Biosurfactant Use in Heavy Metal Removal from ...

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Biosurfactant Use in Heavy Metal Removal from Industrial Effluents and Contaminated Sites Andrea Franzetti, Isabella Gandolfi, Letizia Fracchia, Jonathan Van Hamme, Panagiotis Gkorezis, Roger Marchant, and Ibrahim M. Banat

CONTENTS 17.1 Introduction........................................................................................................................... 361 17.2 Mechanisms of Biosurfactant–Metal Interactions................................................................. 361 17.3 Removal of Metals from Industrial Effluents........................................................................ 363 17.4 Removal of Metals from Contaminated Sites.......................................................................364 17.5 Conclusions and Future Perspectives.................................................................................... 366 References....................................................................................................................................... 366

17.1 INTRODUCTION Remediation of metal-contaminated environments is particularly challenging given that, unlike organic molecules, metals cannot be biodegraded or mineralized. As such, remediation approaches must focus either on changing the redox state of a metal contaminant to a less toxic form, or on physically removing the metal from the environment. Biological processes can play a central role in the remediation of metal-contaminated water, soil, and sludge as microbes are well known to interact with, and change the properties of, a wide range of toxic and nontoxic metals. For example, metals may be used as electron donors or electron acceptors for energy production within a cell, may be used to shuttle electrons between organisms in syntrophic relationships, or possibly used as cofactors for intracellular and extracellular enzymatic reactions (Croal et al., 2004; Haferburg and Kothe, 2007). Microorganisms have, therefore, evolved mechanisms to oxidize, reduce, transport, bind, and sequester metals to either avoid toxic effects or to assist with basic cellular processes. These physiological responses to metals can be harnessed for bioremediation (Gadd, 2010; Singh et al., 2007; Van Hamme et al., 2006), and the focus of this chapter is on the use of biosurfactants for mobilizing and removing metals from contaminated environments. Specifically, the mechanisms underlying biosurfactant–metal interactions will be described together with applied examples of the use of biosurfactants for treatment of metal-contaminated industrial effluents and contaminated sites.

17.2 MECHANISMS OF BIOSURFACTANT–METAL INTERACTIONS Compared with their synthetic counterparts, biosurfactants hold more promise for being effective in remediation schemes targeting metal removal or mobilization (Sriram et al., 2011). This is, in 361

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part, due to the fact that biosurfactants have been reported to have higher selectivity for a greater number of metal ions and organic compounds, greater tolerance to variations in pH, salt concentrations and temperature, and can generally be produced from widely available, low-cost, and renewable resources (Aşçi et al., 2007; Makkar et al., 2011). In order to save on purification costs, whole microbial cells or microbial exopolymers have been used to concentrate or precipitate metals from liquid waste streams (Banat et al., 2010). Analogous remediation of metal-contaminated soils is more complex because microbial cells and large exopolymers cannot move easily through the soil. In such cases, purified or partially purified biosurfactants avoid that constraint due to their small size, which generally appears to be smaller than 1500 Da (Miller, 1995), in addition to their surface activity that may allow them further penetration of soil particles. On the whole, biosurfactants are less toxic and more biodegradable than chemical surfactants that are being commonly used for in situ remediation strategies designed specifically for metal-contaminated soil (Juwarkar et al., 2008). According to Miller (1995), biosurfactants enhance metal desorption from soils in two ways. First, biosurfactants are able to form complexes with the free, non-ionic forms of metals in solution. This complexation reduces the solution phase activity of metals and speeds desorption following Le Chatelier’s principle. Second, biosurfactants can make direct contact with absorbed metal at the solid–solution interface under conditions of reduced interfacial tension, which allows biosurfactants to accumulate at the solid–solution interface. The mechanisms driving biosurfactant–metal binding include ion exchange, precipitationdissolution, counter-ion association, and electrostatic interaction (Rufino et al., 2012). However, it appears that the ability of biosurfactants to form complexes with metals is the main reason for their utility in remediation of heavy metal-contaminated soil. Specifically, anionic biosurfactants form ionic bonds with metals, generating nonionic complexes with stronger stabilizing forces than those between the metals bonds and soil. Once formed, metal–biosurfactant complexes desorb from the soil matrix and move into the soil solution due to the neutral charge of the complex with a subsequent incorporation of the metal into micelles. In more detail, this mechanism presumes either electrostatic attraction between negatively charged surfaces and metals that form an outer-sphere surface complex, or chemical bonding in which hydroxide groups serve as ligands to form an innersphere surface complex with metals. Both cases are facilitated when oxide groups are easily protonated or deprotonated and surrounded by water molecules. Unlike anionic biosurfactants, cationic biosurfactants can replace charged metal ions on the surface of soil particles by competition for some but not all of the negatively charged surfaces (i.e., ion exchange). Remarkably, the mono-rhamnolipid biosurfactant produced by Pseudomonas aeruginosa has been demonstrated to have a strong affinity for metals such as Cd+2, Zn+2, and Pb+2 through its carboxyl group (Herman et al., 1995; Juwarkar et al., 2007). The strength of these charge interactions means that metal ions can be removed from soil surfaces even in the absence of biosurfactant micelles. A study focusing on the kinetics of Cd2+ desorption from Na-feldspar after rhamnolipid application at a concentration of 77 mM has suggested that the rate-controlling step was correlated with the surface reaction mechanism (Aşçi et al., 2012). Given the uncharged and hydrophobic nature of the micellar core, presumably metal removal was due to charge interactions with the charged polar head groups on the surface of the biosurfactant micelles. Indeed, Das and colleagues reported that lipopeptides produced by Bacillus circulans were able to remove lead and copper from water both below and above the CMC concentration, showing that the metals, being positively charged, bind to the outer hydrophilic surface of the biosurfactants, rather than being incorporated within surfactant micelles (Das et al., 2009). It has been suggested that the high content of uronic acids provide exopolymers produced by Pseudoalteromonas sp. strain TG12 with an ability to complex with metal species such as Na+, followed by Mg2+, K+, Mn2+, Fe2+/3+, and Al3+ (Gutierrez et al., 2008). Interestingly, the authors showed that the presence of 0.6 M NaCl drastically reduced the polymer’s ability to desorb these metals from sediment by competition from Na+ for binding sites on the polymer. Similarly, high salinity led to reduction in Cu2+ and Pb2+ binding by extracellular polymeric substance (Bhaskar and Bhosle, 2006).


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Although micelle formation may not be critical for metal removal, it is important to consider when dealing with bioremediation of environments co-contaminated with organic pollutants. When biosurfactants are released into the environment, they can partition into different abiotic and biotic phases such soil particles, water, air, immiscible liquid, and organic matter, altering the physicochemical conditions at the interfaces (Marchant and Banat 2012a,b). Some of these alterations directly affect interactions between bacteria and contaminants such as hydrocarbons and metals (i.e., micelle formation and emulsification of contaminants, interaction with sorbed contaminants, sorption to soil particles and the alteration of cell-envelope composition and hydrophobicity) (Paria, 2008; Volkering et al., 1997). Therefore, it is necessary to take into account all the processes affecting the fate of biosurfactants before deploying them into a contaminated environment (Franzetti et al., 2006, 2012). Furthermore, environmental conditions can influence the mobility and sorption properties of biosurfactants toward metals. Dahrazma et al. (2008) highlighted the importance of pH on the morphology of rhamnolipid aggregates in heavy metal solutions. Specifically, larger aggregates (>200 nm) formed at more basic conditions than acidic conditions (55–60 nm), thus affecting the mobility of the micelles in porous media like soil. The rhamnolipids were observed to form star-like microstructures at pH 5 and 6 while at pH 7 or 8 regular vesicular dispersions dominated. Raza et al. (2010) hypothesized that the addition of Sr2+/Pb2+ might regulate micelle formation in rhamnolipid solutions due to electrostatic bonding between Sr2+ and negatively charged rhamnolipid carboxylate groups while it can influence the chelating activity via a bidentate ligand in the case of Pb2+.

17.3 REMOVAL OF METALS FROM INDUSTRIAL EFFLUENTS Industrial wastewater may contain significant concentrations of toxic metals, which require removing or recovering prior to discharge. The use of biosurfactants to enhance metal removal from industrial effluents has been proposed by some researchers. A biosurfactant produced by Flavobacterium sp. grown on used vegetable oil was simply added to water in stirred batch reactors. This compound was able to remove over 75% of lead from 100 mg/L lead-contaminated water at 10 × CMC, and was more effective than the synthetic surfactants Triton X-100 and SDS (Kim and Vipulanandan, 2006). The plant-derived surfactant saponin was also used for the removal of metals from water and industrial sludge (Gao et al., 2012; Pekdemir et al., 2000). The effectiveness of saponin from different origins was compared with other biological amphiphilic compounds in the removal of Cd and Pb from contaminated water, but the percentage removal achieved was lower than that obtained with tannic acid (Pekdemir et al., 2000). In comparison with sophorolipid, nonionic saponin, used in batch experiments, was more effective in removing Pb, Ni, and Cr from a contaminated sludge taken from an industrial water treatment plant (Gao et al., 2012). Huang and Liu (2013) suggested the biosurfactant-producing Pseudomonas sp. strain LKS06, rather than its purified product, may be used to remove Cd and Pb from industrial wastewater. In this case, biomass would act as a biosorbent, on which both physical and chemical sorption can take place simultaneously. Biosurfactants have also been exploited as ion collectors in wastewater treatment using a foam flotation process. This two-stage technique is based on the application of a surface-active material or compound to adsorb the metals from the water and a subsequent separation by flotation of the resulting foam. Such a method has been applied to different metals and by using different biosurfactants. For example, Zouboulis et al. (2003) investigated the removal of Zn and Cr ions from aqueous solutions. They concluded that the application of the biosurfactants Surfactin-105 and Lichenysin-A as flotation collectors for the separation of the metal-loaded sorbents, resulted in better float abilities of metal-laden sorbents compared with chemically produced surface active compounds such as SDS or dodecylamine. Similar results were obtained by Chen et al. (2011), who observed a higher Hg removal from artificially contaminated water with surfactin than with SDS and Tween-80, when all were used at a concentration of 10 × CMC.


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The potential of tea-derived saponin to remove Cd, Pb, and Cu through foam flotation was also investigated. The maximum total removal was 81.8% when all operating conditions were properly optimized (Yuan et al., 2008). Recently, more efforts have been devoted to process optimization and modeling. Rangarajan and Sen (2013) studied the removal of Ca, Mg, and Fe(II) in bubble column experiments using the lipopeptide produced by a marine Bacillus megaterium strain. They compared the effect of a simulated biosurfactant solution and of real culture broths, with or without cells, and found that the presence of proteins in the broth without cells increased the overall stability of lipopeptide-enriched foam. However, the presence of cells adversely affected the foam stability. Bodagh et al. (2013) investigated the best conditions for the removal of Cd, Zn, and Cu from wastewater through the use of rhamnolipid produced by P. aeruginosa MA01, although the percentages of removal were not particularly high compared with other papers (not more than 57% for cadmium and even lower for other metals). Interestingly, they also found that Cd removal was affected by the rhamnolipid congener used (di- or mono-rhamnolipid). Another promising method to remove metals present at low concentrations from large volumes of polluted water is micellar-enhanced ultrafiltration (Baek et al., 2003; Ferella et al., 2007). The application of biosurfactants to this method had already been proposed by Hong et al. (1998), who used spiculisporic acid from Penicillium spiculisporum and derived compounds to remove Cu, Zn, Cd, and Ni from aqueous solutions, both metal mixtures and single component solutions. Recently, El Zeftawy and Mulligan (2011) used a rhamnolipid biosurfactant in micellar-enhanced ultrafiltration application targeting metals from contaminated water and concluded that the rhamnolipid-based ultrafiltration technique is an efficient technique for the removal of Cd, Pb, Cu, Zn, and Ni ions from contaminated industrial wastewater. New approaches and attempts for metal stabilization using biosurfactants have also been recently addressed by Gnanamani et al. (2010) who showed bioremediation of Cr(VI) by a biosurfactantproducing marine isolate Bacillus sp. MTCC 5514. Removal of Cr(VI) was obtained in two steps: reduction of Cr(VI) to the trivalent form Cr(III) followed by entrapment in the micelles of the biosurfactant. Biosurfactants have also been reported for the ability to mobilize arsenic from mine tailings (Wang and Mulligan, 2009). Particularly, the mobilization of As(V) under alkaline conditions using rhamnolipid was found to be positively correlated with the mobilization of other metals (i.e., Fe, Cu, Pb, and Zn). Rhamnolipids were also used to extract copper from a mining residue containing 8950 mg Cu per kg ore. A 2% rhamnolipid solution was required to extract about 28% of copper from the ore, while adding 1% NaOH to the biosurfactant solution dramatically improved the copper extraction up to 42% (Dahrazma and Mulligan, 2007). Menezes et al. (2011) treated aqueous effluent produced by acid mine drainage by dissolved air flotation using biosurfactants produced by Candida lipolytica and Candida sphaerica. High percentages of removal of Fe(III) and Mn(II), above 94%, were obtained and the values were found to be similar to those obtained with the use of the synthetic surfactant sodium oleate. Recently, the use of Quillaja bark saponin was proposed to develop a new method of Cr removal from tannery sludge to achieve a cost-effective and environmentally acceptable remediation solution (Kiliç et al., 2011). However, the maximum Cr removal obtained was only 24% at pH 2, while the chemical oxidative process carried out with H2O2 and sulfuric acid at the same pH recovered approximately 70% of the chromium. The low efficiency of saponin was ascribed to the presence of high organic content in the tannery sludge, which affects chromium mobility primarily by its high sorptive capacity and therefore represents a major constraint to the biosurfactant-assisted removal of the metal.

17.4 REMOVAL OF METALS FROM CONTAMINATED SITES These processes have been exploited to achieve the removal of heavy metals from soil for the past 20 years. Since the first demonstration by Miller (1995) showing the ability of biosurfactants to



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facilitate removal of heavy metal from soil, numerous investigations have been published assessing their potential. In recent years, however, some authors have reported concerns regarding the possible toxic effects to autochthonous soil microorganisms, which should be taken into consideration as well as the overall effect of releasing surface active compounds into the environments (Bondarenko et al., 2010; Franzetti et al., 2006). Mulligan et al. (2001) evaluated the performance of surfactin from Bacillus subtilis, rhamnolipids from P. aeruginosa, and sophorolipid from Torulopsis (Starmerella) bombicola and concluded that removal of metals from sediments by use of a solution containing these biosurfactants is feasible. Juwarkar et al. (2008) have shown that a di-rhamnolipid produced by P. aeruginosa BS2 selectively removed chromium, lead, cadmium, copper, and nickel from a multi-element contaminated soil in the order of Cd = Cr > Pb = Cu > Ni. Wen et al. (2009) studied the behavior of rhamnolipids in soils contaminated by Cd and Zn, and suggested that rhamnolipids enhanced metal phytoextraction without the possible increase of metal mobility in the long term. The extent of metal removal by biosurfactants is related to the soil type, pH, cation exchange capacity (CEC), and the nature and concentrations of contaminants and co-contaminants (Singh and Cameotra, 2004). Aşçi et al. (2010) found that metal ions could be efficiently recovered from quartz using rhamnolipid treatment and reported that 91.6% of sorbed Cd (0.31 mmol Cd(II)/kg) and 87.2% of sorbed Zn (0.672 mmol/kg) were recovered. Commonly, soils are co-contaminated with metals and organic pollutants that may be treated with biosurfactants for simultaneous removal of both contaminants. For example, surfactin and fengycin from B. subtilis A21 were effective at removing high concentrations of petroleum hydrocarbons (64.5% with an initial concentration of 1,886 mg/kg) and metals (cadmium, cobalt, lead, nickel, copper, and zinc) resulting in reduced soil phytotoxicity (Singh and Cameotra, 2013b). A washing agent composed of (bio)surfactant and an inorganic ligand was found to be useful for removal of Cd and phenanthrene from soil (Lima et al., 2011). In this study, the removal of Cd2+ increased with increasing iodine concentration, particularly in solutions containing biosurfactants produced by B. subtilis LBBMA155 (lipopeptide) and Flavobacterium sp. LBBMA168 (a mixture of flavolipids) in combination with Triton X-100. Biosurfactant produced by the yeast C. lipolytica was also used for the removal of heavy metals and petroleum derivatives using a soil barrier. Biosurfactant significantly reduced soil permeability, demonstrating its applicability as an additive in reactive barriers allowing the removal of around 96% Zn and Cu and the reduction of Pb and Cd concentrations in groundwater (Rufino et al., 2011, 2012). Much research has been directed toward developing biosurfactant formulations for improving metal removal from soil and water. In this respect, both the addition of other chemicals to biosurfactant solutions as well as the physical form of the formulations (i.e., liquid or foam) have been considered. Liu and colleagues investigated the ability of rhamnolipids, ethylenediaminetetraacetic acid (EDTA), and citric acid to remove metals. The authors concluded that rhamnolipids removed less metals compared with EDTA and citric acid, but increased the effect of the other two kinds of chelating agent in Cu leaching (Liu et al., 2013). Similarly, the rhamnolipid biosurfactant blend (JBR-425) was found to be effective in removing Zn, Cu, Pb, and Cd from soil, both alone and when amended with citric acid and EDTA (Slizovskiy et al., 2011). With respect to the physical form of biosurfactant formulations, Wang and Mulligan (2004) reported that the application of rhamnolipid foam was more effective than rhamnolipid solution for removal of Cd and Ni from a sandy soil. Chen et al. (2011) evaluated the separation of mercury ions from artificially contaminated water using a foam fractionation process with a surfactin, compared with the chemical surfactants (SDS and Tween-80). They concluded that using the biodegradable, nontoxic, and cost-effective anionic biosurfactant surfactin resulted in a higher mercury recovery compared with the synthetic counterpart, probably due to the presence of two carboxylate groups in the surfactin molecule. Given the interest in using plants for phytoremediation of metal-contaminated soils, there is potential to exploit microorganisms that produce both biosurfactants and plant-growth promoting compounds to enhance metal phytoextraction (Rajkumar et al., 2012). In this context, researchers


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have reported both the isolation of plant-associated biosurfactant-producing bacteria and metalresistant microorganisms with potential applications in phytoremediation (Becerra-Castro et al., 2012; Singh and Cameotra, 2013a). A Pseudomonas sp. strain produced both mucoid biofilm and biosurfactant and could tolerate high levels of chromate (Bramhachari et al., 2012). The recently discovered lipopeptide produced by a multi-metal-resistant Escherichia fergusonii strain showed stability at extremes of temperature, pH, and osmotic concentrations (Sriram et al., 2011). Despite the promise, there have been negative impacts reported for the effects of biosurfactants on phytoextraction (Jensen et al., 2011; Wen et al. 2010). Jensen and colleagues found that rhamnolipid treatment was unsuitable because of insufficient mobilization of Cu and Zu during phytoextraction. Similarly, Wen et al. (2010) suggested that neither low nor high concentrations of rhamnolipid are likely to consistently assist Cd phytoextraction using maize or sunflower. Beyond microbial biosurfactants, saponin, a plant (Quillaja)-derived biosurfactant has been evaluated for its ability to remove metals from soil. Chen et al. (2008) observed that 2000 mg L −1 of saponin could remove 83% of the Cu and 85% of the Ni from kaolin containing 0.45 mg copper/g kaolin and 0.14 mg nickel/g kaolin. Gao et al. (2012) concluded that (a) plant-derived nonionic saponin is more efficient than sophorolipid for the removal of metals from polluted sludge; and (b) saponin interacts very well with metals bound to carbonates and Fe-Mn oxides in soils. Indeed, Gusiatin and Klimiuk (2012) found that saponin effectively decreased the total metal concentration in soils contaminated with Cu, Cd, and Zn during soil-washing experiments. More recently, saponin was found to effectively remove high levels of copper, lead, and zinc from soil using foam fractionation (Maity et al., 2013).

17.5 CONCLUSIONS AND FUTURE PERSPECTIVES Biosurfactants are a very diverse group of biomolecules ranging from the low molecular weight glycolipids to the high molecular weight compounds such as extracellular polymeric substance or lipopolysaccharides. Not surprisingly, the physicochemical properties of these molecules also vary greatly, which accounts for the wide range of results that have been achieved using different combinations of biosurfactants and metal ions. What is clear is that high removal of metals can be achieved from both contaminated liquid industrial effluents and from contaminated solid materials and soils. The use of foam fractionation clearly provides an exciting prospect for dealing with the often large volume of effluents produced from industrial processes without the need for recourse to complex technology. One of the major advantages regularly bandied about for the use of biosurfactants is their green credentials, that is, lack of toxicity, biodegradability, and relative stability under a wide range of physicochemical environments. However, we must bear in mind that biosurfactants have been shown to have significant biocidal and biostatic effects on certain groups of microorganisms and therefore the unrestricted addition of biosurfactants to natural environments may have unforeseen consequences. We must also be aware that biosurfactants may not be without deleterious effects on plants, particularly on their roots. Bearing in mind the above caveats biosurfactants are clearly effective in remediation of metals from effluents and environments and may in the future have a significant role on a large scale.

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