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. 2022 Dec 30;14:100234. doi: 10.1016/j.ese.2022.100234

Photocatalytic synergistic biofilms enhance tetracycline degradation and conversion

Chuanbao Xiao a, Jilin Yuan a, Linyang Li a, Nianbing Zhong a,∗∗, Dengjie Zhong b, Quanhua Xie a, Haixing Chang b,∗, Yunlan Xu b, Xuefeng He a, Min Li a
PMCID: PMC9852288  PMID: 36685749

Abstract

Tetracyclines are refractory pollutants that cause persistent harm to the environment and human health. Therefore, it is urgently necessary to develop methods to promote the efficient degradation and conversion of tetracyclines in wastewater. This report proposes a photobiocatalytic synergistic system involving the coupling of GeO2/Zn-doped phosphotungstic acid hydrate/TiO2 (GeO2/Zn-HPW/TiO2)-loaded photocatalytic optical hollow fibers (POHFs) and an algal–bacterial biofilm. The GeO2/Zn-HPW/TiO2 photocatalyst exhibits a broad absorption edge extending to 1000 nm, as well as high-efficiency photoelectric conversion and electron transfer, which allow the GeO2/Zn-HPW/TiO2-coated POHFs to provide high light intensity to promote biofilm growth. The resulting high photocatalytic activity rapidly and stably reduces the toxicity and increases the biodegradability of tetracycline-containing wastewater. The biofilm enriched with Salinarimonas, Coelastrella sp., and Rhizobium, maintains its activity for the rapid photocatalytic degradation and biotransformation of intermediates to generate the O2 required for photocatalysis. Overall, the synergistic photocatalytic biofilm system developed herein provides an effective and efficient approach for the rapid degradation and conversion of water containing high concentrations of tetracycline.

Keywords: Optical hollow fiber, GeO2/Zn-doped phosphotungstic acid hydrate/TiO2, Algal–bacterial biofilm, Synergy, Tetracycline

Graphical abstract

Image 1

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Highlights

  • •

    Photocatalytic fibers are intimately coupled with an algal–bacterial biofilm.

  • •

    GeO2/Zn-HPW/TiO2-coated fibers have high catalytic activity and luminous intensity.

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    Biofilm-enriched Salinarimonas and Coelastrella sp. degrade photocatalytic products.

  • •

    O2 generation by phototrophs aid photocatalytic aids .•OH and •O2− production.

  • •

    Synergistic system rapidly and sustainably degrades and transforms tetracycline.

1. Introduction

Antibiotics that are widely used in the medical field are known to accumulate in the environment [1]. In particular, large amounts of tetracycline have been detected in terrestrial and aquatic environments owing to its wide application and high adsorption capacity [2,3]. The detected concentration of residual tetracycline in pharmaceutical wastewater has been as high as 200 mg L−1 [4]. Furthermore, long-term, low-dose tetracycline residue in the environment can adversely affect exposed organisms, including endocrine disorders, chronic toxicity, and antibiotic resistance [5]. Importantly, tetracycline cannot easily be degraded naturally because of its antibiotic properties and chemical stability, and moreover, its degradation byproducts are sometimes more toxic than the parent compound [6,7]. Therefore, it is necessary to develop an efficient technology for removing tetracycline from water.

Intimately coupled photocatalysis and biodegradation (ICPB) has demonstrated promising applicability for degrading toxic organic pollutants, such as antibiotics [8], phenolic compounds [9,10], chemical oxygen demand (COD) [11], and odorous compounds [12]. Yahiat et al. [13] reported high tetracycline removal using ICPB, where a photocatalyst (TiO2/SiO2) was fixed on non-woven paper and excited using 365 nm UV lamps. Later, Xiong et al. [8] evaluated the removal and mineralization of tetracycline hydrochloride (TCH) using silver-doped TiO2 as a photocatalyst and a polyurethane sponge as a carrier via a visible-light-induced ICPB approach. Farissi et al. [14] and Ma et al. [15] confirmed that photocatalytic synergistic bacteria play an important role in the mineralization of TCH and its intermediates. However, the adhesion between the photocatalyst and substrate was insufficient in these cases, which affected the recyclability of the system. To mitigate this issue, Li et al. [16] pioneered a powder spraying method, which allowed the photocatalyst to adhere more firmly to the outer surface of the carrier while retaining its internal pore structure for biofilm formation. This system enabled a TCH degradation rate of up to 97.2% and retained high stability throughout six cycles under visible light irradiation. To further improve the biotransformation and mineralization of TCH, a readily biodegradable co-substrate (acetate) was added to an ICPB system to serve as an energy source and an electron donor. The resulting TCH removal and mineralization increased by ∼5% and ∼20%, respectively, and almost all photocatalysis products were consumed by the bacterial biofilm. The enhanced TCH removal in this system was ascribed to adding acetate increased biomass activity and promoted microbial community evolution; thus, the abundant evolved community accelerated the photocatalysis and biotransformation of intermediates [17].

In general, ICPB systems can rapidly degrade various bio-recalcitrant pollutants because the photocatalysis and biodegradation processes occur simultaneously in the same reactor. Nevertheless, the pH value within the ICPB system that is most conducive to photocatalysis and bacterial biofilm growth can be further optimized [18]. At the optimal pH, the photocatalytic reaction can rapidly degrade the persistent and nonbiodegradable organic pollutants to generate readily biodegradable organic products that can be degraded by the bacterial biofilm [9]. Although ICPB technology has outstanding advantages in terms of treating antibiotic-contaminated wastewater, it still has certain shortcomings, such as the poor optical characteristics of the carriers [19], the consumption of electron acceptors (i.e., O2) by photocatalysis and aerobic bacteria (which may reduce the number of electron acceptors available for photocatalysis, thereby reducing photocatalytic activity) [9], and difficulties in biomass conversion of tetracycline in water [10].

The present study aimed to (1) develop novel GeO2/Zn-HPW/TiO2-loaded (HPW = phosphotungstic acid hydrate) photocatalytic optical hollow fibers (POHFs) for enhanced light utilization efficiency; (2) characterize the surface morphologies, compositions, absorption spectra, and photoelectric conversion capabilities of the modified photocatalysts; (3) integrate algal-bacteria biofilms to increase tetracycline detoxification and the production of biodegradable intermediates; (4) employ a light-conducting nuclear pore filter membrane as an algal–bacterial biofilm carrier to deliver photocatalytic intermediates and biofilm metabolites (e.g., O2); and (5) evaluate the performance of the developed ICPB system compared with a photocatalyst or algal–bacterial biofilm alone.

2. Experimental details

2.1. Materials

Zinc nitrate hexahydrate (analytical reagent [AR] grade, 99%), acetone (AR grade, ≥99.5%), and absolute ethanol (gas chromatography [GC] grade, ≥99.8%) were purchased from Sigma-Aldrich, China. Titanium(IV) oxide (TiO2; anatase, nanopowder, <25 nm particle size [P25], 99.7% trace metals basis), phosphotungstic acid hydrate (AR grade), hydrofluoric acid (AR grade, ≥40%), hydrochloric acid (AR grade, 37%), ethylene glycol (GC grade, ≥99.5%), citric acid monohydrate (AR grade, ≥99.8%), ammonia solution (AR grade, 25–28%), Triton X-100 (biochemical reagent grade), isopropyl alcohol (GC grade, ≥99.9%), phosphotungstic acid hydrate (H3PW12O40·xH2O, HPW; AR grade), and methanol (AR grade, 99.9%) were purchased from Aladdin, China. Tetracycline (AR grade, 96%), GeO2 raw powder (99.999% metals basis), sodium hydroxide (AR grade, ≥98%), and dimethyl sulfoxide (≥99.7%) were purchased from Sinopharm Chemical Reagent Co., Ltd. Optical hollow fibers (OHFs; length = 200 nm, outer diameter = 1.45 nm, inner diameter = 0.8 mm) were purchased from Taixing Hechen Crystal Technology Co., Ltd., Jiangsu, China. Nucleopore membranes (PET115745, thickness = 20 μm, average pore density = 5 × 107 pores cm−2) was purchased from Wuwei Kejin Xinfa Technology Limited Liability Company, Lanzhou, China.

2.2. Preparation of GeO2/Zn-HPW/TiO2 photocatalytic optical hollow fibers

In this work, the GeO2/Zn-HPW/TiO2 catalyst (Supplementary Information, S1) was prepared via a two-step impregnation method with TiO2 (P25) as the catalytic carrier [20]. The TiO2 was used because it is inexpensive and non-toxic, GeO2 was selected because of its wide bandgap (∼5 eV), which acted as a potential trap for photogenerated electrons to limit the recombination of charge carriers, and the dopant (Zn) was added to broaden the absorption edge of the photocatalyst. Integrating these materials enabled the construction of GeO2/Zn-HPW/TiO2 photocatalysts with core–shell structures that exhibited high photoelectric conversion and other characteristics conducive to charge transfer. The photocatalytic sol (Supplementary Information, S2) was prepared using a previously reported method [21]. Briefly, the OHFs were first ultrasonically cleaned for 10 min using acetone, isopropyl alcohol, and ethanol successively and then dried under a nitrogen atmosphere. Next, the prepared GeO2/Zn-HPW/TiO2 sol was uniformly coated on the surface of the optical fibers using a dipping method. Finally, the quasi-photocatalytic fibers were dried at 200 °C for 8 h to obtain GeO2/Zn-HPW/TiO2-coated POHFs.

2.3. Characterization of photocatalysts and POHFs

To study the surface morphology and chemical composition of the photocatalytic materials, TiO2, HPW, HPW/TiO2, and the GeO2/Zn-HPW/TiO2 photocatalysts were characterized using scanning electron microscopy (SEM; JSM-7800F, JEOL Ltd., Japan), X-ray photoelectron spectroscopy (XPS; ESCALAB250Xi, Thermo Scientific, USA), energy-dispersive X-ray spectroscopy (EDS) and transmission electron microscopy (TEM; Tecnai G2 F20 S-Twin, ZEISS Co., Germany), X-ray diffraction (XRD; D/Max 2500 PC, Rigaku Corporation, Japan), and Fourier-transform infrared spectroscopy (FT-IR; Thermo Fisher, Nicolet is5, USA). An electrochemical workstation (CHI660E, CHI instruments, USA) was employed to examine the photoelectric conversion characteristics of the photocatalysts. The absorption spectra of the photocatalysts and surface spectra of the POHFs were recorded using an optical spectrometer (QE65 Pro, Ocean Optics, USA), an optical power meter (Hs211, spectral detection range = 200–‍1100 nm, lower detection limit = 100 pW), and a deuterium halide light source (DH-2000, Ocean Optics, USA) in 190–2000 nm range to study the surface light emission of the catalytic fibers. The surface luminous intensity of the POHFs was tested using a power meter (36R, Newport Corporation, USA).

2.4. Bioinformatics analysis

In this study, the microalgae Scenedesmus obliquus was added to the upper layer to promote the biodegradation of tetracycline and its intermediates. This particular microalga was selected because (1) it has a high capacity to degrade tetracycline via biodegradation using intracellular P450 enzymes and via photolysis using extracellular polymer substances, and (2) microalgae is a valuable resource, which can produce bioenergy (e.g., biodiesel and biohythane) and chemicals (e.g., biodegradable plastics) following downstream processing [22]. In the ICPB system, the microalgae biofilm is fixed on the upper side of the nuclear pore membrane to avoid ultraviolet light damage to cells and to facilitate molecular exchange between the microalgae layer and the photocatalytic layer.

The microalgae S. obliquus was purchased from the freshwater algae seed bank of the Wuhan Institute of Hydrobiology, Chinese Academy of Sciences, and it was grown using a BG-11 medium. The specific microalgae cultivation method is described in detail in Supplementary Information (S3). The microalgae biomass and biological community of the biofilm were examined to study the resource conversion performance of the ICPB system toward tetracycline degradation. Disinfected scraper and ultrasonic treatments were used to obtain biofilm samples. The microalgal biomass that had been dried at 105 °C was measured using an ultra-microbalance (XPR6U; Mettler-Toledo, Greifensee, Switzerland), and 16S ribosomal RNA (16S rRDA) was used to analyze the sequencing information of the microalgae membrane. The bioinformatics analysis is presented in detail in Supplementary Information (S4).

2.5. Experimental system operation

The ICPB system for wastewater-derived tetracycline degradation (Fig. S1) comprised a stable voltage and current power supply, a UV–Vis LED, a photobioreactor, 36 GeO2/Zn-HPW/TiO2-coated POHFs, a peristaltic pump (L100-1s-2, LONGER, China), a nuclear pore membrane, and a constant-temperature water bath (DCW-0530, Shunmatech, China). The operation of the ICPB system and the liquid- and gas-phase analyses are described in the Supplementary Information (S5 and S6, respectively).

3. Results and discussion

3.1. Photocatalyst characterizations

The SEM characterization of TiO2, HPW/TiO2, and the GeO2/Zn-HPW/TiO2 coating are shown in Fig. 1a–c. These samples all have fine-grained and dense characteristics. The corresponding TEM images (Fig. 1d–f) clearly show the existence of core–shell particles in HPW/TiO2 and GeO2/Zn-HPW/TiO2. Specifically, the core comprises TiO2 microcrystals (20–30 nm), and the shell comprises HPW (layer thickness ≈ 1–‍2 nm). Meanwhile, small zinc clusters are dispersed on the catalyst surface. TEM-EDS mapping was used to analyze and characterize the elemental compositions of TiO2, HPW/TiO2, and GeO2/Zn-HPW/TiO2. The elements W, P, Ge, Zn, Ti, and O are clearly observed in the TEM-EDS maps (Fig. S2). Fig. 1g and h shows that the GeO2/Zn-HPW/TiO2 material was evenly distributed on the surface of the POHFs, whereas the OHFs had smooth surfaces. This observation indicated that the photocatalytic GeO2/Zn-HPW/TiO2 material was successfully coated on the OHFs.

Fig. 1.

Fig. 1

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Characterization of TiO2, HPW/TiO2, GeO2/Zn-HPW/TiO2, OHF, and POHF. a–c, SEM images of TiO2 (a), HPW/TiO2 (b), and GeO2/Zn-HPW/TiO2 (c). d–f, TEM images of TiO2 (d), HPW/TiO2 (e), and GeO2/Zn-HPW/TiO2 (f). g–h, SEM images of OHFs (g) and GeO2/Zn-HPW/TiO2-coated POHFs (h). i, XPS of TiO2, HPW/TiO2, HPW, and GeO2/Zn-HPW/TiO2. j, XRD of TiO2, HPW/TiO2, HPW, and GeO2/Zn-HPW/TiO2.

The XPS spectra of the TiO2, HPW/TiO2, and GeO2/Zn-HPW/TiO2 photocatalysts (Fig. 1i) all contain strong peaks at 459.08 and 464.08 eV, which correspond to Ti 2p, and at 530.08 eV, which corresponds to O 1s, thus confirming that all three materials contain TiO2 [23]. Characteristic W 4f and P 2p peaks are also present in the HPW, HPW/TiO2, and GeO2/Zn-HPW/TiO2 spectra at 36.08 and 113.18 eV, respectively, although the lower P content in the latter two materials resulted in unclear P 2p peaks [24]. In addition, the presence of Zn 2p (1021.58 eV) and Zn LM2 (498.78 eV) peaks confirmed that Zn is present in the GeO2/Zn-HPW/TiO2 material [25]. However, no characteristic peak corresponding to Ge 3d is observed in the GeO2/Zn-HPW/TiO2 spectrum because the Ge content in the material is too low; therefore, the peak is obscured by miscellaneous peaks. Overall, the XPS spectra of these four materials verified the successful synthesis of the GeO2/Zn-HPW/TiO2 photocatalyst.

The XRD patterns of HPW, TiO2, HPW/TiO2, and GeO2/Zn-HPW/TiO2 are shown in Fig. 1j. We observed characteristic diffraction peaks of Keggin-structured HPW and anatase TiO2. However, the diffraction peaks corresponding to Keggin-structured HPW were not observed in the XRD patterns of the HPW/TiO2 or GeO2/Zn-HPW/TiO2 samples. This may have been because of the low HPW content in these two samples or because HPW was highly dispersed in the materials [20]. The characteristic diffraction peaks of α-quartz GeO2 were observed in the spectra of the GeO2/Zn-HPW/TiO2 samples at 2θ = 26.1°, 36.1°, and 39.0°, corresponding to the (101), (110), and (111) lattice planes, respectively. Furthermore, Zn was detected in the hexagonal wurtzite phase in GeO2/Zn-HPW/TiO2, with characteristic diffraction peaks at 2θ = 31.8° (100) and 34.4° (002).

The FT-IR spectra of TiO2, HPW, HPW/TiO2, and GeO2/Zn-HPW/TiO2 are shown in Fig. 2a. HPW is known to have a typical Keggin structure, and the vibrational peaks at 1079, 983, 889, and 805 cm−1 correspond to the P–O, W Created by potrace 1.16, written by Peter Selinger 2001-2019 O, W–Ob–W, and W–Oc–‍W bonds in the PO4 unit structure, respectively [26]. However, when HPW was loaded on the TiO2, these characteristic HPW peaks shifted to 1200–700 cm−1. This shift was due to strong chemical interactions between the synthesized HPW/TiO2 and GeO2/Zn-HPW/TiO2 composites, which induced tensile vibrations of the P–O, W Created by potrace 1.16, written by Peter Selinger 2001-2019 O, and W–‍O–‍W bonds of the Keggin structural unit [27]. The weak intensity of the offset peaks was attributed to low HPW content in the composite photocatalytic material. Taken together, the results in Figs. 1, 2a and 2S confirm that the GeO2/Zn-HPW/TiO2 was successfully synthesized.

Fig. 2.

Fig. 2

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FT-IR and electrochemical characterization of TiO2, HPW/TiO2, GeO2/Zn-HPW/TiO2. a, FT-IR. b, EIS Nyquist. c, Current vs. time curves.

The comparison of the electrochemical impedance spectroscopy (EIS) Nyquist characterizations of TiO2, HPW/TiO2, and GeO2/Zn-HPW/TiO2 (as shown in Fig. 2b) contributes to a better understanding of the catalytic performance of the photocatalytic materials in terms of photogenic electron (e−) and hole (h+) separation. The micro-semicircle radius of GeO2/Zn-HPW/TiO2 is smaller than those of TiO2 and HPW/TiO2, indicating that GeO2/Zn-HPW/TiO2 has the smallest charge-transfer resistance. This lower resistance can effectively promote electron transfer between the photocatalytic materials, thereby limiting the recombination of photogenerated carriers [28]. In addition, Fig. 2c shows that the GeO2/Zn-HPW/TiO2 composite material has a better photocurrent response than TiO2 or HPW/TiO2. These behaviors can be explained as follows. First, GeO2/Zn-HPW/TiO2 exhibited a broad absorption edge reaching up to 1000 nm, with particularly intense absorption in the UV region (<400 nm), as shown in Fig. S3a. The broad absorption edge was ascribed to the localized surface plasmon resonance of the dopant Zn [29]. The intense absorption arose because the HPW band gap is approximately 3.12 eV and lower than that of TiO2 (Eg = 3.20 eV). Additionally, doping with Zn had a minimal effect on the band gaps of HPW and TiO2 [30]. The core–shell structure of Zn-HPW/TiO2 created a semiconductor heterojunction and increased the charge separation and lifetime of the charge carriers [31]. Finally, the dopant GeO2, which has a wide bandgap (∼5 eV), served as a potential trap for the photogenerated electrons, thereby decreasing the recombination of charge carriers [32], as shown in Fig. S3b. These results illustrate that the GeO2/Zn-HPW/TiO2 photocatalyst is capable of high photoelectric conversion, which is conducive to charge transfer.

As shown in Fig. S3c, all POHFs gave high-quality surface luminous spectra in the 550–930 nm spectral range. In particular, the GeO2/Zn-HPW/TiO2-coated POHFs exhibited the highest quality surface luminous spectrum in the 760–930 nm range and the highest luminous intensity in the spectral range 400–1000 nm (Fig. S3d). These results can be explained as follows. First, the refractive indices of the POHFs increase from the core to photocatalyst coating, which directs light beams into the coating and increases the number of reflection points in the fiber [9]. Second, GeO2 has good UV–visible–near infrared light transmission; therefore, the dopant GeO2 increases the surface luminous intensity of POHFs in the visible–near infrared region. These features make GeO2/Zn-HPW/TiO2-coated POHFs good candidates for photocatalysis and biofilm photosynthesis in an ICPB system owing to the high light intensity they provide to the photocatalyst and biofilm.

3.2. Degradation of tetracycline using photocatalysis alone

3.2.1. Effect of pH and temperature on photocatalytic activity of POHFs

To explore the tetracycline degradation performance of photocatalytic fibers coated with various photocatalytic materials, preliminary tests of photocatalytic tetracycline degradation were performed using different fibers under the same conditions (Fig. S4). Among the TiO2-, HPW/TiO2-, and GeO2/Zn-HPW/TiO2-coated POHFs, the GeO2/Zn-HPW/TiO2-coated POHFs achieved the highest photocatalytic activity. This was likely due in part to the fact that the GeO2/Zn-HPW/TiO2 composite comprised small particles (20–30 nm), which leads to a high surface-to-volume ratio and enables indirect electron transfer to improve the rate of photogenerated carrier (e−–h+) generation, i.e., improved photocatalytic activity [33,34]. Additionally, there is a synergistic effect between HPW and TiO2. Specifically, HPW has a strong ability to accept electrons, rapidly capturing electrons photogenerated on the TiO2 surface and then transferring them from TiO2 to the Zn species. This phenomenon effectively inhibits photogenerated electron–hole recombination. As a result, the photogenerated holes on the TiO2 surface have sufficient time to react with H2O to generate •OH, thereby increasing the photocatalytic activity of the composite photocatalytic material [8]. Simultaneously, the photogenerated electrons transferred to the Zn species are removed by O2 to generate O2•− [35], reducing dissolved oxygen (DO) content in the substrate solution. In this work, •OH and O2•− play key roles in tetracycline degradation, as shown in Fig. S5. Moreover, Zn in the composite is mainly dispersed on the HPW surface in the form of ZnO, which can form a charge transfer excited complex (Zn+–‍O−) and has a positive effect on photocatalytic activity [21]. Therefore, the GeO2/Zn-HPW/TiO2-coated POHFs were chosen to develop the ICPB system in this work.

The optimal substrate solution temperature and the initial pH of the photocatalytic reaction were screened to optimize the photocatalytic efficiency of the system (Fig. S6). Figs. S6a and b shows that the tetracycline wastewater degradation performance of the GeO2/Zn-HPW/TiO2 photocatalytic fibers first increased and then decreased as the temperature increased (at pH 6.8), reaching the optimal value at 35 °C. With increasing temperature, the movement of the tetracycline molecules in the wastewater was accelerated, thus increasing the probability that tetracycline would come into contact with the photocatalyst. However, an excessively high temperature reduced the DO content in the wastewater, thereby inhibiting the combination of photogenerated electrons with oxygen from producing •O2− for tetracycline degradation.

The experimental results in Figs. S6c and d indicate that photocatalytic performance can be improved by increasing the pH in the range of 4–7 (at 35 °C); however, the photocatalytic performance decreased upon further increasing the pH value (up to pH 10). This is because tetracycline molecules can adopt cationic, amphoteric, and anionic molecular forms under different pH conditions [36]. The zero charge point (pHzpc) of TiO2 is approximately 6.25, which means that it has a net positive charge in acidic media (pH < 6.25) but a net negative charge under relatively alkaline conditions (pH > 6.25) [34]. As the pH increases from 4 to 7, the tetracycline changes from TCH3+ to TCH2±, and the TiO2 surface changes from positively to negatively charged. These changes promote tetracycline adsorption by TiO2 and enhance the interaction between tetracycline and TiO2 surface sites through hydrogen bonding. As the pH increases further from 7 to 10, the TiO2 surface becomes negatively charged, and tetracycline exists mainly as TCH− and TC2−. The electrostatic repulsion between these two species weakens the adsorption capacity of TiO2 toward tetracycline [37]. Therefore, the temperature and initial pH of the tetracycline wastewater were set at 35 °C and 7.0, respectively, in the following experiments.

3.2.2. Degradation of tetracycline using GeO2/Zn-HPW/TiO2-coated POHFs

Two identical reactors were used for parallel experiments. As shown in Fig. 3a and b, POHFs with GeO2/Zn-HPW/TiO2 coatings maintained the same level of tetracycline degradation after repeated experimental cycles. This was because the GeO2/Zn-HPW/TiO2 coating was strongly attached to the fiber surface following the introduction of the cross-linking agent, Triton X-100, and polyethylene glycol (Fig. S7) [9]. Meanwhile, the photocatalytic products accumulated on the POHF surface are not abundant enough to block the reaction sites of the photocatalyst because the tetracycline solution was maintained in a flowing state. The tetracycline wastewater degradation rate and COD removal rate of the POHFs reached 95.8% and 45.8%, respectively, within 10 h at pH 7 and 35 °C. The calculated photocatalytic degradation rate of tetracycline was 4.31 μmol h−1.

Fig. 3.

Fig. 3

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Photocatalytic tetracycline degradation performance and changes in the liquid phase during the reaction. a–b, Removal of tetracycline (a) and COD (b) by GeO2/Zn-HPW/TiO2-loaded POHFs. c–d, Associated changes in the pH (c) and DO concentration (d).

Furthermore, Fig. 3c shows that the pH of the substrate solution first increased and then decreased, which may be because tetracycline degradation was initiated by the cleavage of the azo linkage, which results in acetamide formation [36,38]. During the degradation process, biodegradable intermediate products, such as C8H16O9 (m/z = 256), C9H10O2 (m/z = 149), C3H4O5 (m/z = 120), and C5H6O3 (m/z = 114) were generated and identified using high-performance liquid chromatography-mass spectrometry (Fig. S8). However, the photocatalytic degradation of tetracycline deteriorates with the accumulation of organic acids, such as C9H10O2 (C8H9–COOH), and the activity of the POHFs decreases with decreasing pH (i.e., under acidic conditions; Fig. S6d).

As shown in Fig. 3d, the DO concentration decreases continuously during the photocatalytic reaction; this observation was attributed to oxygen consumption (via O2•− generation) by the photocatalytic oxidation of tetracycline. Therefore, it is crucial to continuously compensate for the reduced oxygen concentration to enhance the tetracycline removal efficiency.

3.3. Biodegradation and conversion of tetracycline using biofilm alone

When the initial pH and temperature were set to 7.0 and 35 °C, Fig. 4a and b indicates that tetracycline wastewater treatment with a biofilm alone is ineffective, with a tetracycline degradation rate and COD removal rate of only 14.1% and 5.7%, respectively. Moreover, the tetracycline biodegradation rate was only 0.64 μmol h−1. This was because tetracycline is a complex molecule with biological resistance and toxicity; therefore, it is difficult to effectively remove such compounds using microalgae alone. During the treatment period, the pH of the substrate solution first increased slightly and then decreased to neutral (Fig. 4c). This behavior was attributed to dissolved (aqueous) CO2 absorption and utilization by microalgae cells can increase the pH. However, microalgae metabolism slowed sharply because of the high biotoxicity of tetracycline; then, the solution gradually returned to neutral by adsorbing CO2 from the air. Fig. 4d shows that the DO concentration in the substrate solution first increased and then decreased. The increase in DO concentration was due to O2 generation via photosynthesis in the biofilm, whereas the decrease in DO concentration indicated reduced metabolic activity of the microalgae due to the biotoxicity of tetracycline. Therefore, Fig. 4 demonstrates the inhibitory effect (i.e., biotoxicity) of tetracycline on a microalgae biofilm.

Fig. 4.

Fig. 4

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Biodegradation and changes in the DO and pH. a–b, Biodegradation of tetracycline (a) and COD (b) by the biofilm over 10 h. c–d, Changes in pH (c) and DO concentration (d).

As shown in Fig. 5a, microalgae growth was slow. The antibiotic tetracycline affected the membrane permeability of freshwater green algae [39], thereby allowing toxic substances to enter algal cells more easily and bind irrevocably with the 30S subunit of cell ribosomes; this prevented aminoacyl transferase binding to RNA and inhibited cellular protein synthesis, thus hindering microalgae growth [40]. Fig. 5b shows that the tetracycline biodegradation rate continued to decrease and dropped to almost zero after 45 days. In addition, Fig. S9 shows that as the biofilms were incubated in tetracycline, they gradually turned yellow in color and eventually sloughed off the nucleopore membrane surface after 45 days because of cell death. These observations confirm that it is difficult for a microalgae biofilm alone to degrade and convert tetracycline.

Fig. 5.

Fig. 5

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Changes in microalgal biomass (a) and tetracycline degradation rates (b) over 45 days during tetracycline degradation by the biofilm alone.

3.4. Degradation and conversion of tetracycline using the ICPB system

In the ICPB system, the POHFs and biofilm are intimately coupled to enable the coordinated degradation and transformation of tetracycline via photobiocatalysis. The suitability of this approach was highlighted by the overwhelmingly higher tetracycline degradation rate in the ICPB system relative to pure adsorption, biodegradation, and photocatalysis (Fig. S10). As shown in Fig. 6a and b, the tetracycline degradation rate reached 98.1% within 5 h. Meanwhile, the COD removal rate was 95.0% when the experiment was carried out over 10 h. The tetracycline degradation rate was calculated to be 8.82 μmol h−1. Fig. S8 shows that the overall content of photocatalytic intermediates decreased, and C8H9–COOH was not detected in the ICPB system after 5 h. This is because of the rapid detoxification of tetracycline by the POHFs, which increased its biodegradability. Biofilms can use readily biodegradable intermediates to maintain their growth and metabolism rates, thus reducing the competition among photocatalytic products for •OH and O2•− and improving the photocatalytic tetracycline degradation efficiency. In addition, the O2 generated following biofilm photosynthesis can be transferred to the POHFs to promote the photocatalytic reaction.

Fig. 6.

Fig. 6

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Degradation of tetracycline by the ICPB system and changes in the liquid. Changes in the tetracycline concentration (a), COD (b), pH (c), and DO (d) in the liquid phase.

As shown in Fig. 6c and d, pH variations during the collaborative degradation of tetracycline via photobiocatalysis were consistent with those observed with the biofilm alone. However, in the early stage of degradation, the photocatalytic activity is high, the •OH and O2•− production efficiencies are high, and the O2 consumption rate is higher than the biofilm phototroph production rate, which decreases the DO concentration. Then, as the tetracycline concentration decreases and biodegradable products are generated, the biofilm's ability to degrade and transform tetracycline is improved. This improvement is accompanied by enhanced O2 production (by the biofilm) over O2 consumption (by photocatalysis), which contributes to the increase in DO concentration. These results indicate that the O2 produced by the biofilm was transferred to POHFs to help generate O2•− for photocatalysis to enhance the photocatalytic activity of the POHFs.

Similarly, to study the continuous degradation performance and biotransformation efficiency of ICPB toward tetracycline, a 120-day experiment was performed (Fig. 7). The tetracycline degradation rate (Fig. 7b) and COD of the effluent (Fig. 7c) remained at 8.83 μmol h−1 and 16.83 mg h−1, respectively, over 120 days. After 120 days of growth in the presence of tetracycline, the areal biomass concentration of the microalgae biofilm reached 37.62 mg cm−2, representing an ∼11-fold increase over initial biofilm biomass (Fig. 7a and S11). These experimental results confirmed that the developed ICPB system could simultaneously remove and transform tetracycline in water.

Fig. 7.

Fig. 7

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Changes in biomass dry weight (a), tetracycline degradation rate over 120 days (b), and COD degradation rate over 120 days (c) in the ICPB.

3.5. Changes in the microbial community

The species distribution and a clustering heat map of species abundance in the biofilms were presented in Fig. 8 and S12, respectively, both of which vary greatly depending on the sample. Azospirillum (34.1%) and Brevundimonas (31.4%) were the dominant species in the initial microalgal biofilms (I1, I2, I3). These two bacterial strains have a mutually beneficial symbiotic relationship with microalgae [41], which improves the activity of microalgae and promotes their growth while inducing a positive effect on wastewater treatment [42]. Although these two types of bacteria still existed in the microalgal biofilms (C1, C2, C3) in the coupling stage, their abundance had decreased significantly to only 10.6% and 15.7% of the initial values, respectively. In addition, under the stress of tetracycline, Rhizobium (6.7%), Salinarimonas (21.4%), and Coelastrella sp. (7.0%) were enriched in the biofilms at the coupling stage. The intracellular cytochrome P450 enzyme system in Rhizobium can enhance the degradation of organic matter (e.g., tetracycline and photocatalytic products) through dealkylation and dehalogenation [43,44], and Salinarimonas is known for its metabolism of various pollutants. During the rapid degradation of tetracycline via photobiocatalytic coupling, low tetracycline concentrations stimulate Coelastrella sp. in biofilms and improve the ability of the biofilm to utilize pollutants for lipid production [45]. The biofilms (S1, S2, S3) in the microalgae-only system were the most severely stressed by tetracycline, and their biodiversity differed significantly from that of the first two biofilms. Four dominant species (Bacteroidia, Reyranella, Gemmatimonas, and Sandaracinaceae) were present in the microalgae biofilm, accounting for approximately 60% of the total community. Recall that the activity of microalgae in the microalgae-only system was severely inhibited by long-term exposure to tetracycline; this phenomenon was further confirmed by the enrichment of Bacteroidia, which are exclusive anaerobes [46], i.e., their enrichment indicates an anoxic environment. In addition, Reyranella and Gemmatimonas were adaptively enriched under the stress environment containing tetracycline, and they were able to degrade macromolecular organic matter [47], such as polycyclic aromatic hydrocarbons [48].

Fig. 8.

Fig. 8

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Relative abundance of the top 20 associated bacterial genera in S. obliquus biofilms and changes based on 16S rDNA sequences. The total number of 16S rDNA reads was 718,613, and the average number of counts per sample was 79,656. The 1, 2, and 3 notations represent the triplicated samples from three ICPB systems with the same culture conditions: (C1–C3) microalgal biofilm in the coupled system; (I1–I3) microalgal biofilm in the initial system; (S1–S3) microalgae biofilm in the microalgae-only system.

4. Conclusions

In this study, a novel GeO2/Zn-HPW/TiO2 POHF was developed and intimately coupled with an algal–bacterial biofilm to create an ICPB system for the highly efficient removal and biomass-induced conversion of tetracycline. The rapid detoxification of tetracycline by the POHFs, which exhibit high photocatalytic activity, generates biodegradable intermediates that can be degraded by the biomass of the biofilm. The photosynthetic capabilities of the biofilm can then provide the O2 required for photocatalysis. In addition, biodegradation decreases the competition among photocatalytic products for •OH and O2•− and enhances photocatalysis. Rhizobium, Salinarimonas, and Coelastrella sp., which can promote algal growth and resource transformation via interactions between algae and bacteria, were enriched in the biofilm. As a result, the tetracycline removal and mineralization rates of this photobiological synergistic ICPB system reached 98.1% in 5 h and 95.0% in 10 h. Meanwhile, the biomass concentration of the biofilm in the reactor increased 11-fold. This study provides guidance for developing systems to promote the rapid and sustainable degradation of toxic organic pollutants for biomass conversion applications.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

CRediT authorship contribution statement

Nianbing Zhong and Haixing Chang: Conceptualization, Methodology, Investigation, Data curation, Writing – original draft. Chuanbao Xiao and Jilin Yuan: Investigation, Validation, Writing – review & editing. Linyang Li and Dengjie Zhong: Formal analysis, Validation, Writing – review & editing. Yunlan Xu and Quanhua Xie: Investigation, Writing – review & editing. Xuefeng He: Investigation, Writing – review & editing. Min Li: Resources, Supervision, Writing – review & editing.

Acknowledgments

We acknowledge the service of Biomarker Technologies, Beijing, China, for the 16S rDNA sequencing analyze. This work was supported in part by the National Natural Science Foundation of China (NSFC) (52176178, 51876018), Innovation Research Group of Universities in Chongqing (CXQT21035), Scientific and Technological Research Program of Chongqing Municipal Education Commission of China (KJZD-M202201101), Chongqing Postgraduate Innovation Project (CYS22318), and Chongqing University of Technology Graduate Education High Quality Development Project(gzlcx20222022).

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ese.2022.100234.

Contributor Information

Nianbing Zhong, Email: zhongnianbing@163.com, nzhong@asu.edu.

Haixing Chang, Email: changhx@cqut.edu.cn.

Appendix A. Supplementary data

The following is the Supplementary data to this article.

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