Facile shape-controlled synthesis of lanthanum oxide with different hierarchical micro/nanostructures for antibacterial activity based on phosphate removal

Abstract

In this study, three La₂O₃ hierarchical micro/nanostructures, nanospindles, nanopolyhedra and nanospheres, were synthesized to remove phosphate from microbial growth media for bacterial inactivation as an antimicrobial strategy. The experiment results showed that the morphology of La₂O₃ hierarchical micro/nanostructures can be controlled by the concentration of the reactants, reaction temperature and cooling treatment. Meanwhile, the properties of the La₂O₃ were researched for phosphate removal and antibacterial activity. The results showed that the different morphologies of the La₂O₃ micro/nanostructures had different removal abilities for phosphate, and can differently inhibit growth of bacteria. Spherical La₂O₃ possesses the best removal ability and antibacterial activity, which indicates that the smaller the La₂O₃ hierarchical micro/nanoparticles are, the stronger the phosphate removal capacity. Compared with nanoparticles, the hierarchical micro/nanoparticles have a significant advantage: they not only have the properties of nanoparticles, but also are relatively stable, not easy to aggregate, and are easy to separate after the reaction. Therefore, the La₂O₃ hierarchical micro-nanomaterials may have very good application prospects for phosphate reduction in open water and to inhibit algae overgrowth.

---

1 Introduction

Recently, lanthanum compounds have attracted considerable attention in hydrogen storage, electrode and sorbent materials, gate insulators and superconductors due to their versatility and multifunctionality.^1–4 Meanwhile, it is known that lanthanum compounds, such as lanthanum carbonate (La₂CO₃), lanthanum hydroxide (La(OH)₃), lanthanum oxide carbonate (La₂O₂CO₃),^5–7 and mixtures of lanthanum compounds (La₂O₃, La₂O₂CO₃ and La₂(OH)₃),⁸ can bind to phosphate so strongly that they can form LaPO₄ and remove excess phosphate in bacterial or algal growth media,⁸ and lead to inhibit the growth of microorganisms and algae. As a typical representative, lanthanum carbonate has been developed as a medicine to reduce the excess phosphate in the human body.⁹ Based on the existing reports on bacterial and algal limitation utilizing lanthanum species,^10–12 we here synthesize three La₂O₃ hierarchical micro/nanostructures and investigate their phosphate removal ability and antibacterial activity.

It is widely accepted that phosphate is essential for growth of all organisms and serves as the main building block for nucleic acids, proteins, and energy carriers.¹³ Phosphate is the only form of phosphorus that can be directly assimilated by microorganisms. Firstly, the initial assimilation of inorganic phosphate for microorganisms proceeds via phosphorylation of ADP, which is affected by phosphate limitation in the environment.⁵ In addition, abundant phosphate is an essential condition to synthesize the cell wall of Gram-positive bacteria and the lipid composition of the membranes of Gram-negative bacteria. It could be affected strikingly within phosphate limitation environment.⁶ Consequently, the lack of phosphate often limits their growth, and efficient phosphate removal in water is expected to be a green strategy to prevent the growth of microorganisms and algae, which would avoid toxic substances released from antibacterial agents.^14–16 On the other hand, reuse of secondary municipal effluent from wastewater treatment plants in water bodies could effectively alleviate freshwater resource shortage.⁹ During the wastewater treatment, excessive nutrients, e.g. phosphate, must be efficiently removed to prevent eutrophication.¹⁷

Considering the strong combination of lanthanum to phosphate and the valid antimicrobial strategy resulted from nutrient starvation of phosphate removal, it is meaningful to explore a facile, high quality and low cost method to synthesize La₂O₃ with micro/nanostructure. In the current study, shape-controlled La₂O₃ hierarchical micro/nanostructures were prepared through the regulation of the concentration of the reactants and the reaction temperature. Three morphologies of La₂O₃ micro/nanostructures were obtained, and were utilized to compare antimicrobial activity. The results indicated that lanthanum oxide can provide a broadly applicable antimicrobial strategy.

2 Experimental section

Material preparation

Series of morphologies micro-nanostructures of La₂O₃ were synthesized by a simple urea homogeneous precipitation process. All the chemicals, lanthanum nitrate hexahydrate La(NO₃)₃·6H₂O, and urea were of analytical pure grade. The morphologies of La₂O₃ were controlled by the adjustment of the concentration of the reactants and the reaction temperature. The synthesis process consists of two steps: synthesis of La(OH)CO₃ precursor and La₂O₃ product. Firstly, spindle La(OH)CO₃ was synthesized at 90 °C with the concentration ratio of 1 : 2 between La (NO₃)₃ and CO (NH₂)₂. While polyhedron La(OH)CO₃ were prepared at 125 °C with the concentration ratio of 1 : 6 between La (NO₃)₃ and CO (NH₂)₂. In the same manner, when the concentration ratio between La (NO₃)₃ and CO (NH₂)₂ is 1 : 400, spherical La(OH)CO₃ was successfully synthesized at 85 °C. Subsequently, the La(OH)CO₃ precursor was calcined from room temperature to 800 °C with a heating rate of 1 °C min⁻¹ and maintained at this temperature for 4 h. Then spherical micro/nanostructures La₂O₃ were obtained. Other La₂O₃ (spindles, polyhedrons) samples were prepared by a similar procedure with different La(OH)CO₃ precursors.

Characterization

XRD measurements were determined using a D8 ADVANCE X-ray diffractometer at a scanning rate of 15° min⁻¹ in the 2θ range from 10–80°, with graphite monochromatic Cu Ka radiation (λ = 0.15405 nm). Perking-Elmer 580B infrared spectrophotometer was used to measure Fourier transform infrared spectroscopy (FT-IR) spectra with the KBr pellet technique. Thermogravimetric and differential thermal analysis (TG-DTA) data were recorded with Thermal Analysis instrument (SDT 2960, TA Instruments, New Castle, DE) with the heating rate of 10 °C min⁻¹ in an air flow of 100 mL min⁻¹. SEM micrographs were obtained using a field emission scanning electron microscope (FE-SEM, S-4800, Hitachi). Microstructures and morphologies were investigated using scanning electronic microscopy (SEM, JEOL JSM-6390LV), transmission electron microscope (TEM, JEM-2100) and field emission scanning electron microscopy (FESEM, SUPRA40). All the measurements were performed at room temperature (RT). Brunauer–Emmett–Teller (BET) (Tristar Micromeritics, Norcross, GA, USA) method was used to determine the specific surface area at 77 K. The BET analysis was measured after out gassing for 90 minutes at 250 °C.

Phosphate absorption capacity of lanthanum oxide nanoparticles and antibacterial activity

To evaluate the binding affinity of the nanoparticles to phosphate, PO₄³⁻ was tested by colorimetry assay. Firstly, standard curve was drawn. Secondly, residual PO₄³⁻ was determined. Specifically, 10% ascorbic acid was freshly prepared as follow: 10 g ascorbic acid was dissolved in 100 mL ddH₂O. Then molybdate solution were prepared as follows: 13 g of (NH₄)₆Mo₇O₂₄·4H₂O was dissolved in 100 mL of double distilled water (ddH₂O). Meanwhile, 0.35 g K(SbO)C₄H₄O₆·1/2H₂O was dissolved in 100 mL of ddH₂O. The prepared (NH₄)₆Mo₇O₂₄ and K(SbO)C₄H₄O₆ solutions were added to 300 mL of dilute sulfuric acid successively. Whereafter the mixed solution was stirred and stored in 4 °C. Then La₂O₃ micro/nanoparticles with different morphologies were added to 15, 25, and 50 μg mL⁻¹ phosphate solution, respectively. 1 mL of ascorbic acid (10%), 2 mL of molybdate solution and above La₂O₃ samples were mixed to determine residual PO₄³⁻ according to absorbance at 710 nm by 752 Ultraviolet Spectrophotometer.¹⁸

Escherichia coli (strain C43) and Staphylococcus aureus (strain TM300) were grown in Difco™ LB broth (Chemie Brunschwig) for 4 h at 37 °C and gently agitation to a concentration of about 10⁸ CFU mL⁻¹. This suspension was diluted to the required concentration with physiological saline (0.9 wt% NaCl in water) or where medium free (in particular phosphate free) was needed, repeatedly (5 times) centrifuged for 60 min at RCF = 1300 (Mistral 3000E, 2500 rpm). Subsequently, the supernatant was removed and the bacterial pellet was resuspended in minimal media. Minimal media was produced from 5 g glucose, 1 g NH₄Cl, 5.4 g NaCl, 0.1 g MgSO₄ and 0.02 g CaCl₂ hexahydrate filled up to 1 liter with ddH₂O and sterilized by autoclaving at 121 °C for 15 min. To quantify the CFU load in a sample, a dilution row (10⁻¹–10⁻⁸) was plated in duplicate on dextrose agar plates (PDA, VWR BDH Prolabo). The plates were incubated at 37 °C for 24 h before readout.

3 Results and discussion

Phase structure, morphology and formation mechanism of La₂O₃

Polyhedral, spherical and spindles-like La₂O₃ micro/nanomaterials with hierarchical micro/nanostructures were synthesized by a simple precipitation method with urea and lanthanum nitrate. The synthesis process consists of two steps: synthesis of La(OH)CO₃ and La₂O₃ (Scheme 1).

Scheme 1 Schematic illustration for preparation of micro/nanostructures La₂O₃ with a simple precipitation method using urea and lanthanum nitrate.

The morphology and microstructure of the products were characterized by SEM and TEM (shown in Fig. 1). The SEM images reveal that three different morphologies of La₂O₃ samples are successfully obtained, including polyhedral, spherical and spindles-like micro-nanostructures. The sizes of the samples are about 1 μm, 10 μm and 12 μm for spherical La₂O₃, polyhedral La₂O₃ and spindles La₂O₃ respectively. From Fig. 1 A(b), B(e) and C(h), the HRTEM images reveal that the surfaces of samples are very rough. It can be further observed that the samples consist of many even smaller nanoparticles with the size of 8–15 nm (inset of Fig. 1A(b), 2B(e) and 2C(h)), showing that the three morphologies of La₂O₃ possess hierarchical micro-nanostructures. The average diameters of the smaller nanoparticles are 8.58 ± 0.08 nm for spherical La₂O₃ (Fig. 1 A(c)), 15.58 ± 0.08 nm for polyhedral La₂O₃ (Fig. 1B(f)) and 13.45 ± 0.08 nm for spindles-like La₂O₃ (Fig. 1C(i)), respectively. In addition, the HRTEM shows that the values of inter planar lattice spacing are 0.29 nm, 0.31 nm and 0.34 nm, respectively, corresponding to the (101), (100) and (110) plane of La₂O₃. The results further show that the prepared La₂O₃ nanocrystals belong to cubic crystalline phase, which are in agreement with the XRD results (inset of Fig. 1A(b), 2B(e) and 2C(h)). In addition, the existence of detectable diffraction rings in the selected-area electron diffraction (SAED) pattern of three hierarchical nano-La₂O₃ (inset of Fig. 1A(b), 2B(e) and 2C(h)) further reveal the formation of polycrystalline products. These results further confirm the formation of the hierarchical nano-La₂O_3.

Fig. 1 SEM and particle size distribution of La₂O₃ and LaOHCO₃. A(a) Spherical LaOHCO₃; A(b) spherical La₂O₃ (inset: lattice fringes and SAED patterns); A(c) size distribution analysis of hierarchically spherical nano-La₂O₃; B(d) polyhedral LaOHCO₃; B(e) polyhedral La₂O₃ (Inset: lattice fringes and SAED patterns); B(f) Size distribution analysis of hierarchically polyhedral nano-La₂O₃; C(g) spindles-like LaOHCO₃; C(h) spindles-like La₂O₃ (inset: lattice fringes and SAED patterns); C(i) Size distribution analysis of hierarchically spindles-like nano-La₂O₃.

Fig. 2 The growth mechanisms of spindles-like La₂O₃ within different points-in-time: (a) 0.5 h; (b) 1 h; (c) 2 h (inset: TEM); (d) 3 h; (e) 4 h; (f) precursors calcined from room temperature to 800 °C for 4 h.

The growth mechanism of the nanostructures is investigated by FESEM and TEM in time-dependent experiments. The results reveal that three different morphologies of La₂O₃ samples, including polyhedral, spherical and spindles-like, are initially derived from spherical morphology, which show similar growth mechanisms to each other. We take spindles-like La₂O₃ for example to explain the growth mechanism in details (shown in Fig. 2). Initially, the La(OH)CO₃ precursors of spherical morphology are formed within 0.5 hour reaction time (Fig. 2a), similarly to the formations of polyhedral and spherical La₂O₃ samples. Then, more La(OH)CO₃ precursor products of spherical morphology assemble to form spindles-like morphology via oriented attachment within 1–3 hours (Fig. 2b–e). Meanwhile, non hollow structures are observed by characterization of TEM (inset of Fig. 2c). Then, we find spindles-like La(OH)CO₃ precursors consist of small particles (inset of Fig. 2e). Finally, the La(OH)CO₃ precursors are calcined from room temperature to 800 °C and maintained at this temperature for 4 h to form La₂O₃ samples with micro/nanostructures (Fig. 2f). The growth mechanisms of polyhedral and spherical products are also researched in time-dependent experiments. The similar growth mechanisms are observed.

XRD patterns of three samples are very similar, one of which is depicted in Fig. 3A as a representation. From Fig. 3A, a strong intensity peak is detected at a diffraction angle of 30°, which is assigned to (101) plane of La₂O₃. The other five peaks are assigned to (100), (002), (102), (110) and (103) lattice planes belonging to cubic crystalline phase of La₂O₃ (JCPDS no. 26-0815). The results indicate that the pure La₂O₃ crystals are successfully prepared by the simple method. Representative FTIR spectra of spherical La₂O₃ and La(OH)CO₃ precursor are shown in Fig. 3B. In the spectrum of La(OH)CO_3, the bands at 1486 and 1412 cm⁻¹ are attributed to the stretching vibration mode of the C–O bond, and the flexural vibration of CO₃²⁻ appear at 859 cm⁻¹, 720 cm⁻¹, 695 cm⁻¹. In the spectrum of La₂O₃, the La–O stretching vibration is at about 653 cm⁻¹, showing La₂O₃ is prepared successfully. The thermogravimetric analysis (TGA) and differential temperature analysis (DTA) traces disclosed the formation process of La₂O₃ from pyrolysis of the La(OH)CO₃ precursor. The TGA curves of the as-prepared La(OH)CO₃ are shown in Fig. 3C. It can be noticed that there are three weight loss steps around 250 °C to 300 °C, 450 °C to 500 °C and 700 to 790 °C. For La(OH)CO₃, the weight loss between 250 °C to 300 °C could be attributed to the removal of water, accompanying the formation of La₂O(CO₃)₂ (see reaction (1)). Then La₂O(CO₃)₂ decomposes to form La₂O₃ and release CO₂, approximately to lose weight 28% (see reaction (2) and (3))

2LaOHCO₃ → La₂O(CO₃)₂ + 2H₂O (1)

La₂O(CO₃)₂ → La₂O₂CO₃ + CO₂ (2)

La₂O₂CO₃ → La₂O₃ + CO₂ (3)

Fig. 3 (A) XRD patterns of polyhedral La₂O₃ and LaOHCO₃. The top red line depicts the diffraction pattern of La₂O₃ nanocrystals, whereas the lower black line corresponds to LaOHCO₃ nanocrystals; (B) FTIR of the spindles La₂O₃ and LaOHCO₃; (C) the thermogravimetric (TG) and DTA of LaOHCO₃; (D) XPS spectra of (a) La 3d, (b) O 1s; (E) N₂-sorption isotherms and pore size distribution curves (inset) for different morphology micro-nano La₂O₃. (a) Spherical La₂O₃, (b) polyhedral La₂O₃, (c) spindle-like La₂O₃.

Fig. 3D presents the X-ray photoelectron spectroscopies of La₂O₃. These spectra exhibit characteristic La 3d and O 1s peaks. As indicated in Fig. 3D(a), the La 3d spectrum shows two peaks at the binging energy 839.48 and 856.77 eV, corresponding to La 3d_5/2 and 3d_3/2, respectively. Meanwhile, the peaks located at a binding energy of around 528.9 and 531.65 eV are both corresponding to the La₂O₃ and H₂O spectrum (Fig. 3D(b)). These results are in accordance with the previous reports on La₂O₃.¹⁹

Brunauer–Emmett–Teller (BET) gas adsorption measurements were used to characterize pore volume, pore diameter and specific surface area (see Fig. 3E). The N₂ adsorption/desorption isotherms of the synthesized La₂O₃ exhibit typical type-IV hysteresis, indicating the presence of pores (Fig. 3E). The samples are mainly mesoporous (inset of Fig. 3E). The BET surface area is measured to be 18.76 m² g⁻¹ for spherical La₂O₃, 12.43 m² g⁻¹ for polyhedral La₂O₃ and 8.14 m² g⁻¹ for polyhedral La₂O₃, respectively.

To determine absorption capacity of La₂O₃ micro-nanostructures for phosphate, ascorbic acid and molybdate solution were employed to measure phosphate group. The initial concentrations of phosphate were 15 μg mL⁻¹, 25 μg mL⁻¹ and 50 μg mL⁻¹, respectively. As shown in Fig. 4, the residual phosphate reduce when La₂O₃ was added. It is worth highlighting that phosphate is absolutely removed by spherical La₂O₃ for only 12 h (Fig. 4a black wire) when initial phosphate concentration is 15 μg mL⁻¹, while 24 h for spindles-like micro-nano La₂O₃ (Fig. 4b black wire), 35 h for polyhedral La₂O₃ (Fig. 4c black wire). Moreover, when initial phosphate concentration is 25 μg mL⁻¹ (red wire), phosphate removal have been accomplished completely by spherical La₂O₃ after 24 h, but accomplished 68% by spindle-like La₂O₃ and 78% by polyhedral La₂O₃ in the meantime. Likewise, superior removal capacity of spherical La₂O₃ is observed, when initial phosphate concentration is 50 μg mL⁻¹. The results show that spherical La₂O₃ has best phosphate removal capacity from water, which attributes to that the spherical La₂O₃ has the smallest particle sizes and the largest BET surface area.

Fig. 4 Phosphate absorption capacity of different morphology micro-nano La₂O₃. (a) Spherical La₂O₃, (b) spindle-like La₂O₃, (c) polyhedral La₂O₃. Black wire, red wire and green wire: initial phosphate concentration is 15 μg mL⁻¹, 25 μg mL⁻¹ and 50 μg mL⁻¹ respectively.

To investigate the effect of phosphate addition and phosphate starvation on microorganism growth, the growth curve of Escherichia coli (a Gram-negative bacteria) and Staphylococcus aureus (a Gram-positive bacteria) were analyzed. Meanwhile, residual phosphate was calculated after microorganism grows for 8 h. As shown in Fig. 5a, the phosphate addition is beneficial to microorganisms growth (both Gram-positive and Gram-negative bacteria) (Fig. 5a and b). It is about 32 times and 26 times larger than the growth rate of E. coli in 2 h when adding phosphate (15 μg mL⁻¹, red line and 50 μg mL⁻¹, blue line), showing that phosphate addition to minimal medium could be beneficial to growth of Escherichia coli (Fig. 5a) and Staphylococcus aureus (Fig. 5b) when growth less than 5 h. However, the benefit of phosphate is suppressed following the addition of La₂O₃. The growth rates of Escherichia coli (Gram-negative bacteria) and Staphylococcus aureus (Gram-positive bacteria) were drawn in Fig. 5a–d. From Fig. 5a, it is only 5 and 2.5 times larger than the growth rate of E. coli in 2 h when adding La₂O₃ to medium in 4 h although the existence of phosphate (15 μg mL⁻¹ and 50 μg mL⁻¹). The results show that the growth rates of E. coli and S. aureus are obviously limited within 5 h when La₂O₃ is added, attributed to effective binding of La₂O₃ to phosphate, namely that phosphate starvation results in limited microbial growth. Given this, phosphate removal ability capacity of three morphology micro-nano La₂O₃ could be a key point to compare antimicrobial properties of La₂O₃. Due to superior removal capacity of spherical La₂O₃, spherical La₂O₃ exhibited better antibacterial property than other two morphologies La₂O₃. It means that phosphate absorption capacity of La₂O₃ is consistent with the antibacterial property of La₂O₃.

Fig. 5 Antibacterial activity (Escherichia coli and Staphylococcus aureus) and phosphate adsorption of spherical La₂O₃ (a, c) Escherichia coli, (b, d) Staphylococcus aureus.

4 Conclusion

We successfully obtained shape-controlled (spindle, polyhedron, and sphere) micrometer-scaled La₂O₃, hierarchically assembled by nanoparticles, through a facile, high quality and low prices method. Meanwhile, they have strong removal ability for phosphate and excellent antibacterial property, especially for sphere micro-nano structure La₂O₃. These hierarchical La₂O₃ micro-nanomaterials may have very good application prospects in water pollution of eutrophication, or reduce excess phosphate in human body in biomedical areas.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (21571053), the Program for Innovative Research Team in Science and Technology in University of Henan Province (18IRTSTHN002), Key Scientific Research Project of Higher Education of Henan Province (18A150046), the 111 project (D17007).

References

1. S. I. Boldish and W. B. White, Vibrational spectra of crystals with the A-type rare earth oxide structure. La₂O₃ and Nd₂O₃, Spectrochim. Acta, Part A, 1979, 35, 1235.
2. J. Gouteron, D. Michel, A. M. Lejus and J. Zarembowitch, Raman spectra of lanthanide sesquioxide single crystals: Correlation between A and B-type structures, J. Solid State Chem., 1981, 38, 288.
3. S. W. Kang and S. W. Rhee, Deposition of La₂O₃ Films by Direct Liquid Injection Metallorganic Chemical Vapor Deposition, J. Electrochem. Soc., 2002, 149, 345.
4. A. M. De Asha, J. T. S. Critchley and R. M. Nix, Molecular adsorption characteristics of lanthanum oxide surfaces: the interaction of water with oxide overlayers grown on Cu (111), Surf. Sci., 1998, 405, 201.
5. W. Harder and L. Dijkhuizen, Physiological Responses to Nutrient Limitation, Rev. Microbiol., 1983, 37, 1.
6. T. F. Thingstad, U. L. Zweifel and R. F. Limnol, P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean T. Frede Thingstad, Limnol. Oceanogr., 1998, 43, 88.
7. C. V. Cardemil, D. R. Smulski, R. A. Larossa and A. C. Vollmer, Vollmer. Bioluminescent Escherichia coli Strainsfor the Quantitative Detection of Phosphate and Ammoniain Coastal and Suburban Watersheds, DNA Cell Biol., 2010, 29, 519.
8. L. C. Gerber, N. Moser, N. A. Luechinger, W. J. Stark and R. N. Grass, Phosphate starvation as an antimicrobial strategy: the controllable toxicity of lanthanum oxide nanoparticles, Chem. Commun., 2012, 48, 3869.
9. M. Kasmi, M. Hamdi and I. Trabelsi, Eco-friendly process combining physical-chemical and biological technics for the fermented dairy products waste pretreatment and reuse, Water Sci. Technol., 2017, 75, 39.
10. F. Haghseresht, S. Wang and D. D. Do, A novel lanthanum-modified bentonite, Phoslock, for phosphate removal from wastewaters, Appl. Clay Sci., 2009, 46, 369.
11. M. M. Gibbs, C. W. Hickey and D. Oezkundakci, Sustainability assessment and comparison of efficacy of four P-inactivation agents for managing internal phosphorus loads in lakes: sediment incubations, Hydrobiologia, 2011, 658, 253.
12. M. J. Barry and B. J. Meehan, The acute and chronic toxicity of lanthanum to Daphnia Carinata, Chemosphere, 2000, 41, 1669.
13. M. Lürling and F. V. Oosterhout, Controlling Eutrophication by Combined Bloom Precipitation and Sediment Phosphorus Inactivation, Water Res., 2013, 47, 6527.
14. J. J. He, W. Wang, F. L. Sun, W. X. Shi, D. P. Qi, K. Wang, R. S. Shi, F. Y. Cui, C. Wang and X. D. Chen, Highly Efficient Phosphate Scavenger Based on Well-Dispersed La(OH)₃ Nanorods in Polyacrylonitrile Nanofibers for Nutrient-Starvation Antibacteria, ACS Nano, 2015, 9, 9292.
15. J. Xie, Y. Lin, C. J. Li, D. Y. Wu and H. N. Kong, Removal and recovery of phosphate from water by activated aluminum oxide and lanthanum oxide, Powder Technol., 2015, 269, 351.
16. M. A. H. Johir, T. T. Nguyen, K. Mahatheva, M. Pradhan, H. H. Ngo, W. Guo and S. Vigneswaran, Removal of phosphorus by a high rate membrane adsorption hybrid system, Bioresour. Technol., 2016, 201, 365.
17. D. L. Correll, The Role of Phosphorus in The Eutrophication of Receiving Waters: A Review, J. Environ. Qual., 1998, 27, 261.
18. P. P. Veerle, J. B. Geert, R. B. An, E. D. B. Marc and C. D. Patrick, Lanthanum: A Safe Phosphate Binder, Semin. Dial., 2006, 19, 195.
19. Y. Gao, Y. Zhang, Y. Zhou, C. Zhang, H. Zhang, S. Zhao, J. Fang, M. Huang and X. Sheng, Synthesis of ordered mesoporous La2O3-ZrO2 composites with encapsulated Pt NPs and the effect of La-dopping on catalytic activity, J. Colloid Interface Sci., 2017, 503, 178.

---

Footnote

† These authors contributed equally to this work.

---