoir dropped below the set value. The duration for which the

pump was operated depended on the HRT, bioreactor salinity and the DS concentration. For

19
example, the pump was operated for longer duration at lower HRT when the DS was diluted

faster, and vice versa.

On the contrary, the MPBR setup was simple with a single peristaltic pump used to draw

water directly through the MF membranes. Since ECP was not an issue, the pump speed was

regulated based only on the HRT. It was also observed that the MF membrane module could

draw a large volume of water even at a very low pump speed. For example, even at the lowest

speed of 3 rpm (using 3.1 mm ID tubing) and negligible TMP (pressure could not be detected

using pressure gauge), the water drawn by the peristaltic pump was > 12 mL/min, whereas

the actual requirement at all times was < 4 mL/min. Consequently, the peristaltic pump in the

MPBR setup had to be operated with smaller tubing of 0.8 mm ID to maintain the flux in the

required range. In order to make a fair comparison, the operating cost for the MPBR was

calculated assuming the pump speed 3 rpm and tubing size of 3.1 mm ID. Since water drawn

through MF in the MPBR at 3 rpm (using 3.1 mm ID tubing) was higher than that required in

the actual operation, the operating cost calculated for MPBR was higher than the actual cost

of operation.

Based on Fig. S3 (supplementary data) and Table 2, the cost of operating the MBR was < $

0.22 day-1 throughout the operating period under different HRTs. On the other hand, the costs

for OMPBR varied between s$ 0.29-0.32 day-1 depending on the HRTs. Consequently, the

cost of OMPBR operation at 2 days, 1.5 days and 1 day HRTs were 32%, 36% and 45%

higher than those for the MPBR, respectively. It was also observed that the cost of bioreactor

illumination was the highest among all, and it was more than the cost of operating all the

other equipment taken together. It was also observed that the cost of filtration in OMPBR was

3.5-4.6 folds higher than that in the MPBR. While the cost of DS recirculation was the

highest contributor to the filtration cost, the feedback control system too was energy

20
intensive, especially during the last stage of operation, when the HRT was lower and the

salinity of the bioreactor was high.

While these results are not in agreement with most of the early literature on FO-based

filtration, where FO has been described as more economical than conventional filtration

process (McGinnis & Elimelech, 2007; Zhao et al., 2012), these are consistent with recent

studies highlighting the high operating costs of FO-based processes (McGovern & Lienhard,

2014; Semiat et al., 2010). Some of these studies have demonstrated that the cost of recycling

and concentrating the DS from the diluted effluent is very high, and FO cannot energetically

outperform traditional filtration processes, including RO. This implies that the cost of

OMBRs with DS recycle will never be lower than the cost of conventional MBR. In this

research however, the costs of the DS and the costs of DS recycle were not considered in the

energy calculations. Despite that, the total operating cost of the OMPBR was higher than that

of the MPBR.

The large difference between the operating costs of the MPBR and OMPBR could be a result

of operating the bioreactor at a relatively low flux (< 4 mL/min). Under these operating

conditions, the TMP in the MPBR was very low particularly since the effective membrane

area was relatively high at 360 cm2. On the other hand, DS recirculation in the OMPBR was

independent of the permeate flux. Therefore, if the bioreactors had been operated at a lower

HRT of 6-8 h, it is possible that the operating costs of the MPBR could have risen faster than

that of the OMPBR. It is also possible that the OMPBR could have been more effective, if the

bioreactor operation had been longer and there was significant membrane biofouling, as the

cost of traditional MBR operation under fouling conditions is typically higher than that of the

OMBRs (Luo et al., 2015). The cost of OMPBR operation can also be lowered significantly if

seawater or wasted brine solution from desalination plants were to be used, which are readily

available and do not need any recycling (Van der Bruggen & Luis, 2015). In such a scenario,

21
continuous supply of the DS will obviate the need for DS recirculation, resulting in additional

cost savings. Nevertheless, based on this study, using the laboratory-scale bioreactors setup,

the operating costs of the OMPBR was significantly higher than that of the MPBR. Besides,

the OMPBR also resulted in various operating challenges, especially due to salt

accumulation, which must be mitigated to sustain OMPBR performance in long-term

operation.

4 Conclusions

The integration of membrane filtration with photobioreactors in both MPBR and OMPBR has

enormous implications in microalgae-based wastewater treatment processes. These

bioreactors allow high biomass retention independent of the HRT, and yield high removal

rates and efficiency. However, there are several challenges pertaining to filtration: biofouling,

concentration polarization and salt accumulation, which must be addressed to make this

technology more economical and sustainable. Since bioreactor illumination constituted the

dominated component of the operating costs, future studies should harness solar irradiation to

lower the operating cost of MPBR/OMPBR.

Acknowledgement

This research was funded by the Singapore National Research Foundation under its

Competitive Research Program for the project entitled, “Advanced FO Membranes and

Membrane Systems for Wastewater Treatment, Water Reuse and Seawater Desalination”

(Grant Number: R-279-000-338-281).

22
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27
Figure Captions

Figure 1 Schematic diagram of the OMPBR setup: (1) compressed air; (2) compressed CO2;

(3) flow meter; (4) humidification tank; (5) MBR tank; (6) membrane module; (7) air

diffuser; (8) feed tank; (9) weighing scale; (10) stirring plate; (11) DS; (12) concentrated DS

stock; (13) effluent; (14) peristaltic pump; (15) conductivity meter, and; (16) data logger

Figure 2 Kinetics of nutrients removal and removal efficiency in MPBR: (a) NH4+-N; (b)

NO3--N, and; (c) PO43--P

Figure 3 Kinetics of nutrients removal and removal efficiency in OMPBR: (a) NH4+-N; (b)

NO3--N, and; (c) PO43--P

Figure 4 Suspended biomass concentrations in MPBR and OMPBR during wastewater

treatment

Figure 5 Comparison of nutrients removal efficiencies in MPBR and OMPBR at different

HRTs: (a) NH4+-N; (b) NO3--N, and; (c) PO43--P

Figure 6 Comparison of nutrients removal rate in MPBR and OMPBR at different HRTs: (a)

NH4 +-N; (b) NO3--N, and; (c) PO43--P

28
Figure 1

29
 HRT = 2 days HRT = 1.5 days HRT = 1 day

(a)

(b)

2.0 100
(c)
Removal efficiency (%)

80
PO43--P conc. (mg/L)

1.5
60
1.0
40
0.5
20

0.0 0
0 5 10 15 20 25 30 35 40
Time (days)

Figure 2
30
 HRT = 2 days HRT = 1.5 days HRT = 1 day

(a)

(b)

10 100
Removal efficiency (%)

(c) 8 80
PO43--P conc. (mg/L)

6 60

4 40

2 20

0 0
0 5 10 15 20 25 30 35 40 45 50
Time (days)

Figure 3

31
 300

250
Biomass conc. (mg/L)

OMPBR
200
MPBR
150

100

50

0
0 5 10 15 20 25 30 35 40 45 50
Time (days)

Figure 4

32
 105
(a) MPBR OMPBR

NH4+-N removal efficiency (%)

100

95

90

85

80

75
2 1.5 1
HRT (days)

100
(b) MPBR OMPBR
NO3--N removal efficiency (%)

80

60

40

20

0
2 1.5 1
HRT (days)

(c) 120 MPBR OMPBR

PO43--P removal efficiency (%)

100

80

60

40

20

0
2 1.5 1
HRT (days)

Figure 5

33
 4.0

NH4+-N removal (mg/L-day)

(a) MPBR OMPBR
3.0

2.0

1.0

0.0
2 1.5 1
HRT (days)

0.20
(b) MPBR OMPBR
NO3--N removal (mg/L-day)

0.16

0.12

0.08

0.04

0.00
2 1.5 1
HRT (days)

2.0
MPBR OMPBR
PO43--P removal (mg/L-day)

(c)
1.6

1.2

0.8

0.4

0.0
2 1.5 1
HRT (days)

Figure 6

34
Table 1 Comparison of MPBR and OMPBR performance with other studies

Max.
Wastewater
HRT cell %N %P
Microalgae composition Reference
(days) conc. removal removal
(mg/L)
(g/L)

NH4 +-N = 15 Gao et al.,

C. vulgaris 2 1.37 95-96 85-86
PO43--P = 0.8 2015

C. vulgaris,
TN = 7.5 Honda et
B. braunii, 1-2 0.92 91 60
TP = 0.15 al., 2012
S. platensis

C. vulgaris, TN = 6.81 Gao et al.,

1 1.1 86.1 82.7
S. obliquus TP = 0.42 2016

TN = 40.02 Choi,
C. vulgaris 3.4 - 96.4 92.8
TP = 9.24 2015

TN = 7-22 Marbelia
C. vulgaris 2 0.7 80 50-80 et al.,
TP = 1.6-2.2 2014

TN = 18.8 Boonchai
Chlorophyceae
2 1.3 66.5 94.5 & Seo,
sp. TP = 1.01 2015

NH4 +-N = 8-22 Praveen &

C. vulgaris 2-4 5 95 89 Loh,
PO43--P = 2.4-6 2016a

NH4 +-N = 25-30 Singh &

Chlorella sp.
1.6 - 50 60 Thomas,
Scenedesmus sp. PO43--P = 8-12 2012

TN = 9.51 Xu et al.,
C. vulgaris < 0.5 1.5 73.4 91.3
TP = 1.81 2015

NH4 +-N = 4 MPBR, MPBR,

This
C. vulgaris 1-2 2 84-97; 28-47;
PO43--P = 1.8 study
OMPBR, OMPBR,

35
92-99 100

36
Table 2 Energy input and operating costs of MPBR and OMPBR

OMPBR MPBR

OMPBR Power (kWh) Cost ($) MPBR Power (kWh) Cost ($)

Weighing scale 0.004 0.012 Weighing scale 0.004 0.012

Lights 0.050 0.143 Lights 0.050 0.143

Feed Pump 0.013 0.037 Feed Pump 0.013 0.037

DS pump 0.024 0.070 DS pump - -

Stirring plate 0.008 0.023 Stirring plate - -

Sub-Total 0.099 0.286 Sub-Total 0.067 0.192

Feedback control Microfiltration

2 days HRT 0.002 0.006 2 days HRT < 0.0096 < 0.028

1.5 days HRT 0.005 0.014 1.5 days HRT < 0.0096 < 0.028

1 day HRT 0.012 0.035 1 day HRT < 0.0096 < 0.028

Total Total

2 days HRT 0.101 0.292 2 days HRT < 0.0766 < 0.220

1.5 days HRT 0.104 0.300 1.5 days HRT < 0.0766 < 0.220

1 day HRT 0.111 0.321 1 day HRT < 0.0766 < 0.220

*Based on electricity cost of US$ 0.12 per kWh

37
Highlights

• Forward osmosis and microfiltration based membrane photobioreactors were operated

• Bioreactors exhibited excellent N and P removal efficiency

• Membrane rejection played important role in osmotic membrane photobioreactor

• More than 2 g/L microalgae were accumulated in the bioreactor

• Operating costs for FO-based system was 32-45% higher

38