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Intimate coupling of photocatalysis and biodegradation for degrading phenol using different light types: visible light vs. UV light Dandan Zhou, Zhengxue Xu, Shanshan Dong, Ming-xin Huo, Shuangshi Dong, Bin Cui, Xiadi Tian, Houfeng Xiong, and Tingting Li Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 15 Jun 2015 Downloaded from http://pubs.acs.org on June 15, 2015

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Environmental Science & Technology

ACS Paragon Plus Environment


1 2 3 4

Intimate coupling of photocatalysis and biodegradation for degrading phenol using different light types: visible light vs. UV light

5 6

Dandan Zhou†‡, Zhengxue, Xu†, Shanshan Dong†, Mingxin Huo*‡, Shuangshi

7

Dong*†§, Xiadi Tian†, Bin Cui†, Houfeng Xiong†, Tingting Li†, Dongmei Ma†

8 9 10

†

Key Lab of Groundwater Resources and Environment, Ministry of Education, Jilin

University, Changchun 130021, China

11 12

‡

School of Environment, Northeast Normal University, Changchun 130117, China

§

State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of

13 14 15

Technology (SKLUWRE, HIT), Harbin 150090, China

16 17

ABSTRACT

18

Intimate coupling of photocatalysis and biodegradation (ICPB) technology is

19

attractive for phenolic wastewater treatment, but has only been investigated using UV

20

light (called UPCB). We examined the intimate coupling of visible-light-induced

21

photocatalysis and biodegradation (VPCB) for the first time. Our catalyst was

22

prepared doping both of Er3+ and YAlO3 into TiO2 which were supported on A


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1

macroporous carriers. The macroporous carriers was used to support for the biofilms

2

as well. 99.8% removal efficiency of phenol was achieved in the VPCB, and this was

3

32.6% higher than that in the UPCB. Mineralization capability of UPCB was even

4

worse, due to less adsorbable intermediates and cell lysis induced soluble microbial

5

products release. The lower phenol degradation in the UPCB was due to the serious

6

detachment of the biofilms, and then the microbes responsible for phenol degradation

7

were insufficient due to disinfection by UV irradiation. In contrast, microbial

8

communities in the carriers were well protected under visible light irradiation and

9

extracellular polymeric substances secretion was enhanced. Thus, we found that the

10

photocatalytic reaction and biodegradation were intimately coupled in the VPCB,

11

resulting in 64.0% removal of dissolved organic carbon. Therefore, we found visible

12

light has some advantages over UV light in the ICPB technology.

13 14

15

Phenolic compounds are bio-recalcitrant organic pollutants, and they are common

16

components of some industrial wastewaters, such as oil refining, coking plants, steel

17

industry, ceramic industry, and textile processing wastewaters 1,2. Advanced oxidation

18

processes (AOPs) are techniques that are effective at degrading phenol, but it is

19

difficult to achieve the full mineralization 1,3,4. Although biological treatment has been

20

used as cost-efficient technique for many years

21

phenolic compounds which are bio-recalcitrant. Thus, combined treatment processes

22

have been proposed to degrade phenol, such as, AOP followed by a biological

INTRODUCTION

1,5

, they are limited to degrading

B



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1

treatment 4 or a biological treatment followed by an AOP 6-8. Several problems exist

2

when using combined treatment. First, AOPs rely on hydroxyl radical reactions,

3

which are indiscriminate, and some less biodegradable products can be formed.

4

Second, we should oxidize the organics only to the degree that they are easily

5

biodegraded and not overly oxidized which would waste energy and/or oxidizing

6

chemicals 3. Third, it may difficult to achieve the special conditions that is required by

7

AOPs (for example, the proper pH and/or low turbidity).

8

A novel alternative to the sequential combined treatments is the intimate coupling

9

of photocatalysis and biodegradation (ICPB), which was firstly proposed by Marsolek

10

et al 9. For the ICPB, macroporous biofilm-carrier sponge cubes with 3.5 - 4.0 mm in

11

side length were coated by TiO2 and were used to accumulate biomass. TiO2

12

photocatalysis produced free radicals that transformed the phenolic compound into

13

more easily bio-consumable intermediates. These bio-consumable intermediates were

14

degraded by the attached biomass in a single reactor. And then the ICPB process was

15

investigated with the aim of enhancing the removal of phenolic organics

16

complex compounds

17

carrier cube was free of bacterial cells due to the participation of photocatalytic

18

reaction. And only some bacteria inside the macroporous carrier were alive, growing

19

as a biofilm, and metabolically active. The protected biofilm that remained had a

20

substantial substrate removal capacity in the ICPB process and was found to be the

21

main contributor to the removal of the chemical oxygen demand (COD) or dissolved

22

organic carbon (DOC) 1, 3,9.

10, 11

1

and even

from wastewater. It was found that the exterior face of the

C


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1

In fact, UV light, which accounts for less than 4% of the entire solar spectrum 12,

2

is the only light source that has been used for previous ICPB studies. Exposure to UV

3

light will definitely destroy biofilm on the exterior of the carriers, and could

4

potentially affect the biofilm in the interior of the carrier. For the ICPB that used UV

5

light, detached biofilms was found suspending in the bulk water and this interfered

6

with irradiance of the photocatalyst, wasted energy, and degraded the reactor

7

performance. Worse yet, soluble microbial products (SMPs) could potentially release

8

to the effluent from an intimate coupling of UV photolysis/photocatalysis and

9

biodegradation (UPCB), due to the attack of the strong free radicals on the biofilms.

10

Actually, higher DOC concentrations were found in the UPCB effluent than using

11

photodegradation alone 9, even though most of present publications revealed that

12

biofilms could be well protected in the porous carriers with size of 3.5-8.0 mm (see

13

Table S1). But, smaller carrier is expected to be employed, which could take greater

14

surface-area-to-volume ratio to achieve more exposure of catalysts on the carrier

15

surface. Thus, ICPB, a novel attractive process, still meets many challenges, such as

16

high operational energy, and even potentially SMP releasing if small carrier applied.

17

Indeed, UV light employed in the ICPB system led to these problems.

18

Visible light photocatalysis has recently attracted a lot of attention

13-15

. Good

19

degradation efficiencies have been achieved for many kinds of inhibitory or

20

recalcitrant pollutants using visible light photocatalysis, followed by a biological

21

process to enhance the mineralization of the pollutants 16. Our hypothesis is that the

D



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1

problems mentioned above, could be solved by using an intimate coupling of

2

visible-light-induced photocatalysis and biodegradation.

3

In the present work, we compared the degradation of phenol using intimate

4

coupling of visible-light-induced photocatalysis and biodegradation (VPCB) and

5

ultraviolet-light-induced

6

degradation and mineralization, biofilms development, extracellular polymeric

7

substances distributions and microbial community changes were examined, and the

8

advantages of using VPCB over using UPCB were determined. The results were also

9

directly compared with those findings using protocols of only biodegradation,

10

visible-light photocatalysis alone or UV-light photocatalysis alone. To our best

11

knowledge, this is the first report on the use of VPCB.

12

photocatalysis

and

biodegradation

(UPCB).

Phenol

MATERIALS AND METHODS

13

Production of the synthetic wastewater containing phenol. Phenol was

14

purchased from the Beijing Chemical Works (99%, China). Synthetic wastewater was

15

prepared by adding 50 mg/L of phenol and supplemental inorganic salt to ultra-pure

16

water. The supplemental inorganic salt was composed of 29 mg/L of NH4Cl, 8 mg/L

17

of Na2HPO4·2H2O, and 4 mg/L of NaH2PO4.

18

Sponge cube and Photocatalyst coating procedure. The sponge in this study is

19

2mm×2mm×2 mm cube and made of polyurethane. The wet density of the pristine

20

and phtocatalyst coated sponge is 0.89 and 1.04 g/mL, respectively, with 100-300 µm

21

in the pore size and 87 % in porosity. Full and close-up views of the sponge were

22

provided in Supporting Information (Figure S1). The preparation of Er3+:YAlO3/TiO2 E


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1 2

photocatalyst and its characterization has been described in our previous publication 14

. The Er3+:YAlO3/TiO2 samples were ultrasonically dispersed in C2H5OH to give a

3

17.95 g/L nanoparticle suspension. Then, 8 g of uncoated sponge carrier cubes

4

(Hayi-diverse, Yixing, China)were added to 400 mL of the coating solution, and this

5

was ultrasonically dispersed and incubated in an oven at 80 °C for 5 h (mixed every

6

30 min) until all of the liquid had evaporated, and the Er3+:YAlO3/TiO2 was coated on

7

the carriers. Finally, the coated carriers were ultrasonically treated for 5 min and

8

rinsed by deionized water. This rinsing process was repeated 3 times.

9

Biofilm cultivation procedure. Activated sludge was obtained from the underflow

10

of a secondary clarifier at the Southern Municipal Wastewater Treatment Plant in

11

Changchun, China. The photocatalyst-coated carriers were immersed in the activated

12

sludge for 24 h and then the carriers were cultivated in an internal loop airlift-driven

13

reactor described in our previous publication17. The biofilms were cultivated using a

14

synthetic feed water that contained 330 mg/L of sodium acetate, 29 mg/L of NH4Cl, 8

15

mg/L of Na2HPO4·2H2O, and 4 mg/L of NaH2PO4. During cultivation, dissolved

16

oxygen was maintained at 5±1 mg/L, the temperature was kept at room temperature

17

(20±2 °C), and the cultivation time was 6 d.

18 19

Figure 1. The schematic of the photolytic circulating-bed bioreactor (PCBBR) F



1

Photolytic circulating-bed bioreactor (PCBBR) setup and operation. The PCBBR

2

was an internal loop airlift-driven reactor with a working volume of 540 mL (see

3

Figure 1), which was filled in around 750 carriers and operated at room temperature.

4

The draft tube section of PCBBR was a plexiglass tube with a diameter of 40 mm and

5

a height of 130 mm, and an aeration disc diffuser with a diameter of 40 mm was

6

mounted at the bottom of the draft tube. The annular section was an annular quartz

7

tube, with an inner diameter of 70 mm and a total height of 180 mm, through which

8

the liquid mixture flowed down to be recycled into the draft tube section. Air was

9

supplied by a 35 W aeration pump (SOBO, Weifang, China), resulting in an aeration

10

rate of 480 g O2/ (g phenol • h) and an air superficial velocity in the draft tube of 10.6

11

mm/s. The PCBBR was illuminated by a UV lamp (6 W, giving peak emission at 254

12

nm; Philips, Amsterdam, the Netherlands) or with visible light from an LED panel (42

13

W; giving wavelength range of 420-700 nm; Hueler, Guangdong, China). The light

14

intensities reached at the outer wall of the reactor for UV and visible light

15

(wavelength between 420 to 700 nm) are 1.26 and 43.13 mW/cm2 in this study, which

16

are very close to the values for those in the standard solar light intensity (see details

17

given in Supporting Information SI-1). The corresponding incident light intensities

18

h=6.6260693 =6.6260693 were 3.93×10 10-7J s hand 5.38 ×10 10-5J seinstein/(L • s) for UV and visible illuminance

19

respectively, by supposing their average wavelengths of 254 nm and 560 nm for

20

simplicity. The detailed on light intensity measurement and calculation protocol are

21

given in the SI-2.

22

The phenol removal by various phenomena in the PCBBR were evaluated using the G


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1

following protocols: (1) the contribution from phenol adsorption (AD) was evaluated

2

using catalyst-coated carriers without the biofilm and light; (2) the contribution from

3

biodegradation (B) was evaluated using biofilm and catalyst-coated carriers in the

4

dark; (3) the contribution of photocatalysis was evaluated using catalyst-coated carrier

5

without the biofilm illuminated with visible light (VPC) and with UV light (UPC) to

6

evaluate photocatalysis; (4) the coupled effect was evaluated using catalyst-coated

7

carriers coupled with biofilm illuminated with visible light to evaluate the VPCB or

8

catalyst-coated carriers coupled with a biofilm illuminated with UV light to evaluate

9

the UPCB. All of above protocols were conducted in the separate reactor with the

10

same configuration (see Figure 1).

11

In this work, VPCB was novelty realized by intimate coating of the upconversion

12

photocatalysts (Er3+:YAlO3/TiO2) and biofilms on the sponge carriers. The

13

crystallized Er3+:YAlO3 could upconverse visible light with wavelengths of 553 nm

14

(close to the average visible light emission wavelength of this work, 560 nm) to UV

15

light with wavelengths 320 and 360 nm according to our previous fluorescence

16

spectra analysis 14. That is, Er3+:YAlO3 firstly absorbed the incident pump visible light

17

(from LED) and then continuously emitted UV in situ by the excited state absorption

18

(ESA) and/or energy transfer upconversion (ETU) mechanism under one- or

19

multiple-pulsed excitation

20

nanoparticles and resulted in the electron-hole pair generation to conduct the phenol

21

photodegradation. The produced less inhabited intermediates was mineralized finally

22

by biodegradation immediately.

18

. Then, the UV effectively excited the anatase TiO2

H



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1

Analytical methods. Analytical methods on phenol, DOC, intermediates (analyzed

2

by High Performance Liquid Chromatography, HPLC), and molecular weight (MW)

3

distribution (analyzed by Gel Filtration Chromatography, GFC) are given in the

4

Supporting Information SI-3. Pretreated procedure for carrier microstructure

5

observation by scanning electron microscopy (SEM) and the biofilm staining

6

procedure for confocal laser scanning microscopy (CLSM) imaging are presented in

7

the Supporting Information (SI-4) and (SI-5), respectively. Microbial community

8

analysis procedure is provided in the Supporting Information (SI-6).

9

RESULTS

10

Phenol degradation and intermediates. The phenol and DOC degradation

11

protocols for AD, B, VPC, UPC, VPCB and UPCB are shown in Figure 2a and b.

12

Phenol, as a kind of typical biological inhibitory pollutants, experienced a slow

13

degradation term as long as 10 hours in the B, in which biofilms was not previously

14

acclimated. Interestingly, such problem could be successfully solved when

15

photocatalysis took part in (ICPB). Both of the VPCB and UPCB almost did not

16

experience

17

microbe-utilizable intermediates by photocatalysis (confirmed by HPLC analysis,

18

Figure 2c). The photocatalytic reaction relies only on the continuous generation of

19

electron-hole pairs, which leads to radical chain reactions that oxidize phenol

20

Thus, adaptive phase (lag phase in the B) is not necessary for the UPC and VPC

21

protocols, and then also for the ICPB protocols which consisted UPC/VPC and

22

coupled with biodegradation. Previous work fully confirmed that B alone was not

lag

phase,

in

which

phenol

was

immediately

I


degraded

to

19,20

.

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1

competent with ICPB when it was used to remove more stable and bio-recalcitrant

2

pollutants such as trichlorophenol, whereas B presented significantly lowered removal

c

3

d

efficiencies than those of ICPB 21.

4 5

Figure 2 Phenol concentrations (a), DOC concentrations (b), HPLC analysis of phenol

6

intermediates (c) versus time with protocols of AD, B, VPC, UPC, UPCB and VPCB, and GFC

7

chromatograms of effluent samples (at the 16th h, d). AD is the adsorption of the carriers alone, B

8

is biodegradation (dark) alone, VPC is visible photocatalysis (no biofilm cultivation) alone, UPC J



1

is ultraviolet photocatalysis (no biofilm cultivation) alone, UPCB is ultraviolet photocatalysis and

2

biodegradation, VPCB is visible photocatalysis and biodegradation. Average values of triplicate

3

samples were used here in Figure 2a, b and c. Legends of Figure 2c represent compounds and their

4

retention time in HPLC.

5

The advantages of ICPB also reflected on the efficiency enhancement when

6

visible light was used in this present work, i.e., phenol concentrations in the VPCB

7

were generally 10 mg/L lower than those in the B before 12 h. To be specified, when

8

VPCB was used, 25.5% phenol was rapidly removed in only 2 h due to adsorption,

9

and then the concentration quickly decreased during the following time. The phenol

10

removal efficiency was 98.8% in 12 h, and only 0.6 mg/L of phenol remained after 12

11

h of operation. At the end (16 h), the phenol removal efficiency reached 99.8%.

12

Similarly, the final (16 h) phenol removal efficiency in the B was also as high as

13

99.4%, though it experienced a longer term (16 h). When the UPCB protocol was

14

used, however, phenol removal efficiency was only 67.7% in 12 h, and the phenol

15

concentration did not decrease further, with a residual phenol concentration of 15.7

16

mg/L at the end. It indicates that photocatalysis under UV light did not enhance

17

phenol removal capability when it was coupled with biodegradation. Similarly

18

situation was also found for DOC degradation. The DOC concentrations with the

19

UPCB protocol decreased dramatically from the initial concentration (38.3 mg/L) and

20

reached 21.9 mg/L in the first 5 h, but it then rebounded after between 5 h and 8 h of

21

operation, and then remained at around 30.0 mg/L. In contrast, the DOC concentration

22

decreased dramatically from 38.3 to 13.8 mg/L in 8 h with the VPCB protocol.

23

Generally, DOC removal efficiencies of B, UPCB and VPCB were 56.9%, 21.7% and K


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1

64.0%, respectively after 16 h of operation, in which UPCB presented the worst.

2

Actually, the UPC protocol generally led to more effective degradation of both of

3

phenol and DOC than the VPC protocol (see Figure 2a and b). As shown in Figure 2c,

4

enhanced photocatalytic activity excited by UV (UPC) resulted in more extra

5

intermediate species, such as catechol, hydroquinone and two unidentified ones, than

6

those in the VPC at each sampling time. However, the UV light unfortunately played

7

a negative role in the ICPB, whereas relative higher phenol and DOC levels remained

8

in the UPCB.

9

To identify mechanisms which induced different performances of VPCB and

10

UPCB, intermediates were termly analyzed by HPLC (see Figure 2c). Totally 6

11

intermediates were detected during phenol degradation. As compared with the

12

intermediates of VPC and UPC protocols, pathway of phenol degradation of ICPB

13

could be deduced. Photocatalytic oxidation produced reactive oxygen species (such as

14

•OH) to attack phenyl ring, yielding catechol and hydroquinone

15

rings in these compounds broke up, providing less or none inhibitory food to microbes.

16

This step was mainly conducted by photocatalysis in the ICPB, as they were detected

17

as early as 3 h of photocatalysis and ICPB, while biodegradation in the B was

18

inhibited by then. After that, short chain organic acid (such as maleic and oxalic) was

19

produced during either photocatalysis or biodegradation, and finally was converted to

20

CO2. It seemed that the terminal conversion of CO2 in the VPCB was much better

21

than photocatalsis solely, confirmed either by DOC degradation or HPLC analysis.

22

However, catechol and hydroquinone accumulated in the UPCB at 16 h, then L


22

, then the phenyl


1

biodegradation in the UPCB was speculated to be notably weaker. GFC

2

chromatograms, which presented molecular weight (MW) distribution of the effluent

3

samples of the protocols (see Figure 2d), could further support this speculation.

4

Apparently, much higher level of high MW compounds (300-1400 kDa) were

5

detected in the bulk water of the UPCB, and they were definitely in the range of the

6

reported cellular macromolecules MW (290-5000 kDa)

7

was normally originated from cell lysis, and exhibited refractory characteristics 24. It

8

seemed cell lysis also occurred in the VPCB and B due to food exhaustion at the end

9

of operation, but the amounts of these SMP were much less. In summary, UV and UV

10

photocatalysis could probably result in cell hurt, then caused UPCB presented higher

11

phenol and DOC residual as compared with VPCB.

12

23

. Such high MW fractions

The released SMP could contribute to the increment of DOC. As indicated by 10

13

Wen et al.

, less adsorbable intermediates release could be another reason of DOC

14

increment of UPCB. In this work, maleic acid should be the product less adsorbable to

15

the sponge carrier, as it could be well degraded via photocatalysis alone; however, it

16

turned out to accumulate either in the VPCB or the UPCB whereas the attached

17

biofilms occupied most of the sponge carriers’ adsorption positions. Thus, release of

18

SMP and less adsorbable intermediates both caused DOC increment.

19

M


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Initial (surface)

Initial (core)

B (surface)

B (core)

UPCB (surface)

UPCB (core)

VPCB (surface)

VPCB (core)

1 2

Figure3. SEM images of the catalyst-coated biofilm carriers. Biofilm on the surface of the carriers (left);

3

biofilm in the core, 1 mm from the surface of the carriers (right) Bar= 5 µm

N



1

Scanning electron microscopy observations. Samples of the TiO2-coated carriers

2

with biofilms attached were collected from the B, UPCB, and VPCB reactor

3

operations before and after the phenol degradation tests, and SEM images of these

4

samples are shown in Figure 3. The SEM images of the initial carriers after the

5

biofilms had been cultivated showed that large numbers of microbes were

6

successfully attached. The numbers of microbes on the carriers decreased to different

7

degrees when they were exposed in the B, VPCB, and UPCB reactor operations.

8

The UPCB carriers had the lowest biofilm coverage than those used in other reactor

9

operations during the phenol degradation tests. There were almost no cells on the

10

surface of the UPCB carrier, and only some catalysts uniformly coated on the carrier

11

surface were observed, after the degradation test had been performed. Similarly, only

12

a few microbes were found in the cores of the UPCB carriers, and there were large

13

areas with no biofilm coverage. Such numerous detached biomass from both of

14

exterior and interior of the carriers was observed when they were fluidized in the

15

UPCB. This phenomenon is different from the results of previous publications. The

16

Rittmann group

17

interior of the carriers but not on the outer surface at all during and at the end of

18

UPCB. According to the comparison results of carrier characteristics and UV light

19

intensity of this work and Rittmann group’s (Table S1), the influence of carrier pore

20

size and UV illumination intensity could be excluded, as the carrier of this work was

21

generally with smaller pore size (2.0±0.3 mm), and illuminated under UV light with

22

weaker intensity. In contrast, 3.5 mm sponge carrier and up to 8 mm ceramic carrier

1,3,9-11

reported that microorganisms were clearly protected in the

O


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1

were mostly employed in Rittmann group’s. In this work, smaller size sponge carrier

2

led to an enhanced surface-area-to-volume ratio to promote photocatalytic reaction.

3

Unfortunately, the enhanced reactive oxygen species (ROSs) production by UV

4

photocatalysis in this work, probably resulted in biofilms detachment. Furthermore,

5

small carrier size gave more opportunity for the ROSs to penetrate into sponge

6

interior.

7

In contrast, the cores of the VPCB carriers after the degradation test appeared to be

8

still densely covered with microbes, but only the biofilms on the surfaces of the

9

carriers were detached, which resulted in the exposure of coating catalyst to the light.

10

It was found that the detachment was mainly occurred on the carrier surface according

11

to the SEM images (VPCB core and surface in Figure 3), which possessed a very

12

small proportion of the total biomass, and no obvious turbidity of wastewater was

13

observed in the VPCB. The integration of biodegradation and photocatalysis in the

14

VPCB protocol favored the efficient intimate coupling reaction, because the

15

photocatalysis did not over-interfere with biofilm growth. This synergy made the

16

VPCB reactor operation more effective than the other operations.

P



Skeleton with

1 2

Figure 4. The CLSM images of the catalyst-coated biofilm carriers for polysaccharide (PS) and protein

3

(PN). Optical microscopy photograph (left); β-D glucopyranose polysaccharide (calcoflour white,

4

middle); protein (FITC, right). Slice thickness was 5 µm obtained by cryosectioning, the layer slices 10

5

µm from surface were the selected for imaging, white point shows the center area of the carrier.

6

Bar=200 µm

7 Q


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1

CLSM observations. The spatial distributions of the extracellular polymeric

2

substances (EPSs which taken to be PS and PN for this study) in the B, UPCB, and

3

VPCB carriers after the phenol degradation tests were compared by multi-staining

4

combined with CLSM imaging (see Figure 4). Compared with the biofilms before the

5

phenol degradation tests, the amounts of both polysaccharides (PSs) and proteins

6

(PNs) appeared to have increased to some degree (determined from the fluorescence

7

intensity) in all of the biofilms after the phenol degradation tests had been performed.

8

This proved that the microorganisms responded by attempting to resist external

9

damage by hydroxyl free radicals or phenol that was present in the bulk water during

10

the tests 3. However, the PS and PN distributions in the carriers used in the three

11

protocols were still different. Less PS and PN was found in the core than in the outer

12

area of the carriers of B protocol, by comparing the fluorescence intensity in the core

13

(white point in the image) and the outer layer of the carrier. Less PS and PN were also

14

found in the exterior than in the interior of the VPCB carriers (according to the

15

fluorescence intensity). But, a large proportion of the EPSs were detached from the

16

UPCB carriers, and some of the carrier structures appeared to be completely exposed

17

without EPSs attachment in either exterior or interior.

R



1 2

Figure 5. DGGE patterns analysis by Quantity One software

3 4

PCR-DGGE analysis. The microbial communities in the protocols changed

5

significantly during the phenol degradation tests, as is shown in Figure 5 and S2. The

6

DGGE image and the optical degree analysis of that image shows bands 1, 3, 4, and 6

7

remained relatively dominant and stable in the VPCB and B protocol systems during

8

the phenol degradation tests, and these bands should represent the microbial groups

9

that were responsible for the biodegradation of phenol. However, the population of

10

some microbial genera became dramatically less in the UPCB protocol system during

11

the phenol degradation test. For example, the intensities of bands 4 and 6 decreased

12

significantly and band 3 disappeared. This disappearance for the UPCB protocol was

13

probably caused by the large amount of damage to the microorganisms by UV light,

14

which is consisted with SEM images. S


Page 20 of 31

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1

DISCUSSION

2

UV limitations in the intimate coupling process. The large amount of energy

3

contained in UV light can be used in UV photocatalysis to convert photon energy into

4

chemical energy because UV has short wavelengths, from 100 to 400 nm 27. This

5

work also confirmed that UV photocatalysis (UPC) performed obviously enhanced

6

capability on phenol degradation as compared with that of photocatalysis induced by

7

visible light (VPC), even though the consumed energy (photon energy, in einstein/(L •

8

s), or electric energy, in W/L) of UPC was significantly lower than that of VPC.

9

Similarly, the use of UV in the UPCB protocol should allow phenol efficiently to be

10

transformed into un-recalcitrant intermediates that microbes could use as sources of

11

energy. However, UV irradiation is disinfectant and it is extremely harmful to

12

microbes because proteins and nucleotides in the microbes absorb photons 25,26. The

13

UV photons are absorbed by proteins in the outer membranes of cells exposed to high

14

doses of UV light. Ultimately this absorption leads to the membranes being disrupted,

15

and the cells die because the protoplasm leaks out of the cells 27 DNA molecules and

16

nucleotides also absorb photons of UV light even at low doses of UV light. This

17

causes disruption in the abilities of the cells to replicate DNA and DNA breakage,

18

which results in cell death

19

light with a wavelength of 254 nm, which is within the broad band, 190-260 nm, at

20

which DNA absorbs UV light 30. The microbes in the biofilm, especially at the surface

21

of the carrier in the UPCB protocol system, therefore suffered fatal levels of damage

22

to the cell membranes or DNA and large amounts became detached because they were

28,29

. The mercury vapor lamp used in this work emitted

T



Page 22 of 31

1

exposed to UV for 16 h (Figure 3). The detached biofilm caused the bulk water to

2

become turbid, and it has been found that turbidity decreases the penetration of UV

3

light 26. Moreover, the powerful free radicals that are produced by UV-photocatalysis

4

were transferred into the interior of the carrier. The transport of these radicals and

5

killed the microorganisms that were located there and the biomass became detached.

6

Soluble microbial products (SMPs) release using the UPCB protocol. UPCB

7

protocols have previously been successfully used to treat recalcitrant compounds1,3,9,10.

8

However, they released SMPs that remain in the effluent and the organic carbon was

9

not completely removed 1,10. In our study, we have found 30.0 mg/L of DOC remained

10

in the UPCB protocol system after a 16 h degradation test (Figure 2), whereas the

11

DOC was decreased to 13.8 mg/L in 8 h only in the VPCB system. Such high residual

12

DOC in the UPCB was caused by the effect of UV on microbe lysis, and then the

13

following SMP release occurred.

14

The release of SMPs has been found to be closely associated with the occurrence of

15

EPSs during biological treatment. Duan et al. found that the release of SMPs was

16

positively correlated with the EPSs amount that are produced

17

have found that SMPs originate from soluble EPSs, and are rich in PSs and PNs,

18

where are released during cell lysis 32. Organic matters originated from cell lysis was

19

classified to biomass associated products (BAP). BAP mainly consisted of high MW

20

fractions (290-5000 kDa) 23. Apparently, the MW of organic matters in the effluent of

21

UPCB were in this range (see Figure 2c). However, organic matters with MW >10

22

kDa were refractory and inhibited microbial growth

24,33

31

. Some researchers

. This gives us the clue of

U


Page 23 of 31


1

DOC maintained at a stable high level for the UPCB protocol from 6 to 16h,

2

accompanied by the detachment of biofilms and EPSs (Figs. 3 and 4)

3 4

Figure 6. Biodegradability variation in UPCB and VPCB protocols with error bar

5 6

The SMPs in the UPCB protocol system were released because of environmental

7

stress on the microbes. The release of SMPs would have been aggravated by the

8

detachment of the biofilms caused by the UV light disinfection and hydroxyl radicals

9

attack. The release of SMPs triggered in this way would have altered the quality of the

10

bulk water. SMPs are poorly biodegradable especially when released from cell lysis

11

under stressful condition

12

UPCB protocol system during the phenol degradation test (see Figure 6), i.e.,

13

BOD/DOC decreased from 3.3 after 6 h to 1.8 after 12 h, and finally ended in a value

14

of 1.4 after 16 h. The poorly biodegradable substrates in the UPCB protocol system

15

would have strengthened the inhibition of the microorganisms 34, and was considered

16

to contribute to the decreased quantity of microbes to some degree also. In contrast,

17

BOD/COD in the VPCB was increased obviously at first as compared with its level at

34

. This was consistent with the BOD/DOC ratio in the

V



1

6 h and 12 h. As discussed previously, phenyl ring break up and small chain organic

2

acid production contributed to biodegradable ability enhancement. At the end,

3

BOD/COD also decrease due to food exhausted induced BAP release, as confirmed

4

by phenol degradation trend and GFC results.

5

Advantages of using VPCB protocols. To the best of our knowledge, the novel

6

intimate coupling protocol VPCB is described here for the first time. We found that

7

VPCB with Er3+:YAlO3/TiO2 photocatalysts offered obvious advantages over UPCB.

8

Firstly, visible light itself caused almost no harm to the biofilms that were present on

9

the exteriors and in the interiors of the carriers (Figure 3). Secondly, the

10

photocatalysis induced by visible light allowed the biofilm to perform active

11

metabolism, and the excessive biomass detachment in the UPCB was avoided when

12

using the VPCB protocol (Figure 4). A lower concentration of free radicals was

13

generated by visible light than that by UV light, because phenol was found to be

14

degraded more quickly using the UV-induced photocatalysis protocol than using the

15

visible-light induced photocatalysis protocol (see Figure 2). The hydroxyl free

16

radicals and phenol intermediates that were produced led to a mild degree of biofilm

17

detachment on the carrier surfaces using the VPCB protocol. And this increased the

18

area of the VPCB catalyst that was exposed to visible light, enhancing the

19

photocatalysis efficiency. Meanwhile, the dominant microbial genera that were

20

responsible for biodegrading phenol in the carrier interior were preserved using the

21

VPCB protocol (Figure 5), so the DOC was mostly removed from the effluent.

22

Thereafter the efficiency at which the VPCB degraded phenol was improved, and the W


Page 24 of 31

Page 25 of 31


1

VPCB protocol remained more efficient than the UPCB protocol at degrading phenol

2

(Figure 2). Probably, a UPCB with lower light intensity could reduce the hurt of UV

3

on microbe, and still competent in transform recalcitrant pollutants to biodegradable

4

intermediates. However, the reasonable UV intensity for treatment of wastewaters

5

with different turbidity or reactor with different depth are still hard to be specified. In

6

summary, the VPCB protocol led to the more efficient removal and mineralization of

7

phenol than the UPCB protocol in this work, because of synergy between the

8

photocatalysis induced by visible light and the biodegradation.

9 10

11

Supporting Information

12

Light intensities selection basis, light intensity calculation protocol, SEM and CLSM

13

imaging pretreat procedures, comparison of carrier characteristics and UV light

14

intensity between this work and other publications, microscope and SEM image of the

15

sponge carrier, and PCR-DGGE analysis is available in the Supporting Information

ASSOCIATED CONTENT

16 17

18

Corresponding Author

19

*(S. Dong) Phone: +86 13604331853; fax: +86 43188502606

20

E-mail: [email protected]

21

*(M. Huo) Phone: +86 13904304481; fax: +86 43185099550

22

E-mail: [email protected]

AUTHOR INFORMATION

X



Page 26 of 31

1 2

Notes

3

The authors declare no competing financial interest.

4 5

6

The authors thank the Natural Sciences Foundation of China (51238001), State Key

7

Laboratory of Urban Water Resource and Environment, Harbin Institute of

8

Technology (QA201418) and Science and Technology Development Program of Jilin

9

province, China (20140101159JC) for ﬁnancial support for the project.

ACKNOWLEDGEMENTS

10 11 12

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DD


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