Recent advances in the environmental applications of ...

Accepted Manuscript Title: Recent advances in the environmental applications of biosurfactant saponins: a review Authors: Zhifeng Liu, Zhigang Li, Hua Zhong, Guangming Zeng, Yunshan Liang, Ming Chen, Zhibin Wu, Yaoyu Zhou, Mingda Yu, Binbin Shao PII: DOI: Reference:

S2213-3437(17)30579-1 https://doi.org/10.1016/j.jece.2017.11.021 JECE 1988

To appear in: Received date: Revised date: Accepted date:

13-8-2017 12-10-2017 5-11-2017

Please cite this article as: Zhifeng Liu, Zhigang Li, Hua Zhong, Guangming Zeng, Yunshan Liang, Ming Chen, Zhibin Wu, Yaoyu Zhou, Mingda Yu, Binbin Shao, Recent advances in the environmental applications of biosurfactant saponins: a review, Journal of Environmental Chemical Engineering https://doi.org/10.1016/j.jece.2017.11.021 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Recent advances in the environmental applications of biosurfactant saponins: a review Zhifeng Liu a,b *, Zhigang Li a,b, Hua Zhong a,b,c *, Guangming Zeng a,b, Yunshan Liang d, Ming Chen a,b, Zhibin Wu a,b, Yaoyu Zhou e, Mingda Yu a,b, Binbin Shao a,b a

College of Environmental Science and Engineering, Hunan University, Changsha, 410082,

P.R. China. b

Key Laboratory of Environmental Biology and Pollution Control (Hunan University),

Ministry of Education, Changsha 410082, P.R. China. c

State Key Laboratory of Water Resources and Hydropower Engineering Science, Wuhan

University, Wuhan, Hubei 430072, P.R. China. d

College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha, 410128,

China. e

College of Resources and Environment, Hunan Agricultural University, Changsha 410128,

China. * Corresponding authors: E-mail: [email protected] (Z. Liu) E-mail: [email protected] (H. Zhong)

Graphical abstract

Highlights: 1. Recent advances in the environmental applications of saponins were systematically reviewed. 2. The source and properties of saponins were summarized. 3. Organic pollutants and heavy metals remediation mechanism and process by saponins were analyzed. 4. Future research on environmental applications of saponins was proposed.

Abstract In recent years, more and more studies have devoted to investigate the application of biosurfactants to enhance the removal of hydrophobic organic compounds (HOCs) and heavy metals from contaminated soils and water. Saponins are non-ionic surfactants derived from plants, which have special molecular structure with hydrophilic glycoside backbone and lipophilic triterpene derivative. This review introduced the source and properties of saponins, and discussed the environmental application of saponins in the remediation of organic and inorganic contaminants, especially in remediation of the hydrophobic organic compounds pollutants and heavy metals in soils or water. These advantages indicate the good prospect of applying saponins in environment remediation. Moreover, further research on full-scale pollutants remediation using saponins and potential areas for future application of saponins are also proposed.

Keywords: Saponins; Biosurfactants; Environment protection; Mechanism; Hydrophobic organic compounds; Heavy metal

1. Introduction In recent years, the contaminations of soils and water by hydrophobic organic compounds (HOCs) and heavy metals have drawn public attentions. Therefore the removal of HOCs and heavy metal from the environment has become a major problem [1-8]. Fortunately, surfactants can promote the removal of HOCs and heavy metals from contaminated soils and water by partitioning them into the hydrophobic cores of micelles or chelating with metal elements by the oxygen-containing groups [9-15]. Currently, chemical surfactants have been used in enhanced solubilization for HOCs and removal of heavy metals, and usually synthesized by chemical materials [16-19]. However, the chemical surfactants will be retained in the soil matrix and may cause other environmental problems due to their special structures and refractory characteristics. Compared with chemical surfactants, biosurfactants were isolated from plants or produced by microorganisms. And it is easy to obtain and show the excellent performance for remediation process owing to their lower toxicity, better surface activity, readily biodegradable and huge environmental compatibility [20-25]. However, several challenges still remain. For example, it is difficult to obtain large amounts of biosurfactants due to high cost. Therefore, few biosurfactants have been applied to environmental remediation. Fortunately, saponins as non-ionic biosurfactant with excellent performance and wide presence in nature, are mainly secondary compounds in many plants resulting in mass production with low cost [26]. In fact, a number of researchers have reported that saponins could enhance solubilization of HOCs [27-31]. Due to their special molecular structure and superiority with hydrophilic glycoside backbone and lipophilic triterpene derivative, saponins possess of excellent solubilization for HOCs. For example, Kobayashi et al. [31] demonstrated that saponins could increase apparently solubility of the tested three to five rings polycyclic aromatic hydrocarbons (PAHs) above the critical micelle concentration (CMC). Zhou et al. [32] found sapindus saponin could enhance the solubilization for phenanthrene about 87.4% from contaminated soil. In addition, saponins may promote metal removal because this kind of biosurfactants could chelate with heavy

metal by the external oxygen-containing groups and saponins micelle. Previous studies have revealed that saponins could mobilize or remove heavy metal pollutants from soils or water, providing valuable information for saponins used in metal contaminated remediation [29, 3336]. The objective of this review is to describe the source and properties of saponins, and systematically discuss recent advances in the environmental applications of saponins. In addition, it also provides an overview on the mechanism of the removal of various types of contaminants from soils and water. All in all, it provides valuable statements for saponins application in environmental protection.

2. The source and properties of saponins Saponins are secondary compounds derived from many edible and inedible parts of plants, such as roots, stems, bark, leaves, seeds and fruits, and they are natural non-ionic surfactants with excellent performance [30, 37-39]. In addition, they could form stable foam like soap in aqueous solutions [40]. The pure saponins are white, non-volatile, and highly hygroscopic columnar crystal. It is soluble in alkaline aqueous solution and hot glacial acetic acid, cold water, ethanol, petroleum ether and other nonpolar solvents [41]. Saponins are often divided into the triterpenoid saponins and the steroid saponins [42, 43]. Triterpenoid saponins have been extracted from many legumes and alliums, such as soyabeans, peas, beans, lucerne, spinach, tea, sugar beet, sunflower, ginseng, quinoa, liquorice, and horse chestnut etc [44-46]. Steroid saponins are found in tomato seed, aubergine, capsicum peppers, oats, asparagus, alliums, fenugreek, yucca, yam and ginseng [47-50]. Actually, there are few articles about saponins biosynthesis by the enzymes and biochemical pathways. The difference between the triterpenoid saponins and the steroid saponins is that the former can retain 30 carbon atoms, whereas the steroid saponins molecules only existed 27 C-atoms, because they have three methyl groups removed. Structurally saponins are composed of a lipid soluble aglycon, consisting of either a sterol or a triterpenoid and water-soluble sugar

residues. Of which the partial structure is determined as 21-O-angeloyltheasapogenol F 3-O[β-Dgalactopyranosyl (1→2)] [β-D-xylopyranosyl (1→2)-α-L-arabinopyranosyl (1→3)]-βDglucopyranosiduronic acid. The chemical structure of saponin was shown in Fig. 1. The basic structures of sapogenins were shown in Fig. 2: a triterpenoid (a) and a steroid (b). Spirostan and furostan derivatives are known as two main types of steroid aglycones, and the aglycone might contain one or more unsaturated C–C bonds. Saponins consisting of a sugar moiety in general contain galactose, glucose, xylose, rhamnose, glucuronic acid or methylpentose. Glycoside is linked to a hydrophobic aglycone which may be steroid or triterpenoid in nature. Saponins that have one sugar molecule attached to the C3 position are called monodesmosidic saponins. Another kind is bidesmosidic saponins. As the name suggests, it has two sugars attached to the C22 and C3 [40], respectively. Because of the aglycone structure variable, it became the most complicated structure of saponins, which containing some functional groups such as carboxyl, hydroxy, acetate group and esteric band [51, 52]. And based on elemental analysis of saponins, 42 % carbon and 6.2 % hydrogen are contained in organic elements, while 13.9 % sulfated ash are remained in inorganic elements [53]. Saponins have some shortcomings, such as photosensitization [54, 55]. However, they are widely found in plants and have wide range of properties, such as low toxicity, foaming and emulsifying, pharmacoolgical and medicinal properties, sweetness, haemolytic properties and bitterness as well as insecticidal, antimicrobial and molluscicidal activities. Hence, it enjoys wide applications in medicines, cleansers, beverages, confectionery and cosmetics as additives [37, 51, 56-60]. Surfactants are typically classified by the nature of their head group, which can be negatively charged (anionic), positively charged (cationic), both positive and negatively charged (zwitterionic), or uncharged (non-ionic). Biosurfactants are a group of structurally diverse molecules, and are mainly classified by their chemical structure and microbial origin. As a non-ionic biosurfactant, the structure of saponins might be more complex with the charge of its head group and more hydrophobic alkyl chains at a different length compare with some microbial biosurfactants. On the one hand, it might cause a better alteration of the

active site structure and enzyme’s conformation and hence affected more noticeably the catalytic properties of the enzyme. Moreover, non-ionic surfactant might play the roles both in stabilizing and activating enzyme activity, while anionic surfactant only does so in activating [61]. On the other hand, saponins also show many significant advantages, such as preferable environmental compatibility and higher selectivity for HOCs and metal ions removal. In addition, saponins are widely distributed in nature, with low cost and ease of extraction. These additional economic advantages result in easier mass-production compared with many microbial derived biosurfactants [31]. Therefore it has shown great potential for environmental applications.

3. Environmental applications of saponins 3.1. Application of saponins in HOCs remediation 3.1.1. The mechanism of HOCs removal As known, bioremediation is a main process for the successful detoxication or removal of toxic pollutants from environment due to its inexpensive, efficient and environmentally safety [62, 63]. In recent years, biosurfactants are used for organic polluted soil remediation, mainly based on their predominant performance to enhance solubilization and biodegradation of low solubility compounds [20, 64, 65]. As we know, those biosurfactants could raise the solubility of HOCs by enhancing and partitioning them into the hydrophobic cores of micelles, and can also decrease the interfacial tension between water and hydrophobic pollutants to accelerate pollutants transferring into the aqueous solution [66]. There are two approaches to bioremediate organic contaminated soil by using surfactants: (1) extraction of HOCs from soil by surfactants and (2) subsequent biodegradation of HOCs in the extracts [67]. In addition, the process of surfactant enhancing the solubilization of HOCs also depends on a lot of different parameters, including effect of electrolyte, ionic strength, temperature, pH, soil mineral and organic content, soil composition, etc. Critical micelle concentration (CMC) is an important factor. Below the CMC or above the CMC will form the soil roll-up mechanism

and solubilization, respectively. When the concentration is below the CMC, surfactant monomers accumulate at the soil–water and soil–contaminant interfaces, which can increase the contact angle between the hydrophobic contaminants and the soil to change the wettability of the system. Surfactant molecules adsorbed on the surface of the contaminant cause a repulsion between the head groups of the surfactant molecules and the soil particles, and then enhanced the separation of the contaminants from the soil particles [68]. On the other hand, the surfactant can enhance the solubilization of HOCs in the micelles and then partition of pollutants in the solution thereby distinct increases when surfactant concentration above the CMC. However, some negative effects may occur after the addition of biosurfactants. For instance, biosurfactants may reduce the attachment of cells onto oil-related substrates, which may lead to lower biodegradation rates [69, 70]. Therefore, developing eco-friendly and taking effective measures to remedy the ecocontaminated sites simultaneously are the most essential for researchers.

3.1.2 HOCs remediation process PAHs are a class of persistent toxic organic pollutants widely existing in the environment, mainly deriving from chemical fuels such as oil, coal and incomplete combustion of wood, etc. Because of their persistence, highly hydrophobic, toxic, mutagenic and carcinogenic [71], and their water insoluble property may result in those compounds retaining in solid phase and then posing a long-term threat to human health and ecological safety [72] [73]. So the removal of PAHs has been becoming a main concern about contaminated soil or water. Saponins as biosurfactants can improve the electrostatic repulsion between the negatively charged soil surface and saponins molecules and then restrain the sorption of saponins molecules onto soils owing to its special molecular structure. So saponins have potential applications in enhancing solubilization of PAHs and then removal of them from organic contaminated soils and water [30]. The effect of saponins on the degradation of HOCs is summarized in Table 1. Specifically, phenanthrene is one of the most common PAHs in aquatic environments. And due to its low molecular weight, it may be

accumulated in organisms. There are some studies show that biosurfactants saponins can enhance solubilization and simultaneous degradation of phenanthrene. Wu et al. [74] reported that saponins treatments process of phenanthrene removal efficiency varied from 80.53% to 87.06%. Song et al. [29] indicated that saponins could remove simultaneously cadmium and phenanthrene from contaminated soils, and the results showed that the removal efficiency of phenanthrene achieved 76.2% with 3750 mg/L of saponins. Moreover, saponin molecule contains some acidic and ionizable function group in the hydrophilic fraction (e.g., glucuronic acid). Therefore, the solubilization properties of saponin for HOCs showed a large difference from those of synthetic non-ionic surfactants and anionic biosurfactants. Zhou et al. [30] investigated the solubilization characteristics of saponins for PAHs. The results demonstrated that both the molar solubilization ratio (MSR) and the weight solubilization ratio (WSR) values of saponin for phenanthrene are greater than those of the selected synthetic non-ionic surfactants (e.g., Tween 80, Brij 58 and Triton X-100) and rhamnolipid biosurfactants, which showed strong dependence on ionic strength and solution pH. Zhou et al. [32] also made it clear that the solubilization capability of sapindus saponins for phenanthrene were mainly dependent on solution pH, and the sorption of sapindus saponins onto soils decreased with the increasing pH. The results indicated that increasing pH could enhance the ionization of the acidic groups in sapindus saponins molecules and then increased the electrostatic repulsion between the negatively charged soil surface and sapindus saponins molecules. Kobayashi et al. [31] inferred the apparent solubility of phenanthrene, pyrene and benzo[a]pyrene significantly increased with saponins concentration beyond CMC (approximately 1000 mg/L). Finally, aqueous saponins solution above CMC significantly extracted pyrene from low organic carbon soil. However, a similar effect was not observed in high organic carbon soil. Urum et al. [75] found when removing phenanthrenes with surfactant, saponins were the most efficient compared with rhamnolipid and sodium dodecyl sulfate (SDS). Previous studies have demonstrated that saponins have been applied to remediate other PAHs contamination, such as naphthalene, fluoranthene, and halohydrocarbon, including polychlorinated biphenyls (PCBs) or hexachlorobenzene and other hydrocarbons [34, 35, 76-

78]. Gioia et al. [79] indicated quillaya saponin positively influenced soil remediation by enhancing appreciably the depletion rate and raising the extent of soil PCB dechlorination. Xia et al. [33] found that the low concentrations of tea saponin generally enhanced the availabilities of PCBs and root uptake. Kommalapati et al. [80] reported the solubility of hexachlorobenzene (HCB) increases linearly with saponins surfactant concentration beyond CMC. However, the solubility beyond 10% saponins concentration is not linear but follows a saturation-type curve. Roy et al. [81] demonstrated that compared with the typical commercial surfactants, naphthalene and hexachlorobenzene (HCB) in the natural surfactant solutions were demonstrated vary linearly with the concentration of the surfactant. Cao et al. [34] inferred that the mixed solution of 3000 mg/L saponins and 10 mM ethylenediamineN,N'-disuccinic acid (EDDS) significantly simultaneous promotion on Cu, Pb and PCB desorption. The maximal desorption of Cu, Pb and PCB were achieved 85.7%, 99.8% and 45.7%, respectively. Wang et al. [82] demonstrated the elongation of L. multiflorum roots with adding tea saponin in the contaminated soils could enhance the accumulation of Cd and removal of pyrene. Ye et al. [35] found the application of 5.0 g/L tea saponin and 5.0 mL/L peanut oil after two successive washing cycles, which are efficient in extracting 95.1%, 94.6%, 97.1% and of PAHs, polybrominated diphenyl ethers (PBDEs), PCBs, respectively. From another aspect, saponins also affect the microorganisms on HOCs contaminants remediation. In this respect, bacteria can dissolve the pollutants in the aqueous phase and take up the pollutants from the micellar core to external surface by fusion with the cell member. Addition of saponins can increase the mass transfer and permeabilization of the plasma membrane and modification of cell hydrophobicity of bacteria to influence hydrocarbon biodegradation. And saponins may attach to the cell surface and enhance the cell hydrophilic properties, with superior stability in the solution phase. In addition, saponins could decrease the surface tension of hydrophobic compounds such as PAHs which would enable the degradation of these PAHs by PAH-degrading microorganisms [78]. The effect of saponins on HOCs contaminants remediation by microorganisms was shown in Fig.3. Choi et al. [83]

introduced a saponin based on microbubble suspension, which could enhance aerobic biodegradation by microorganisms and deliver gas phase oxygen into the contaminated subsurface. Pijanowska et al. [27] investigated the quillaya saponins optimal biodegradation concentration is 80 mg/L. Under this condition, the degree of 75% hydrocarbon was biodegradated by Pseudomonsa aeruginosa TK. The results showed that the addition of quillaya saponins increased hydrocarbon biodegradation remarkably. Park et al. [84] used microbubble suspension formed by saponins as a biodegradation enhancing carrier, and illustrated some advantages of microbubbles to bioremediation. Firstly, microbubbles show potential to promote bacterial transport [85]. Secondly, it shows plug flow characteristics, which can overcome the matrix heterogeneity. Thirdly, it can be used in a soil flushing process [86]. On the contrary, saponins occur widely in plant species and exhibit a range of biological properties, beneficial or harmful. Many studies indicated that saponins showed antimicrobial activity against various bacteria, fungi and yeast, and its antimicrobial activity depend on pH values. Li et al. [87] demonstrated that saponin had better antimicrobial activity with lower pH values. The –COOH of saponin kept nonionic, when pH value was 4.8. It might be induced that –COOH have a significant impact on antimicrobial activity. Some researchers have noted that saponins could form a complex with biofilm cholesterol. Nevertheless, the addition of saponins has significant influence on cultivated microorganism. Hence, it is significat to select of appropriate microbial consortium and the addition of optimal concentration surfactant for bioremediation of hydrophobic organic compounds is also necessary. Further study related to the application of saponins as economical and ecofriendly surfactant for the remediation of other different HOCs as well as other contaminant mixtures will be concerned. On the other side, the use of surfactants in washing crude oil from contaminated soil is important industrial and environmental applications. Because the process of soil washing is relatively cost effective and fast, and has the potential to treat and recover large volumes of contaminants. Historically, biosurfactants can enhance the removal of non-aqueous phase liquids (NAPLs) sources from the saturated and unsaturated subsurface zone by two general

mechanisms: mobilization and solubility. The mobilization deals with the reduction of interfacial tension between NAPL and injected solution, while the solubility is related to enhancement of the NAPLs solubility in water by micelle formation. There are many studies showed soil washing with different biosurfactant solutions and noted that biosurfactants are effective in removing crude oil from soil. Urum et al [75] found that biosurfactants can be equally as efficient at removing oil from soil as industrial surfactants. The study showed that both rhamnolipid and saponin removed a significant proportion of the naphthalenes whereas SDS removed only a small amount. Saponin removed the greatest proportion of phenanthrenes and SDS the least, which indicated saponin might remove more aromatic hydrocarbons than the aliphatic hydrocarbons in comparison to rhamnolipid and SDS. These results indicate the superior performance of saponins over synthetic surfactants in terms of mobilization of oil pollutants from the contaminated soil, and provide useful information for the selection of surfactants used to remove crude oil from contaminated soils.

3.2 Application of saponins on heavy metal remediation 3.2.1. The mechanism of heavy metal removal The pollution of heavy metals is a significant environmental issue. Due to their high toxicity, it may show hazardous consequence in environment and toxic effects on living organisms in ecosystems even at a low concentration. They can be accumulated in the food chain to pose a serious threat to human health [88-92]. In addition, heavy metals could persist for a long time, only changing their mobility and toxicity and merely being transferred from one chemical state to another, so they are not biodegradable [93]. Furthermore, because of the adsorption of heavy metals in the surface of the soil particles to form stable form, they are so difficult to be removed. Currently, there are many treatment methods and techniques to clean up heavy metals from aqueous solutions and contaminated soil, such as soil washing technology, phytoremediation and adsorption on activated carbon, ion exchange, ion flotation etc [94-97]. Taking the technologies of precipitation dissolution, ion exchange, and

counterion binding to transfer metal ions from aqoeous solution to organic phase, making these contaminants more available for remediation [98, 99]. Previous studies have shown that saponins can change the surface properties by decreasing the surface tension to weaken adhesion between metal ions and the soil, promote the separation of the metal ions from the soil and complexation with saponins [100]. Primarily, refractory state of heavy metals transform into soluble state in the soil, then chelate with trace metal elements so as to achieve desorption effect to enhance metal removal, due to special molecular structure for external carboxyl groups of saponins. The potential mechanism of metal removal by saponins was shown in Fig. 4. There are two ways for saponins to enhance heavy metals desorption from the soil. The first one is that saponins chelates with heavy metal ions in solution, which will reduce the activity of liquid phase of heavy metal ions and induce the desorption of heavy metals in soil. And the second way is to reduce the interfacial tension under the circumstances, then saponins accumulate on the solid-liquid interface and would directly contact with adsorbed heavy metals, which will lead to heavy metal desorption from the soil [101]. However, there is a great need to develop more efficient soil treatment technologies to remove the metals [102].

3.2.2. Heavy metal remediation process In recent years, saponins were used for remediation of heavy metal contaminated soils or water. Various conditions for saponins removing heavy metals are shown in Table 2. As biosurfactants, saponins have some carbonyl with stronger capability of chelating with heavy metals, which put metal chelating ability down to hydroxyl radical scavenging activity. In addition, the chelating capability of saponins will increase with its concentration and pH increment [103]. Saponins molecules contain some acidic and ionizable carboxyl groups associated with the external surfaces of structure, so that they can chelate cationic metals and then remove them [104]. Thereby further studies should focus on how to increase the removal efficiency of metal chelation.

3.2.3. Application of saponins in soil washing technology Soil washing is still an innovative remediation technology for the treatment of heavy metals contaminated soil, which shows great performance for rapid cleanup of a contaminated site, low cost and decrease or relieved of long term liability [105-107]. And the development of soil washing technology caused great interests in a new kind of washing agents termed biosurfactants. Compare with chemical and synthetic surfactants, they have more advantages, which give credits to the fact that they have a low environmental risk, wide exist in nature, and cost effective cost [108]. Because of their high binding capacity with metal ions and low toxicity, biodegradability, and wide exist in nature, saponins seem a promising cleaning agent for soil washing [21, 81, 109]. A few studies have shown that saponins are a plant-derived biosurfactant and can effectively remove metals from soil. Chen et al. [36] demonstrated that use 2000 mg/l of saponins at pH 5–8 and room temperature conditions could remove 83% and 85% of copper and nickel from kaolin by a single washing, respectively. Gusiatin et al. [108] found that multiple saponins washing would influence on the removal and stability of Zn, Cd and Cu in silty clay, loam and loamy sand three types of soils, respectively. After single washing, metal removal was obtained the highest efficiency in loam (67–88%) and loamy sand (82–90%) and also had higher mobility factors (68–84% Zn, 60–76% Cd, and 44–61% Cu), compared with lowest in silty clay (36% Zn, 28% Cd and 9% Cu). Hong et al. [109] evaluated that saponins can be used as a cleaning agent for heavy metal contaminated soils remediation and 90–100% of Cd, 85–98% of Zn were extracted from andosol, cambisol and regosol, respectively. Zhan et al. [110] demonstrated the high efficiency for saponins solution attained removal efficiency of 20.34%, 83.54%, 95.11% and 43.87% of Zn, Pb, Cd and Cu, compared with water alone which only removed minimal amounts of Zn, Pb, Cd and Cu (less than 5%), respectively. Maity et al. [111] reported that at pH 5 and a saponins concentration of 0.15 g/L removal rate of Ni (99%) from the soil was greater than that of Mn (25%) or Cr (73%). Gusiatin et al. [112] showed that saponins and tannic acid might be used potentially to

remove As from contaminated soils. In all soils, As(V) was almost completely removed, whereas content of As(III) was decreased by 37%–73%.

3.2.4. Application of saponins in phytoremediation Phytoremediation is an emerging technology by using plants and their associated microbes for the prevention and cleanup of environmental pollution [58, 113, 114]. Its mechanism is the accumulation of pollutants by the roots of plants and then by translocation to aboveground plant tissues, and eventually plants were harvested to remove contaminants. Phytoremediation is a lifelong accumulation of high levels of pollutants with plants. When phytoremediation reachs the maximum biomass, adding chelating agents, reversibly combining with metal pollutants in soil and then releasing them from the soil and then making them available for plant absorption. Xia et al. [34] found that adding 0.3% tea saponin resulted in Cd concentration increased by 156.8% in stems, 30.1% in leaves, and 96.9% in roots. Zhu et al. [53] evaluated that saponins played an irreplaceable role in the antioxidative activities of Italian ryegrass. The result show that Italian ryegrass was the efficient in heavy metal uptake, and the order was followed by Zn > Cd > Pb. Translocation factor results were identical to the bioconcentartion factor results. In contrast, the shortcomings of phytoremediation are that the pollutant can not only get access to the roots and have impacts on them, but also it must be bioavailable for absorption as well. There are some factors, such as the toxicity level, soil characteristics and the climate, which have to be amenable to plant growth. And phytoremediation also affects longer than other traditional methods. Further researches should concern mechanical remediation technologies and phytoremediation to improve the environment modification technology, and shorten the needed time for phytoremediation.

3.2.5. Application of saponins used in other technologies This paper also reviewed other methods of soil restoration with saponins. Such as ion flotation, foam fractionation and simultaneous desorption etc [115-118]. Kilic et al. [119]

studied oxidative remediation and Cr remediation from tannery sludge with saponins. The results indicated that the extraction efficiency of saponins was mainly dependent on the organic matter content of the sample, and the saponins extracted 24% of Cr6+ from tannery sludge. Cao et al. [34] demonstrated that add of 3000 mg/L saponin and 10 mM EDDS mixed solution significantly promote synergy on Cu, Pb and PCB desorption. The maximal desorption rate were 99.8%, 85.7% and 45.7% of Pb, Cu and PCB, respectively. Maity et al. [120] investigated that the heavy metal removal efficiency was enhanced with increases in time and the saponins concentration, whereas the removal efficiency was decreased with increasing temperature and pH in the foam fractionation process. It turned out that the removal efficiencies were increased significantly from 85% to 98% of Zn, 57% to 56% of Cu and 55% to 95% of Pb with an increase in the flow rate from 0.2 to 1.0 L/min at 0.15 g/L saponins. The present study shows that foam separation technology which is relative to the soil washing process is more effective in removing heavy metals from contaminated industrial soil. Hong et al. [121] demonstrated that the remediation with saponins extracted 50±60% of Cu, 20±45% of Cr, 100% of Pb and extraction of Zn with the saponins treatment was similar to the HCl treatment from the fly ashes, respectively. Yuan et al. [94] evaluated that the maximum removal of Cd, Cu and Zn can reach 71.1%, 81.13% and 89.95%, respectively. In conclusion, saponins have shown great potential for metal ion removal with their eco-friendly biodegradability, higher selectivity and lower cost [122].

4.

Conclusions and future perspectives Saponins are typical plant-derived non-ionic biosurfactants, and widely applied in many

products, such as medicines, cleansers and cosmetics as additives etc. However, the recent advances in the environmental applications of saponins is not reviewed. This work systematically reviewed the source and properties of saponins, and the environmental applications of saponins for remediation of organic pollutants and heavy metals in soils and water. This is not only because of the saponins’ excellent characteristics, but also their

environmental and economic benefits. However, some challenges still remain in the saponins application, such as the lower production cost and application of saponins in the process of environmental remediation on a large scale. And further research regarding the behavior of saponins in the fate and transport of soil contaminants is still required. Moreover, combined use of saponins with other additives, such as chelating agents, organic solvents, and ligand ions, can also provide a preferable capability to remove soil contaminants. For sustainable use of saponins in the future, these aspects deserve investigation. Firstly, further methods are needed to develop model so as to predict the efficiency of the enhanced biodegradation, washing or flushing processes with saponins under various conditions. Secondly, it is necessary to improved purification techniques and exploit effective screening methodologies to obtain desired quantity and quality of saponins in the future. Therefore, growth conditions/optimized production using economically feasible renewable substrates and an efficient multi-step downstream processing would help to produce saponins more economically feasible and profitable. Then, for deeper research, new applications for the biosurfactants regarding nanoparticles are being developed. Future study should focus on the stabilization of the nanoparticles by saponins before the addition during remediation procedures. Acknowledgments The study was financially supported by the Program for Chang Jiang Scholars and Innovative Research Team in University (No.IRT-13R17), the National Natural Science Foundation of China(No.51679085, No.51378192, No.41401358, No.51521006, No.51378190, No.51508177), the Fundamental Research Funds for the Central Universities of

China (No.531107050930)

2013M542112).

and

China

Postdoctoral

Science

Foundation

(No.

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Fig captions: Fig. 1. Chemical structure of saponin (adapted from [123] with the permission of Elsevier Inc.) Fig. 2. Basic structures of sapogenins: a triterpenoid (a) and a steroid (b) ( Schematic based on [124] with the permission of The Nutrition Society)

Fig. 3. The effect of saponins on HOCs contaminants remediation by microorganisms: . Sorption of saponins molecules onto soils. saponins molecules onto HOCs adsorpted onto soil. micelles.

. Sorption of

. Solubilization of HOCs in

. Mass transfer of HOCs from saponins-coated phase to water phase.

Adhesion of micelles to microorganisms cell surface. HOCs from micelle core.

. Microbial incorporation of

. Microbial incorporation of water dissolved HOCs.

Release of saponins molecules from microbial surface. adhesion of microorganisms to entrapped HOCs.

.

.

. Saponins mediated

. Microbial incorporation of

entrapped HOCs.[125] Fig. 4. Schematic overview of potential mechanism of heavy metals removal by saponin.

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Table 1 Literature review on the effect of saponins on the degradation of HOCs.

Surfactant

Saponin

Matrix

Contaminants

Effects

Reference

900 mg/L

Soil

Phenanthrene and cadmium

Removal

[29]

Saponinbased microbubble suspension

2.0 g/L

Oxygenlimiting environme nt

Phenanthrene

Enhancing degradation

[82]

Quillaya saponin (with soya lecithin)

6.5g/L

Soil


[75]

[78]

Saponin

concentration

Phenanthrene and fluoranthene

10 g/L

Soil

Polychlorobiphen yl

Slightly enhanced the biological degradation and dechlorination

Saponin (with rhamnolipid and SDS)

10%

Soil

Petroleum hydrocarbon

Removal

[74]

Saponin (with tannin, lecithin, rhamnolipid)

10%

Soil

Petroleum hydrocarbon

Removal

[122]

Quillaya saponin

80 mg/L

Soil

Hydrocarbon


[27]

75 mg/L

Polluted ground water and soil

Hydrocarbon


[28]

Microbubble suspension made of saponin

2g/L


Phenanthrene


[83]

Tea saponin

0.01% in solution culture

Soil

Polychlorinated biphenyls and cadmium

Enhancing plant uptake

[33]

10%


PAHs

Enhancing solubilization

[30]

Quillaya Saponin (with Triton X-100)

Saponin (with rhamnolipides )

Saponin

Saponin

2500 mg/L

Soil

PAHs


[31]

Saponin (with EDDS mixed solution)

3000 mg/L

Soil

PCB and trace metal elements

Enhanced desorption

[34]

Saponin

18.4–29.4%

Soil

Phenanthrene

Enhanced washing

[32]

Saponin

20 g/L

Ground water

Fluoranthene


[77]

Mixture Saponin and Tween 80

1:1.2 mmol/L

Polluted marine sediment

Phenanthrene

Enhanced Solubilization and Simultaneous Degradation

[121]

Saponin

200 mg /L

Water

Anthracene and phenanthrene


[116]

Tea saponin

40 mg /L

Soil

Pyrene and cadmium

Enhancing phytoremediate d

[81]

Tea saponin

5.0 g/ L

Electronic waste soil

PBDEs/PCBs /PAHs and heavy metals

Enhanced soil washing process

[35]

Saponin

100 mg/ L

Soil

Hydrocarbon


[117]

Saponin

2%

Paddy Soil

PAHs


[118]

Saponin

3 g/ L

Water

Phenanthrene


[73]

Table 2 Summary of saponins under various conditions to remove heavy metals.

Surfactant

Saponin

Medium Kaolin clay

Method

Soil washing

Contaminant

Cu, Ni

Removal efficiency Remove 83% Cu and 85% Ni

Reference

[36]

91% Cu,

Loamy sand, loam, silty clay

Soil washing

Saponin

Andosol, Cambisol, Regosol

Soil washing

Cd, Zn

90–100% Cd, 85–98% Zn

[107]

Saponin

Sewageirrigated soils

Soil washing

Cu, Cd, Pb, Zn

43.87% Cu, 95.11% Cd, 83.54% Pb, 20.34% Zn

[108]

Saponin

Industrial soil

Soil washing

Ni, Cr and Mn

99% Ni,

Saponin

Brownfield soils

Soil washing

As(V), As(III)

100%As(V), 37%-73%

Tea saponin

Water solution and soil

Saponin

Cu, Cd, Zn

72% Cd,

[106]

64% Zn

Phytoremediation

Cd

73% Cr,

As(III) 96.9% Cd

[109]

[110]

[33]

Tea saponin in a peanut oil–water solvent system

Electronic waste soil

Phytoremediation

Pb, Ni

87.1% Ni

[35]

Saponin

Soil

Phytoremediation

Zn, Cd, Pb

removal efficiency Zn >Cd>Pb

[53]

83.5% Pb,

Saponin and oxidative remediation

Tannery sludge

Adsorption

Cr

24% Cr

[117]

Saponin and EDDS mixed solution

Soil

Adsorption

Pb, Cu

99.8% Pb, 85.7% Cu

[34]

40%-47% Pb, Saponin

Industrial soil

Foam fractionation and soil flushing

Pb, Cu, Zn

30%36%Cu ,

[118]

16% -18% Zn

Saponin

Municipal solid waste

Fractionated

Cr, Cu, Pb, Zn

Saponin

Dilute wastewater

Ion flotation

Cu, Zn, Cd

20±45% Cr, 50±60% Cu, 100% Pb, 100% Zn 89.95%Zn, 81.13% Cu, 71.1%Cd

[119]

[92]