Green Treatment of Phosphate from Wastewater Using a Porous Bio-Templated Graphene Oxide/MgMn-Layered Double Hydroxide Composite.

Excessive phosphorus in water is the primary culprit for eutrophication, which causes approximately $2.2 billion annual economic loss in the United States. This study demonstrates a phosphate-selective sustainable method by adopting Garcinia subelliptica leaves as a natural bio-template, where MgMn-layered double hydroxide (MgMn-LDH) and graphene oxide (GO) can be grown in situ to obtain L-GO/MgMn-LDH. After calcination, the composite shows a hierarchical porous structure and selective recognition of phosphate, which achieves significantly high and recyclable selective phosphate adsorption capacity and desorption rate of 244.08 mg-P g-1 and 85.8%, respectively. The detail variation of LDHs during calcination has been observed via in situ transmission electron microscope (TEM). Moreover, the roles in facilitating phosphate adsorption and antimicrobial ability of chemical constituents in Garcinia subelliptica leaves, biflavonoids, and triterpenoids have been investigated. These results indicate the proposed bio-templated adsorbent is practical and eco-friendly for phosphorus sustainability in commercial wastewater treatment.

Introduction

With the rapid population growth and exacerbating chemical pollution, clean water has become a critical demand all over the world. Thus, how to develop efficient and effective technology of wastewater treatment has become one of the major challenges for scientists from various fields (Zhang et al., 2018) (Lai et al., 2019b, Li et al., 2018b, Lin et al., 2019); Liu et al. (2017) (Liu et al., 2019, Wan and Chung, 2018); Phosphate is often present in wastewater due to the industrial, agricultural, and household activities and can lead to water eutrophication and endanger aquatic creatures (Ooi et al., 2017, Ren et al., 2012). There are over 90% of ecoregion rivers exceeding reference median values of total phosphorus concentration announced by the US Environmental Protection Agency and about $2.2 billion annual economic loss due to eutrophication in the US freshwaters (Dodds et al., 2009). Considering that phosphate is an essential and limited element and is widely used in agriculture and various industries, it is imperative to develop technologies that can separate and recycle phosphate from wastewater to not only reduce the impact on the environment but also produce more resources of fresh water and phosphate. Recently, various researches such as crystallization (Peng et al., 2018), membrane process (Thong et al., 2016), electrodialysis (Zhang et al., 2013), and chemical and biological methods have been proposed for removal of phosphate from wastewater (Li et al., 2016a, Seviour et al., 2003). Adsorption method is considered as one of the most practical techniques because it possesses high efficiency, simplicity, and cost-effectiveness and does not produce other hazardous waste. In this regard, various kinds of materials have been applied as adsorbents, including layered double hydroxides (LDHs) (Mandel et al., 2013), carbon materials (Li et al., 2016c), polymers (Zhao et al., 2018), and metal-organic frameworks (Li et al., 2018a), to remove pollutants from wastewater.

LDHs, composed of lamellar hydroxides of divalent (MⅠ2+) and partially substituted trivalent (MⅡ3+) cations, have attracted great attention as green and sustainable materials for applications in removing environmental substances, organic molecule degradation, and energy production (Arrabito et al., 2019, Gu et al., 2018, Wang and O’Hare, 2012). Its general formula is [MⅠ2+1-xMⅡ3+x(OH)2]x+[(Ay−)x/y]·nH2O, in which A represents internal exchangeable anions to balance the overall charge (Shao et al., 2015). Various compositions of LDHs have been reported as promising materials for phosphate removal owing to their chemical stability, structure memory effect, and high anion exchange capacity (Zhou et al., 2011). Yang et al. prepared Mg-Al and Zn-Al LDHs as adsorbents for phosphate removal, where the adsorption mechanism was thoroughly investigated (Yang et al., 2014). Shimamura et al. proposed a model to explain the thermal behavior of ion exchange using Mg/Al-LDH with interlayer phosphate (Shimamura et al., 2012). However, there is still an imperative demand to develop an economical synthesis method of LDHs for phosphate uptake with high surface area, selectivity, and adsorption capacity.

Carbon materials such as active carbon, carbon nanotubes, and graphene have been widely used as adsorbents for removal of various pollutants in wastewater treatment (Davood Abadi Farahani et al., 2018, Wu et al., 2019). Notably, the two-dimensional graphene oxide (GO) possesses high adsorptive capacity owing to its high specific surface area and a great number of binding sites (Mao et al., 2019; Li et al., 2019). In addition, solution-based GO fabrication methods are straightforward and economic, which makes them suitable for large-scale production. However, the low selectivity of GO for phosphate uptake limits the application for practical wastewater treatment. Previous research has reported that using GO combined with various materials for phosphate adsorption, such as titania (Sakulpaisan et al., 2016), Fe2O3 (Bai et al., 2018), and ZrO2 (Luo et al., 2016).

In our previous work, a GO/MgMn-layered double hydroxide (MgMn-LDH) composite calcined at 300°C (GO/MgMn-LDH-300) was prepared for the uptake and release of phosphate in wastewater treatment (Lai et al., 2019a). The mechanism of phosphate removal in the presence of GO was investigated in detail. In this context, to further enhance the adsorption efficiency, it is crucial to provide a hierarchical porous structure. Herein we develop a novel adsorbent utilizing Garcinia subelliptica leaves as a bio-derived template. MgMn-LDH was in situ grown on the leaf-templated GO (L-GO) to obtain L-GO/MgMn-LDH and its calcined sample (L-GO/MgMn-LDH-300), as shown in Figure 1A. Leaves possess a natural hierarchical porous structure, which is composed of many fibers and vessels and can serve as a potential bio-template (Yang et al., 2013). To the best of our knowledge, most of the previous studies indicate that calcination of LDHs results in the collapse of the layered structure and formation of amorphous structures, which is corroborated by X-ray diffraction (XRD) results (Goh et al., 2008, Yan et al., 2016). Here, in this study, we proposed a new finding that recrystallization of MgMn-LDH occurred and led to a more hierarchical porous structure in the presence of Garcinia subelliptica leaves after calcination at 300°C. In situ transmission electron microscopy (TEM) and high-resolution (HR) TEM have been conducted to directly observe and characterize the variations of nanostructures. In addition, the intercalated biflavonoids and triterpenoids can enlarge the LDH layer distance and produce phosphate-specific active sites for phosphate adsorption as illustrated in Figure 1B. The fabricated L-GO/MgMn-LDH-300 not only shows high adsorption capacity of phosphate but also possesses the antimicrobial property. This work demonstrates a novel adsorbent for the effective recycling phosphate from aqueous solutions, adopting Garcinia subelliptica leaves as an inexpensive and natural template, which is scalable, sustainable, and suitable in commercial wastewater treatment.

Figure 1

Schematic Diagram of the Procedure for Preparation of L-GO/MgMn-LDH-300 and Mechanisms of Selective Phosphate Adsorption

(A) The bio-templated LDH composites can produce a more hierarchical porous structure after calcination.

(B) The mechanisms for the enhancement of selective-phosphate adsorption capacity of L-GO/MgMn-LDH-300. The presence of intercalated biflavonoids and triterpenoids can not only increase and support the LDH layer distance during calcination but also form bonding with phosphate to facilitate the selective phosphate adsorption.

Results

Characterizations of the Hierarchical Porous Structure of LDH Composites

Field emission scanning electron microscope (FESEM) images were used to observe the morphological evolution of the procedure for the preparation of L-GO/MgMn-LDH-300. Figure 2A shows that Garcinia subelliptica leaves possess a natural three-dimensional (3D) hierarchical porous structure (the inset is a higher-magnification FESEM image). As shown in Figure 2B, L-GO successfully exhibited the natural leaf's 3D porous structure after GO coating. The leaf skeleton was covered by GO layers with folding edges and wrinkles, as shown in the inset of Figure 2B. Figure 2C and its inset show that the plate-like MgMn-LDHs were in situ coated on L-GO/MgMn-LDH composite's surface. Figure 2D indicates that L-GO/MgMn-LDH-300 composite remained the 3D porous structure of the leaf template. The inset of Figure 2D shows that numerous mesopores formed after calcination at 300°C. The hierarchical porous structure can provide more active sites and result in more efficient ion transport for phosphate adsorption. The morphology and element distributions of L-GO/MgMn-LDH-300 were further analyzed by TEM images, as shown in Figure S1.

Figure 2

Characterizations of the Hierarchical Porous Structure of LDH Composites

(A–D) FESEM images of the LDH composites: (A) Garcinia subelliptica leaves, (B) L-GO, (B) L-GO/MgMn-LDH, and (D) L-GO/MgMn-LDH-300 composites. Insets are the higher-magnification FESEM images, which show that numerous mesopores formed after calcination.

(E) The typical N2 adsorption-desorption isotherms of LDH composites.

(F) Pore size distributions of L-GO/MgMn-LDH-300 and GO/MgMn-LDH-300 composites. The L-GO/MgMn-LDH-300 possesses high mesopores ratio and specific surface area of 91.39 m2 g−1.

The typical N2 adsorption-desorption isotherms of the LDH composites for the characterization of specific surface area were illustrated in Figure 2E. The isotherms of L-GO/MgMn-LDH-300 show a combination of type Ⅱ and type Ⅳ curves, indicating the presence of meso/macropores among this porous structure (Cheng et al., 2018). In particular, the leaf-templated LDH composite shows a H4 hysteresis loop at medium P/P0, which demonstrates the presence of microporous structure. The pore size distributions of the LDH composites are displayed in Figure 2F. The L-GO/MgMn-LDH-300 exhibits a hierarchical porous structure ranging from about 1.5 nm to more than 400 nm. Notably, the L-GO/MgMn-LDH-300 possesses a high volume of mesopores and specific surface area of 91.39 m2 g−1, as shown in Figure S2 and Table S1, respectively. The higher surface area and mesopore ratio of an adsorbent provide more adsorption sites and rapid ion transfer, which facilitates phosphate adsorption process.

Characterizations of the Compositions of LDH Composites

Fourier transform infrared (FTIR) analysis was conducted to characterize the compositions of the LDH composites. As shown in Figure 3A, the adsorption bands of stretching and bending vibration of the interlayer water molecules are located at 3,350 and 1,630 cm−1, respectively. The band at approximately 1,380 cm−1 is assigned to functional groups on GO (C-H and C=O stretching vibrations) and carbonate anions in the interlayer space (Yang et al., 2014). The band at 850 cm−1 results from the M-O bending (M = metal) (Xu et al., 2014). In addition, the main bands at the same positions are observed in the FTIR spectra of Garcinia subelliptica leaves and L-GO/MgMn-LDH. The bands at 2,924 and 2,852 cm−1 are attributed to the C-H stretching of alkane. The band at 1,625 cm−1 is due to the presence of α, β-unsaturated ketone and aromatic bonding. The strong band at 1,020 cm−1 is ascribed to the C-O stretching of alkyl aryl ether. These results correspond to the FTIR spectra of biflavonoids and triterpenoids, which are the major compounds of Garcinia subelliptica leaves (Inoue et al., 2017, Ito et al., 2013, Kedar Kalyani Abhimanyu, 2012). It is suggested that biflavonoids and triterpenoids are present in L-GO/MgMn-LDH.

Figure 3

FTIR and XRD Analyses of Materials

(A) FTIR spectra of Garcinia subelliptica leaves, GO/MgMn-LDH, and L-GO/MgMn-LDH. The peaks in L-GO/MgMn-LDH agree with those of Garcinia subelliptica leaves, indicating the presence of biflavonoids and triterpenoids.

(B) XRD patterns of GO/MgMn-LDH, L-GO/MgMn-LDH, and their calcined samples. The increase of d layer space of L-GO/MgMn-LDH (from 0.78 to 0.90 nm) suggests the intercalation of biflavonoids and triterpenoids. After calcination, L-GO/MgMn-LDH-300 formed new oxide phase of Mg2MnO4, whereas GO/MgMn-LDH-300 showed amorphous phase owing to collapse of the layer structure.

As shown in Figure 3B, XRD pattern of GO/MgMn-LDH reveals dominant and symmetric peaks of (003) and (006), which are regarded as the basal planes, and the asymmetric peaks of (012), (015), and (018) indicate the reflections of non-basal planes. The peaks of (110) and (113) are referred to as the distance of metal hydroxide layers. These reflections indicate the hexagonal lattice with rhombohedral R3m symmetry of typical LDHs (Li et al., 2017, Yang et al., 2014). Comparing with GO/MgMn-LDH, the broad XRD peaks of L-GO/MgMn-LDH indicate the loose crystal structure. The basal spacing d of 0.78 nm at 2θ = 11.41° increases to 0.90 nm at a lower angle of 9.93° for L-GO/MgMn-LDH. The same value of d, related to the distances and ordering of the metal hydroxide layers, shows the same chemical formula for the GO/MgMn-LDH and L-GO/MgMn-LDH (Mandel et al., 2013). It indicates that the increase of interlayer spacing and the weakening of the crystallinity for L-GO/MgMn-LDH result from the intercalation of biflavonoids and triterpenoids, which agree with the results of FTIR spectra. The increase in the interlayer spacing can facilitate ion access to the LDH composite, contributing to a higher phosphate adsorption capacity. After calcination at 300°C for 4 h, interlayer molecules were removed, resulting in collapsing of the layered structure and leading to the amorphous structure of the GO/MgMn-LDH-300, as illustrated in Figure 1B. In contrast, new peaks corresponding to Mg2MnO4 appeared for the L-GO/MgMn-LDH-300 (JCPDS No. 19–0773), suggesting the formation of new oxide phases.

Characterizations of the Variations of Nanostructures by In Situ TEM

Calcination is reported to be an essential factor to affect the anion adsorption by LDHs (Goh et al., 2008). Medaglia et al. proposed an emerging intense UV photoluminescence in Zn/Al LDH, which was activated by thermal dehydration (Prestopino et al., 2019). It clearly shows that thermal desorption of interlayer water results in the progressive collapse of LDHs. While the calcination temperature is over 300°C, undesired oxide phases form and decrease the phosphate adsorption capacity. The effects of calcination temperature on the phosphate absorption had been discussed in Tezuka's work (Satoko et al., 2004). Therefore, the calcination temperature of 300°C was chosen in this study, which resulted in the collapse of the layered structure of L-GO/MgMn-LDH-300. The in situ TEM provides important information to observe and characterize the variations of nanostructures of L-GO/MgMn-LDH composite during calcination (see Video S1). Figures 4A and 4B show the TEM and the selected area electronic diffraction pattern (SAED) images of L-GO/MgMn-LDH composite before and after thermal process by in situ TEM. In Figure 4A, the inset of SAED pattern shows broad concentric rings with diffused halos, which could be attributed to MnO in loose MgMn-LDH structure. After thermal treatment at 300°C, mesopores appear in Figure 4B, suggesting the formation of hierarchical porous structure of L-GO/MgMn-LDH-300 during thermal treatment. In addition, new diffraction rings emerge in the SAED pattern, which can be ascribed to (311), (220), and (111) planes of Mg2MnO4, which confirms the results of XRD. Figure 4C presents the annular bright-field (ABF) scanning transmission electron microscope (STEM) image of L-GO/MgMn-LDH-300 to further characterize the mechanism of forming a hierarchical porous structure. It shows that the mesopores with the diameter of 3–20 nm (pointed out by orange arrows) are surrounded by Mg2MnO4 nanoparticles. Figure S3 shows the energy dispersive X-ray spectra for elemental analysis of the large area and the crystallization part of L-GO/MgMn-LDH-300 composite. It indicates that the Mg:Mn ratio of 3:1 for overall large area decreases to near 2:1 in the crystallization part, which can be attributed to the formation of Mg2MnO4. High-angle annular dark-field (HAADF) STEM atomic image shown in Figure 4D reveals a lattice spacing of 4.76 Ǻ of the nanocrystal, which shall correspond to the (1 1 -1) plane of Mg2MnO4 phase. The diffraction pattern (inset) also proves the formation of Mg2MnO4. It is suggested that Mn elements tended to migrate and interact with oxygen-containing functional groups in GO and Garcinia subelliptica leaves during the calcination process and therefore were oxidized and formed the Mg2MnO4 phase. Besides, numerous vacancies were generated as the by-product of oxidation in the in situ locations, which resulted in the formation of mesopores. These mesopores can not only contribute to the hierarchical porous structure but also facilitate the fast ion transfer of solution into the adsorbents for efficient phosphate adsorption process.

Figure 4

Characterization of the Variations of Nanostructures by In Situ TEM

(A and B) TEM images and SAED images (in the insets) of L-GO/MgMn-LDH composite (A) before thermal treatment and (B) after in situ thermal treatment at 300°C for 100 min.

(C) ABF STEM image of L-GO/MgMn-LDH-300, which presents mesopores (marked by orange arrows) and surrounding Mg2MnO4 nanocrystals.

(D) HAADF STEM atomic images reveal the presence of Mg2MnO4 phases with lattice spacing of 4.76 Ǻ. Inset shows the diffraction pattern of the Mg2MnO4.

Characterizations of the Elements and Bondings of the LDH Composites

X-ray photoelectron spectroscope (XPS) was used to characterize the elements and oxidation states of the LDH composites and bonding with the phosphate group. The high-resolution C 1s of Garcinia subelliptica leaves is present in Figure 5A. The strong peaks for C-O and C=O are attributed to the presence of biflavonoids and triterpenoids. After in situ coating of GO and growing LDH onto the leaves surface, the peak at approximately 289–290 eV representing for metal carbonate appeared (shown in Figure 5B), indicating the interaction with hydrocarbonate group and metal ions (Shchukarev and Korolkov, 2004). Figure 5C shows that L-GO/MgMn-LDH-300 possesses a more intensive peak of metal carbonate, implying that GO and Garcinia subelliptica leaves with the associated abundant oxygen-containing functional groups facilitated the interaction with metal ions in the LDHs during calcination (Lai et al., 2019a). After adsorption of phosphate, the ratio of metal carbonate decreased from 16.4% to 7.1% of phosphate-loaded L-GO/MgMn-LDH-300 (P-L-GO/MgMn-LDH-300) as shown in Figure 5D. It indicates that the carbonate binding to LDH was replaced by phosphate through ion and ligand exchange (Luo et al., 2016). The peaks shown in Figures 5E and 5F correspond to the Mn 2p3/2 state, which are used to determine the multivalent state of Mn in the LDH composites. The oxidation progress of Mn2+ to Mn4+ can be facilitated through calcination, which produced more phosphate-specific adsorption sites in the L-GO/MgMn-LDH-300 composite (Satoko et al., 2004). Figures 5G and 5H are the phosphate-loaded GO/MgMn-LDH-300 (P-GO/MgMn-LDH-300) and P-L-GO/MgMn-LDH-300, respectively. The peak at 133.3 eV was attributed to P-O bonds, which has a splitting value of ∼0.84 eV for P 2p3/2− P 2p1/2 (Susi et al., 2015). It is noted that the downshift of P-O bonds of P-L-GO/MgMn-LDH-300 is observed, indicating the higher electronic density of P 2p binding on P-L-GO/MgMn-LDH-300 than that on P-GO/MgMn-LDH-300. It is assumed that the P-O groups on phosphate can form bonding with aromatic hydrocarbons and the long pairs on biflavonoids and triterpenoids. The formation of the above bondings can facilitate the selective recognition of phosphate, which contributes to high selective phosphate adsorption capacity for L-GO/MgMn-LDH-300.

Figure 5

Characterizations of the Elements and Bondings of the LDH Composites

(A–D) XPS spectra of high resolution for C 1s. (A) Garcinia subelliptica leaves, (B) L-GO/MgMn-LDH, (C) L-GO/MgMn-LDH-300, and (D) phosphate-adsorbed L-GO/MgMn-LDH-300. The higher intensive peak of metal carbonate on L-GO/MgMn-LDH-300 reveals that the functional groups on GO and Garcinia subelliptica leaves facilitated the interaction with metal ions in the LDHs during calcination. The decrease of metal carbonate ratio on P-GO/MgMn-LDH-300 after phosphate adsorption indicates that the carbonate binding to LDH was replaced by phosphate through ion and ligand exchange.

(E and F) The high-resolution Mn 2p peak of composites. (E) L-GO/MgMn-LDH and (F) L-GO/MgMn-LDH-300. The high oxidation state of Mn in the L-GO/MgMn-LDH-300 composite can produce more phosphate-specific adsorption sites.

(G and H) The high resolution of P 2p of the (G) P-GO/MgMn-LDH-300 and (H) P-L-GO/MgMn-LDH-300. The downshift of P-O bonds indicates the higher electronic density of P 2p binding on P-L-GO/MgMn-LDH-300. It is suggested that P-O groups on phosphate can form bonding with aromatic hydrocarbons and the long pairs on biflavonoids and triterpenoids, which can facilitate the selective recognition of phosphate.

Analyses of Practical Phosphate Sustainability in Wastewater

The time-dependence phosphate adsorption capacities of the GO/MgMn-LDH-300 and L-GO/MgMn-LDH-300 composites are presented in Figure 6A. The GO/MgMn-LDH-300 demonstrated rapid phosphate adsorption in the first 1.5 h and subsequently reached equilibrium after 3 h. Its adsorption capacity reaches 44.50 mg-P g−1 after 24 h. In sharp contrast, the L-GO/MgMn-LDH-300 not only showed even faster adsorption in the first 1.5 h, but also reached high phosphate adsorption capacity of 244.08 mg-P g−1 after 24 h, which is 5.5 times that of the GO/MgMn-LDH-300 composite. The adsorption kinetics of LDH composites were investigated using the pseudo-first-order and pseudo-second-order models, which are shown in Figure S4 and summarized in Table 1. Both LDH composites exhibited higher correlation coefficients (R) of the pseudo-second-order model, indicating that the phosphate adsorption processes of both adsorbents were dominated by chemisorption. It is noted that the proposed bio-templated L-GO/MgMn-LDH-300 exhibited an extremely high phosphate adsorption capacity as compared with the published research results, which were summarized in Table 2.

Figure 6

The Practical Phosphate Sustainability by LDH Composites in Wastewater Treatment

(A) The phosphate adsorption capacities of GO/MgMn-LDH-300 and L-GO/MgMn-LDH-300 as a function of time. With the introduction of leaf-template, the LDH composite shows 5.5 times the phosphate adsorption capacity.

(B) The selectivity of L-GO/MgMn-LDH-300 toward different ions.

(C) The pH dependence of phosphate adsorption capacity of L-GO/MgMn-LDH-300.

(D) The phosphate desorption test using 0.1 M NaOH solution in combination with the same concentration of different kinds of regenerating reagents. It indicates that 85.8% of desorption rate can be reached in a regeneration solution containing 0.1 M NaCl and NaOH.

(E) The E. coli inhibition zones for L-GO/MgMn-LDH-300 and GO/MgMn-LDH-300 dispersions with concentrations of 0, 0.75, and 1.0 wt%. The enhanced antimicrobial ability of L-GO/MgMn-LDH-300 indicates that the proposed adsorbent is practical for phosphate sustainability in wastewater treatment application.

Table 1

The Phosphate Adsorption Kinetic Models Parameters for L-GO/MgMn-LDH-300 and GO/MgMn-LDH-300 Composites

Adsorbent	Pseudo-first-order			Pseudo-second-order
	qe [mg-P/g]	k1 [1/h]	R2	qe [mg-P/g]	k2 [g/mg-P h]	R2
L-GO/MgMn-LDH-300	281.77	0.21233	0.9519	294.12	0.00062	0.9893
GO/MgMn-LDH-300	24.00	0.17157	0.9345	45.66	0.02694	0.9995

Table 2

Comparison of Phosphate Adsorption Capacity of This Work with Published Literature

Adsorbent	pH	Initial HPO42− Concentration (ppm)	Solution Volume (mL)	Adsorption Capacity (mg-P/g)	Reference
BR-LDH	7.0	100	50	18.6	Hu et al., 2017
RGO-Zr	5.0	10	200	27.7	Luo et al., 2016
MgAl-LDH	6.0–9.0	200	25	9.8	Yang et al., 2014
ZnAl-LDH	6.0–9.0	200	25	24.8	Yang et al., 2014
Mg/Al-LDH	9.0	9,600	200	57.3	Shimamura et al., 2012
Mg/Al-LDHs biochar	3.0	50	20	81.8	Li et al., 2016b
MgFe–Zr-LDH	7.0–8.0	10	100	30.0	Mandel et al., 2013
Lanthanum hydroxides	N.A.	200	40	107.5	Xie et al., 2014
Zn2Al-PMA-LDH	3.0	100	N.A.	76.0	Yu et al., 2015
MgMn-LDH-300	8.0	384	50	34.1	Satoko et al., 2004
GO/MgMn-LDH-300	6.7	50	200	44.5	This work
L-GO/MgMn-LDH- 300	6.7	50	200	244.1	This work

The selectivity of phosphate adsorption by L-GO/MgMn-LDH-300 was investigated in the presence of competing ions. A 200 mL solution containing HPO42−, Cl−, SO42−, and NO3− of the same concentration of 50 mg L−1 was prepared to evaluate the phosphate uptake. The results are shown in Figure 6B, where L-GO/MgMn-LDH-300 possessed high selectivity toward phosphate and resulted in higher adsorption capacity than other competing ions. The results agree with previous reports that higher-valence anions have stronger interaction with positively charged LDH sheets than monovalent anions (Goh et al., 2008). Moreover, HPO42− can form hydrogen bonds with aromatic hydrocarbons on biflavonoids and triterpenoids, which facilitate the selective adsorption of phosphate for L-GO/MgMn-LDH-300. The density functional theory (DFT) total energy calculations were performed to study selectivity of phosphate adsorption: HPO4, SO4, NO3, and Cl adsorbed on (on-phase) and away from (off-phase) the MgMn-LDH-biflavonoid system as shown in Figure S5. The adsorption energy of these molecules is thus the total energy difference between the on- and off-phase [E (off)-E (on)]. The calculated adsorption energies of HPO4, SO4, NO3, and Cl molecules are 1.43, 1.40, 0.73, and −2.63 eV, respectively. The HPO4 molecule, superior to SO4, NO3, and Cl, shows the strongest tendency of adsorption on the MgMn-LDH-biflavonoid system.

In wastewater treatment, pH is an important parameter affecting the phosphate adsorption process. Herein, the adsorption of phosphate on L-GO/MgMn-LDH-300 was studied at different pH values ranging from 3.0 to 13.0. In Figure 6C, it can be observed that the phosphate adsorption capacity decreases with the increase in pH value from 3.0 to 11.0. As the pH value increases, the increasing competition between OH− and phosphate as well as the negatively charged surface results in lower phosphate adsorption on LDH composites (Li et al., 2016b). The lowest phosphate adsorption capacity is 42.2 mg-P/g around pH 11, which is higher than most of the results summarized in Table 2. It is noted that, as the solution pH rises to 13.0, the phosphate adsorption increases. Since phosphate is pH-related in solution, it exists differently as H2PO4−, HPO42−, and PO43− with pK = 2.12, pK = 7.21, and pK = 12.67, respectively (Yang et al., 2014). In the pH region above 12.67, PO43− is the dominant species, which has significant effects on the hydrogen bonding network (Tang et al., 2009). The presence of orthophosphate can induce the formation of new interactions between P-O groups and hydrogen groups on biflavonoids and triterpenoids. The results indicate that L-GO/MgMn-LDH-300 has high phosphate adsorption in a wide range of pH, which can be applied to practical wastewater treatment.

To investigate the desorption behavior, the L-GO/MgMn-LDH-300 was treated with a Na2HPO4 solution to obtain phosphate-loaded adsorbent, which possessed the phosphate uptake of 150.91 mg-P g−1. The phosphate desorption test was performed using 0.1 M NaOH solution in combination with the same concentration of different kinds of regenerating reagents. After sonication for 6 h, the desorption results were shown in Figure 6D. The desorption rate reaches 85.8% in a regeneration solution containing 0.1 M NaCl and NaOH, which is much higher than other NaOH solutions mixed with NaNO3, Na2CO3, and Na2SO4, respectively. The results agree with the previous reports that LDHs have a high affinity for carbonate anions in the following order of valent state: CO32− ˃ SO42− ˃ Cl− ˃ NO3− (Seftel et al., 2018). The highest desorption rate using NaCl can be contributed from small ionic radius of Cl− (Yan et al., 2018) and stable CH-Cl hydrogen bonds (de Medeiros et al., 2016), which facilitate intercalation into the LDHs to replace phosphate. In addition, the desorption rate can maintain more than 80% after three phosphate uptake-release cycles, as shown in Figure S6. The results show that the phosphate desorption efficiency and reusability of adsorbent can be enhanced in the presence of NaOH and NaCl.

Bacteria in wastewater not only make water recovery process difficult but also cause biofouling of adsorbent (Bhatti et al., 2018). Therefore, the antimicrobial ability is also an important key factor for wastewater treatment. The antimicrobial abilities of the GO/MgMn-LDH-300 and L-GO/MgMn-LDH-300 composites were determined by Escherichia coli through the disk-diffusion (Kirby-Bauer) method (shown in Figure S7). Figure 6E shows the inhibition zone diameters for LDH composite dispersions with different concentrations (the control group is 0.0 wt%). Both LDH composites possessed the inhibition zones, which might result from the composition of MgO. It is proposed that the MgO in aqueous suspension can produce superoxide ion of O2− and kill bacteria effectively (Huang et al., 2005). The results show that L-GO/MgMn-LDH-300 exhibit higher antimicrobial ability than GO/MgMn-LDH-300. More obvious difference of zone diameters can be observed when the concentration increases. The enhancement of antimicrobial ability for L-GO/MgMn-LDH-300 is due to the presence of Garcinia subelliptica leaves. Garcinia subelliptica leaves have been known to contain various kinds of chemical constituents, notably, biflavonoids and triterpenoids, which possess high antimicrobial activity through inhibition of E. coli DNA gyrase (Cushnie and Lamb, 2005, Inoue et al., 2017, Weng et al., 2003). The enhanced antimicrobial ability of L-GO/MgMn-LDH-300 indicates that the proposed work is practical for phosphate removal in wastewater treatment application.

The Investigations of Selective Phosphate Adsorption

To further investigate the mechanism of selective phosphate adsorption by L-GO/MgMn-LDH-300, Raman mapping technique was used to characterize the P-L-GO/MgMn-LDH-300 surface in the region marked with blue dotted square in Figure 7A. Figure 7B illustrates the intensity distribution map of peak at 945 cm−1 (spectrum A in Figure 7D), which is assigned to P-O bond of HPO42− stretching vibration in the phosphate absorbed by ion exchange (Frost et al., 2011). The broadening and unsymmetrical deformations of the P-O bond results from the interactions of hydrogen bonds with LDH composites (Syed et al., 2012). Figure 7C is the intensity distribution map of peak at 429 cm−1, which is accompanied with an intensive band of 578 cm−1 (spectrum B in Figure 7D). The positions of these two bands, ranging between 400 and 600 cm−1, are observed in typical LDH materials, which depends on the compositions of divalent and trivalent cations (Al-Jaberi et al., 2015, Cunha et al., 2012). These two bands are assigned to the M2+-O-M3+ vibration modes and M-OH translation modes. The decreases of M-OH bands in spectrum A result from the ligand exchange of phosphate. Phosphate can form covalent bonds with metal cations while OH ions previously bonded to the metal cations are released (Seftel et al., 2018). It clearly shows that regions with the high-intensity peak of 429 cm−1 possess the low intensity of P-O bonds, indicating the non-specific active sites for selective phosphate adsorption. Figure 7D shows A and B Raman spectra of the selected regions in Figures 7B and 7C, respectively. The characteristic Raman bands at 665 cm−1 in the high-frequency region is due to the Mn-O symmetric stretching vibrations Ag of MnO2 (Gao et al., 2009, Julien et al., 2003). The higher frequency and intensity of the Mn-O stretching vibration in A Raman spectrum can be ascribed to the change in the manganese oxidation state (Julien et al., 2003). In contrast, B Raman spectrum still possesses intensive typical LDH peaks ranging between 400 and 600 cm−1. These observations indicate that Mn oxidation progress to Mn4+ during calcination can result in weakening the typical LDH structure and creating phosphate-specific active sites in L-GO/MgMn-LDH-300.

Figure 7

Investigations of Selective Phosphate Adsorption

(A) The optical microscope image of P-L-GO/MgMn-LDH-300.

(B–D) The Raman mapping of selected regions marked in the blue dotted square in (A). (B) 945 cm−1 and (C) 429 cm−1. (D) The selected A and B Raman spectra marked by black dotted squares in (B) and (C), respectively. It is noted that the region with higher intensive bands at 665 cm−1 due to the Mn-O symmetric stretching vibrations has a higher intensive peak at 429 cm−1 assigned to P-O bond. It indicates that the Mn4+ oxidation state can create more phosphate-specific active sites in L-GO/MgMn-LDH-300.

Discussion

This study proposes an eco-friendly adsorbent of L-GO/MgMn-LDH-300 composite, adopting Garcinia subelliptica leaves as an inexpensive and natural template, for the effective phosphate sustainability from wastewater. The presence of GO and Garcinia subelliptica leaves can not only form hierarchical porous structure but also provide more mesopores for efficient phosphate adsorption. By using in situ TEM, the mechanism of the phase transition of LDH composite was investigated. Garcinia subelliptica leaves contain biflavonoids and triterpenoids, which can intercalate into LDH layers and facilitate ion access to the LDH composite, leading to high phosphate adsorption capacity. In addition, the aromatic hydrocarbons and the lone pairs on biflavonoids and triterpenoids can form bondings to phosphate, resulting in high-phosphate-selective active sites. The antimicrobial ability of L-GO/MgMn-LDH is also enhanced. An efficient and recyclable selective phosphate adsorbent was proposed in this work, with a phosphate adsorption capacity and desorption rate of 244.08 mg-P g−1 and 85.8%, respectively. The process offers a promising technique for the effective and economical phosphate recycling from aqueous solution, which is scalable, sustainable, and suitable in commercial wastewater treatment.

Limitations of the Study

In this study, we investigated the performance of L-GO/MgMn-LDH-300 composite adopting Garcinia subelliptica leaves as bio-template for the effective phosphate sustainability from wastewater. The mechanism of the phase transition of LDH composite in the presence of GO and Garcinia subelliptica leaves was investigated using in situ TEM. Although the mechanism of selective phosphate adsorption was illustrated using Raman mapping technique, the resolution of Raman mapping is too rough to precisely distinguish the phosphate adsorption sites in nanoscale, as a result, the understanding of the phosphate adsorption of LDH composite can be enhanced with improved technique.

Methods

All methods can be found in the accompanying Transparent Methods supplemental file.