Nanoparticle-Supported Lipid Bilayers as an In Situ Remediation

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Nanoparticle Supported Lipid Bilayers as an In Situ Remediation Strategy for Hydrophobic Organic Contaminants in Soils Hairong Wang, Bojeong Kim, and Stephanie L. Wunder Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es504832n • Publication Date (Web): 02 Dec 2014 Downloaded from http://pubs.acs.org on December 7, 2014

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Environmental Science & Technology

“Nanoparticle Supported Lipid Bilayers as an In Situ Remediation Strategy for Hydrophobic Organic Contaminants in Soils” Hairong Wang1, Bojeong Kim2 and Stephanie L. Wunder1* 1

Department of Chemistry, 2Department of Earth and Environmental Science, Temple University, Philadelphia, PA 19122 *corresponding author [email protected] Abstract Polycyclic aromatic hydrocarbons (PAHs) are persistent environmental organic contaminants, due to low water solubility and strong sorption onto organic/mineral surfaces. Here nanoparticle-supported-lipid-bilayers (NP-SLBs) made of 100 nm SiO2 nanoparticles and the zwitterionic lipid, 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC), are investigated as constructs for removing PAHs from contaminated sites, using benzo-a-pyrene (BaP) as an example. DMPC in the form of small unilamellar vesicles (SUVs) or DMPC-NP-SLBs with excess DMPC-SUVs to support colloidal stability, added to saturated BaP solutions, sorb BaP in ratios of up to 10/1 to 5/1 lipid/BaP, over a 2 week period at 33 oC. This rate increases with temperature. The presence of humic acid (HA), as an analog of soil organic matter, does not affect the BaP uptake rate by DMPC-NP-SLBs and DMPC-SUVs, indicating preferential BaP sorption into the hydrophobic lipids. HA increases the zeta potential of these nanosystems, but does not disrupt their morphology, and enhances their colloidal stability. Studies with the common soil bacteria Pseudomonas aeruginosa demonstrate viability and growth using DMPCNP-SLBs and DMPC-SUVs, with and without BaP, as their sole carbon source. Thus, NP-SLBs may be an effective method for remediation of PAHs, where the lipids provide both the method of extraction and stability for transport to the contaminant site. Abbreviations: polycyclic aromatic hydrocarbons (PAHs); natural organic matter (NOM); soil organic matter (SOM); humic acid (HA), sodium salt (HA); nanoparticles (NPs); supported lipid bilayer (SLB); nanoparticle supported lipid bilayer (NP-SLB); silica (SiO2), small unilamellar vesicles (SUVs); multilamellar vesicles (MLVs); benzo[a]pyrene (BaP); 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC); nano-differential scanning calorimetry (nano-DSC); dynamic light scattering (DLS); transmission electron microscopy (TEM); zeta potentials (ζ)

Introduction Hydrophobic organic contaminants such as polycyclic aromatic hydrocarbons (PAHs)1 are considered as priority pollutants by the USEPA since they are widespread and represent serious risks for ecosystems and human health due to their carcinogenic and mutagenic effects. PAHs are often the contaminants of primary concern at Superfund National Priorities List Sites. They are mainly produced by the incomplete combustion of biogenic organic matter and fossil fuels, but also by coal gasification, petroleum cracking, and crude oil refinement. They have low water solubility and are thus concentrated in sediments and soils. Elevated levels of PAHs have been detected in urban surface and subsurface soils throughout the US2. PAHs can be accumulated in 1 ACS Paragon Plus Environment


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soils in very large amounts3, in concentrations often several orders of magnitude greater than established EPA or state regulatory screening levels.

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The removal of PAHs is complicated by their low water solubility and strong adsorption onto environmental surfaces3a, 16. In aquatic environments hydrophobic contaminants such as PAHs sorb from water17 onto natural organic matter (NOM)18, but also onto clays and minerals19, particularly when there is little organic carbon present20 and then accumulate in soils and sediments18b. PAHs preferentially bind to NOM, which in turn can also interact with naturally occurring inorganic nanoparticles. Components of NOM include humin and humic acid, lipids and their degradation products (e.g. fatty acids).

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Here we investigate a new method for the remediation of persistent hydrophobic contaminants, using benzo[a]pyrene (BaP) (Figure 1), as an example of a common PAH, from contaminated surface and subsurface soils. The method is based on inexpensive, naturally-occurring nanoparticle (NP) silica (SiO2) and lipids, which form nanoparticle-supported-lipid-bilayers (DMPC-NP-SLBs), if the lipid used is 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC). DMPC-NP-SLBs are small, with high surface-to-volume ratios, so that their interactions with each other and with other lipids and organic and mineral fractions in the soil environment are dominated by their surface properties and aggregation states. Here, the lipids in the DMPC-NPSLBs provide both the method of remediation, namely to adsorb and sequester the BaP, and the colloidal stability necessary for transport to the contaminant source. Although lipids in the form of vesicles, e.g. small unilamellar vesicles (SUVs), have better colloidal stability than lipids on NP-SLBs (since the repulsive entropic forces in the former21 are suppressed when the lipids are

The current strategies available for clean-up of these organic toxins in the surface and subsurface environment include site excavation, inoculation of soil with PAH-degrading bacteria4 and in situ remediation using highly reactive zerovalent-iron (Fe0), bimetallic Fe0/Pd or catalytic (Au/Pd)5 nanoparticles (NPs) that chemically transform the organic toxins into innocuous compounds6 7. For in situ remediation, NPs must be transported to the contaminant source, typically through saturated porous media or through variably saturated (vadose zone) permeable media. Transport distances for NPs under those conditions can be short, from a few centimeters for NZVI8 to a few meters for carbon NPs9. Enhanced transport occurs when the colloidal stability of the NPs is increased, often through the use of water soluble polymers or block copolymers8b, 10 and surfactant micelles11. Polymeric nano-network adsorbent NPs (e.g. polyurethane or poly(ethylene) glycol modified urethane based polymers12) solubilize the hydrophobic contaminant and contain a hydrophilic component that provides steric stabilization for suspension of the NPs in aqueous media. However, currently used NPs and methods for their suspension for environmental remediation have the following concerns. First, these NPs are highly unstable under ambient conditions so that their reactivity to organic toxins is dramatically decreased by aging or oxidation. Furthermore, there may be unfavorable ecological effects of zerovalent iron13, such as toxicity to freshwater and marine organisms14 and potential neurotoxicity15. Second, the use of water soluble polymers that are not (or not readily) biodegradable or recyclable is not a sustainable way to resolve complicated environmental problems. Last, they are economically disadvantaged for application to large contaminated areas, with costs between $50 – 110/kg for nano-iron.

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on a rigid support22), the process of SLB formation can also occur on a variety of environmental surfaces, so that the SUVs may prematurely adsorb/fuse to soil components before arriving at the targeted remediation site.

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Since in soils PAH sorption occurs preferentially to soil organic matter (SOM), the interaction of BaP with DMPC-NP-SLBs in the presence and absence of humic acid (HA), one of the main components of SOM/NOM, are both investigated. The ability of Pseudomonas aeruginosa (P. aeruginosa), a gram-negative bacterium commonly found in soil and water environments, to use the lipids and BaP in the DMPC-NP-SLBs as carbon sources, is demonstrated by bacterial growth studies. Thus, DMCP-NP-SLBs can be used to solubilize and sequester hydrophobic organic toxins, making them available for in situ biodegradation23 or removal in the surface and subsurface soils, providing a sustainable and biodegradable method for remediation of these toxins. Once both the lipids and organic contaminants sequestered in the lipids are biodegraded, only SiO2, a natural component of soil, will remain.

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Materials and Methods

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Preparation of multilamellar (MLV) and small unilamellar (SUV) vesicles

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Preparation of supported lipid bilayers

Materials 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC, 14:0 PC) (Avanti Polar Lipids, Alabaster, AL) was used without further purification. All solutions/suspensions were prepared with chloroform and 20 mM NaCl using HPLC grade water (Fisher Chemicals Fairlawn, NJ). The humic acid, sodium salt (STBD5313V) and benzo[a]pyrene (BaP) (SLBF4553V), 98% purity, were obtained from Sigma-Aldrich. The 100 nm SiO2 beads were a gift from Nissan Chemicals.

The DMPC and BaP were separately dissolved in chloroform and mixed to produce varying lipid/BaP molar ratios (100/0 to 2.5/1), in order to provide calibration standards to estimate the amount of BaP uptake by the lipids. These solutions were dried under a nitrogen stream, followed by drying in a vacuum oven at room temperature overnight to remove any residual solvent. The films were hydrated at 50°C (above Tm of DMPC) using 20 mM NaCl in HPLC grade water with constant shaking to produce multilamellar vesicles (DMPC-MLVs). The DMPC-MLVs underwent five freeze-thaw cycles followed by extrusion (40 x) through a 100 nm polycarbonate membrane with a Mini-Extruder (Avanti Polar Lipids) to produce small unilamellar vesicles (DMPC-SUVs).

Supported lipid bilayers (SLBs) were prepared from nominal 100 nm SiO2 beads and DMPC or DMPC with BaP. The DMPC-SUVs and SiO2 were brought to the same temperature (40oC) before mixing, after which the DMPC-SUV/SiO2 mixtures were incubated for one hour at 40°C. The amount of SiO2 added was that required to achieve single bilayer coverage, i.e. where the



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surface area of the lipids in the SUVs (SASUV) is equal to the surface area of the SiO2 beads (SASiO2), i.e. SASUV/SASiO2 = 1/1, or twice that amount, SASUV/SASiO2 = 2/1.

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BaP and DMPC-SUVs or DMCP-NP-SLBs with or without humic acid

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Migration of BaP into DMPC-SUVs or DMPC-NP-SLBs (with or without humic acid) was investigated by mixing them with saturated BaP solutions (with solid BaP still observed) all at 20 mM NaCl. Concentration dependent sorption24 was not investigated.

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Bacterial strain and media

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Wild-type Pseudomonas aeruginosa strain PA01 HS was obtained from Professor Nancy Love (University of Michigan Ann Arbor). The growth media (pH 7) were PAM9, with acetic acid as the sole carbon source, or the same media, referred to as M-PAM9, in which equivalent amounts of lipid or lipid + BaP (in the form of DMPC-SUVs or DMPC-NP-SLBs) were the sole carbon source (Supplementary Information (SI)). All culture media with additives were sterile-filtered through sterile PVDF 0.45um membranes or 0.2 µm filters (Acrodisc with Supor membranes, Pall Co., NY, USA) right before use to remove precipitates that could interfere with particle size analyses and optical measurements.

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For the bacterial growth studies (SI), cells of P. aeruginosa strain PA01 HS were grown in PAM9 in culture tubes at 37ºC for 24 hours with constant shaking. After 24 hours, bacterial cell growth was monitored by measuring the absorbance at 600 nm (OD600) using a Cary Win 50 UV-Vis spectrometer. The culture media was then diluted to an OD600 of 0.07 with fresh PAM9 (an 8-fold dilution). To test their ability to utilize DMCP-SUVs, DMCP-NP-SLBs with and without BaP (with lipid/BaP ratios of 20/1) as the only carbon source, DMPC-SUVs, DMPCNP-SLBs, DMPC-SUV/BaP(20/1), and DMPC-NP-SLBs/BaP (20/1), as well as controls using only M-PAM9 or SiO2 (with PAM9) were prepared, added to the diluted cultures and incubated for another 24 hours at 37oC with constant shaking. Each treatment (referred to as S in Table 1) had an abiotic control (referred to as R in Table 1), i.e., culture tubes were prepared and run in the exactly same way but in the absence of P. aeruginosa PA01 HS. Bacterial cell growth was monitored by measuring OD600. All growth experiments were repeated twice.

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Characterization

Bacterial Growth Studies

A drop of bacterial cells with DMPC-NP-SLB treated with BaP (labeled as 4S in Table 1) was then placed onto Ultrathin Carbon Type-A, 400 Mesh copper TEM grids (Ted Pella, Inc. Lot #260813) and allowed to dry. Once the samples had dried, the TEM grids were washed with distilled water to remove salts and allowed to dry under ambient conditions.

Nano-differential scanning calorimetry (nano-DSC) measurements were obtained on a TA Instruments (New Castle, DE) Nano DSC-6300, at cooling/heating rates of 1oC/min, using 1 mg lipid in 20 mM NaCl.


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Dynamic light scattering (DLS) and zeta (ζ ) potential data was obtained for the vesicles and DMPC-NP-SLBs (SASUV/SASiO2 = 2/1) using a Malvern (Malvern Instrument Ltd. Malvern, U.K.) Zetasizer Nano-ZS. Diameters are reported either as z averages or volume distributions obtained by cumulant analysis25. The concentrations used were the same as for the nano-DSC and the concentrations of humic acid are specified in the text. All measurements were done at 25 o C.

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Transmission electron microscopy (TEM) data was obtained on a JEOL JEM-1400 in the bright field mode at 120 kV to image bacterial cells and DMPC-NP-SLBs with BaP.

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Results and Discussion Quantification of BaP Uptake by Vesicles and NP-SLBs In order to determine how much BaP could be incorporated into DMPC-MLVs/DMCP-SUVs and DMPC-NP-SLBs were prepared with varying molar ratios of BaP. DMPC-NP-SLBs with SASUV/SASiO2 = 1/1, or twice that amount (SASUV/SASiO2 = 2/1) were used. When the surface area of the lipids in the SUVs (SASUV) is the same as the nominal surface area of the added SiO2NPs (SASiO2), SASUV/SASiO2 = 1, the amount of lipid is just that required to form a single DMPCNP-SLB around the nominal 100 nm SiO2. When SASUV/SASiO2 = 2/1, a single DMPC-NP-SLB and a DMPC-SUV are formed on average, and we have previously shown that the DMCP-SUV is adsorbed to the DMPC-NP-SLB25. When SASUV/SASiO2 = 1/1, the DMPC-NP-SLBs are suspended in water, but precipitate at ionic strengths > 10 mM NaCl, while when SASUV/SASiO2 = 2/1, the nanosystems remain suspended at higher ionic strength (up to 100 mM NaCl tested). Nanosystems prepared with incorporated BaP in molar ratios of lipid/BaP of 2.5/1 to 100/1 provide the calibration plots necessary to determine how much BaP sorbed into the DMPCSUVs and DMCP-NP-SLBs when saturated BaP solutions were added to and incubated with pure DMCP-SUVs or DMCP-NP-SLBs. Nano-DSC provides a method of monitoring inclusion of impurities in lipid bilayers since they perturb the main gel-to-liquid crystalline phase transition temperature, Tm, typically by increasing the disorder of the alkyl chains, and thus lowering Tm. Nano-DSC has the advantage that it does not require labelled probes for the impurities, and is only sensitive to impurities actually included in the bilayer, not to free impurities in the aqueous phase, which may be in equilibrium with impurities in the bilayer. In the case of BaP, which has very limited water solubility, the equilibrium should be predominantly in the direction of the hydrophobic alkyl interior of the bilayer. The nano-DSC traces for the DMPC-MLVs and DMPC-NP-SLBs with SASUV/SASiO2 = 2/1 as a function of lipid/BaP molar ratio are shown in Figure 1, and those for the DMPC-SUVs and DMPC-NP-SLBs with SASUV/SASiO2 = 1/1 are shown in SI Figure 1. As the amount of BaP is increased in any of the nanosystems, there is a downward shift in the main gel-to-liquid phase transition temperature, Tm, indicating increasing disorder in the alkyl chains of the lipids. The DMPC-MLVs, which are large, micrometer-sized multiple bilayers, with a large water pocket at their interior, typically have narrower Tms than the small unilamellar vesicles (SUVs). Therefore, the shift and broadening of Tm with increased incorporation of BaP is more pronounced for the 5 ACS Paragon Plus Environment


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DMPC-MLVs than for the DMPC-SUVs. What is of interest is that the phase transition can be observed at all at loadings of lipid/BaP until 2.5/1, when Tm becomes very broad. However, at lipid/BaP < 2.5/1 DMPC-SUVs exuded BaP (it was observed in the filter paper after extrusion), i.e. not all of the BaP was incorporated into the bilayer.

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Figure 1. Nano-DSC traces of (top) DMPC-MLVs prepared with BaP in molar ratios of lipid/BaP of 100/1 to 2.5/1. Neat DMPC-MLVs are shown for comparison; (bottom) DMPCNP-SLBs SASUV/SASiO2 = 2/1 prepared with BaP in molar ratios of lipid/BaP of 100/1 to 5/1. Neat DMPC-NP-SLBs are shown for comparison. Structure of benzo[a]pyrene (BaP) shown as inset. 6 ACS Paragon Plus Environment

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In the case of the DMPC-NP-SLBs, the phase transitions are broader, and the shifts not as apparent until a lipid/BaP ratio of 40/1. However, the shifts for the DMPC-NP-SLB SASUV/SASiO2 = 2/1 sample are the same as the combination of the DMPC-SUVs and DMPCNP-SLB SASUV/SASiO2 = 1/1 sample (SI Figure 1), indicating that the BaP partitions equally between the DMPC-NP-SLBs and the attached DMPC-SUVs. The ability of vesicles to incorporate large amounts of hydrophobic small molecules26, lipophilic drugs27 and cholesterol28 has previously been reported, and can result in a similar calorimetric signature, namely a shift and broadening of Tm29, as observed here for BaP. There is also evidence that lipids from humic acid/humin fractionated extracts preferentially sorb PAHs30. Examination of Stability and Morphology of SUVs and NP-SLBs In order to assess whether the nanosystem morphology remains the same when BaP is incorporated, DLS data was obtained for the DMPC-SUVs and DMPC-NP-SLBs (SASUV/SASiO2 = 2/1) as a function of molar ratio of lipid/BaP. The sizes of the DMPC-SUVs and DMPC-NPSLBs after incorporation of BaP remained the same within the detection limits of the DLS data. However, the sizes and polydispersity indices (PDI) were larger for the DMPC-NP-SLBs (SASUV/SASiO2 = 2/1) (Dz = ± 10 nm; PDI = 0.083) compared with the DMPC-SUVs (Dz = ± 10 nm; PDI = 0.058), indicating that DMPC-SUVs are adsorbed to the NPSLBs, or there are some DMPC-NP-SLB “twins”, as previously observed25, 31. At pH ~ 7, the zeta potential (ζ) of the SiO2 is ζ ~ -44 mV, for the SUVs (with and without BaP) ζ = -1.8 mV, for DMPC-NP-SLBs (SASUV/SASiO2 = 1/1) ζ ~ - 22 mV, and for the DMPC-NP-SLBs (with and without BaP) ζ = -4.1 mV, which indicates that the lipid bilayer on the SiO2 shields its negative charge, and that there is additional shielding from the adsorbed SUVs. Since our goal was to determine if the DMPC-SUVs or DMPC-NP-SLBs were able to sorb BaP from the aqueous phase in the presence of other environmental adsorbants of BaP such as HA, it was first necessary to determine the effect HA on the DMPC-SUVs and DMPC-NP-SLBs themselves. In particular, we were interested in whether the DMPC-SUVs and DMPC- NP-SLBs maintained their morphology (i.e. whether they remained as DMPC-SUVs or DMPC-NP-SLBs) and if so, did their size or zeta potential change in the presence of HA. Alternatively, it was possible that these structures were destroyed and the lipids formed bilayers instead on the HA, leaving bare SiO2 in the case of the DMPC-NP-SLBs. HA was therefore added to the DMPCNP-SLBs and DMPC-SUVs at concentrations between 0.025 and 0.5 mg/mL, with the lipid concentration kept constant at 1 mg/mL. DLS data (SI Figure 2) show no effect of HA on DMPC-SUVs except at the higher HA concentrations (due to HA aggregates ~ 900 nm, DLS data for HA alone (not shown)). However, it is not possible to distinguish between HA adsorbed to the SUVs and HA in suspension. Zeta potential (ζ) measurements (Table I) indicate that ζ of the neat HA suspensions increases (becomes more negative) with increase in HA concentration, and that addition of HA to DMPCSUVs decreases the ζ of the suspensions, and also becomes more negative as the HA concentration increases, as has been reported for Al2O3 and ZnO in the presence of HA32. The ζ measurements also cannot distinguish between HA adsorbed to the SUVs, or an average of the 7 ACS Paragon Plus Environment


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nearly neutral DMPC (ζ~ -2 mV) and free HA in suspension, or some combination of the two. However, HA adsorption does increase the colloidal stability of DMPC-NP-SLBs (SASUV/SASiO2 = 1/1) by at least 10-20 fold in 10 mM NaCl (SI Figure 3), as has been previously reported33 for other NPs32a, 33a, 34, through a combination of electrostatic and steric repulsion35.

Table I. Zeta potentials (ζ) of humic acid (HA) suspensions with and without DMPC-SUVs HA mg/mL 0 0.025 0.050 0.075 0.10 0.12 0.25 0.50 NA -33.4 -39.6 -43.0 -44.8 -46.4 -45.3 -46.8 ζ (mV) of HA -2.0 -15.7 -23.4 -21.6 -20.7 -24.5 -35.3 -37.7 ζ (mV) of HA/SUV* *DMPC SUV concentration is always 1mg/mL However, confirmation that the presence of HA, either adsorbed to the SUVs or free in suspension, does not affect the morpology of the SUVs comes from nano-DSC measurements (SI Figure 2), where Tm of the SUVs is the same in the presence and absence of HA in the concentration range between 0.025 and 0.5 mg/mL. This indicates that the HA does not interact strongly with the SUVs, particularly through penetration of the alkyl chains of the bilayer (that would decrease Tm), and that only a weak association of the HA with the polar headgroups exists, as suggested by the zeta potential measurements. Effect of HA on the BaP Extraction by Vesicles and NP-SLBs The above experiments demonstrate that it is possible to form DMPC-SUVs and DMPC-NPSLBs that incorporate BaP in high amounts, and that HA did not destroy the DMPC-SUV morphology. Of greater interest is whether DMPC-SUVs and DMPC-NP-SLBs can sorb BaP from aqueous media, i.e. whether the water insoluble BaP nevertheless has sufficient solubility to enable migration to the DMPC-SUVs and DMPC-NP-SLBs, where they act as “sinks” for the BaP. Further, we were interested in whether this occurs in the presence of HA, i.e. whether the BaP is preferentially sorbed by the lipids in the DMPC-SUVs or DMPC-NP-SLBs, or remains with the HA. Time-dependent nano-DSC traces of DMPC-SUVs (1 mg/mL) with and without [HA] = 0.5 mg/mL incubated with solid BaP at 33°C are shown in Figure 2 top, and schematically in TOC. Similar results (not shown) were obtained for [HA] = 0.075 mg/mL. Enough BaP was added so that if it all went into the DMPC-SUVs, the molar ratio in the SUVs would be < 2.5 lipid/1 BaP. It is clear from the shifts in Tm that BaP is increasingly incorporated into the DMPC-SUVs, and that the presence of HA does not affect this BaP uptake. After 2 weeks, the amount of BaP sorbed by the SUVs with or without HA is at a lipid/BaP ratio of ~ 10/1 to 5/1, and the DMPCSUVs remained intact (there was no change in their size, not shown), providing sufficient time for microbial degradation in most environmental settings. Controls (without BaP) showed no change in size or Tm (SI Figure 4) over the same time period. The shifts therefore occurred as a result of BaP sorption, not from changes in the SUVs or NP-SLBs themselves. Similar results (Figure 2 bottom) were obtained for the DMPC-NP-SLBs (SASUV/SASiO2 = 2/1); after 2 weeks the amount of BaP sorbed, in the absence or presence of HA, was at a lipid/BaP ratio of ~ 10/1 to 5/1. This suggests that the total amount of lipid available in the system determines the amount of BaP uptake, not the form of lipid (whether DMPC-SUVs or DMCP-NP-SLBs). Although 8 ACS Paragon Plus Environment

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experiments were stopped at this time, these results suggest that further BaP incorporation is possible. While previous investigations have shown that aromatic organic contaminants may interact with soil organic matter36 and humic substances37 through pi-pi interactions, these are presumably weaker than the hydrophobic association between BaP and the lipid core, at least in the model system under investigation here.

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Figure 2. Time dependent nano-DSC traces at 33 oC with and without [HA] = 0.5 mg/mL of (top) DMPC-SUVs; and (bottom) DMPC-NP-SLBs (SASUV/SASiO2 = 2/1). [DMPC] = 1 mg/mL. Also shown (in middle) are calibration samples made with BaP. 9 ACS Paragon Plus Environment


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We also increased the temperature at which the DMPC-SUVs and DMPC-NP-SLBs (SASUV/SASiO2 = 2/1) were incubated with the excess BaP, with and without HA, to 65 oC. In this case, the BaP became incorporated into the lipid bilayers at a faster rate (SI Figure 5).

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While both DMPC-SUVs and DMPC-NP-SLBs incorporate BaP, the latter is more desirable for remediation, since DMPC-SUVs may adsorb prematurely to mineral or clay surfaces in soil, as has been observed for nonionic alkyl ethoxylate surfactants38, preventing migration of the SUVs to the contaminated site. DMPC-NP-SLBs (SASUV/SASiO2 = 2/1) are stable colloids, as are DMPC-NP-SLBs (SASUV/SASiO2 = 1/1) with HA, and lipid exchange/removal from NP surfaces is a much slower process than vesicle fusion39. Studies have shown magnetic, dispersable sorbants using surfactants to be more effective for remediation of hydrophobic organic compounds by minimizing the amount of surfactant needed compared with soil-washing methods40.

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Bacterial growth studies

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The results of the bacteria growth experiments presented in Table II clearly show that P. aeruginosa readily grow even when lipids (in the form of DMPC-SUVs and DMPC-NP-SLBs) were the sole carbon source provided. Control experiments showed no bacterial growth when media (M-PAM) with no carbon source was used (1RR), and the same growth with and without added SiO2 using PAM (acetic acid as carbon source), indicating that SiO2 did not kill the bacteria. Within the uncertainties of the experiments, cell growth occurs at comparable levels whether the same amount of lipid is provided in the form of SUVs (1S), or is attached to SiO2 as a supported lipid bilayer (2S). Secondly, even with addition of BaP (3S and 4S), bacterial growth did not seem to slow down, presenting similar OD600 values to those of the DMPC-SUVs or DMPC-NP-SLBs (1S and 2S) at least at the concentrations (lipid/BaP = 20/1) used for these experiments. In the case of the DMPC-NP-SLBs (with or without BaP), there was some precipitation of the cells in the culture media. OD600 measurements were taken while leaving the precipitate at the bottom of the test tube, and after shaking the test tubes so that these aggregates became resuspended. This explains the discrepancy between the OD600 measurements; at the same total lipid, the former produced lower OD600 values than the latter. We believe that the reason for the precipitation is that in M-PAM9 the DMPC-NP-SLBs have a small positive, while P. aeruginosa has a negative zeta potential, resulting in some agglomeration, as observed in the TEM images (SI Figure 6). The TEM images also indicated that cell membranes maintained intact in the presence of SiO2 NPs and no SiO2 NP internalization occurred.

In order to determine whether P. aeruginosa, a common microorganism found in soil, was able to biodegrade these nano-systems, DMPC-SUVs and DMPC-NP-SLBs, with and without BaP were provided as the sole carbon source in growth media, and growth was monitored by optical density (OD) measurements. TEM analysis of samples of bacteria cultured with DMPC-NP-SLB with BaP (SI Figure 6) was used to examine the physical interactions between the DMPC-NPSLBs and bacteria, and to enable visualization of cell membrane disruption.

Table II. Bacterial growth studies using Pseudomonas aeruginosa strain PA01 HS 10 ACS Paragon Plus Environment

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Name 1S

Sample Composition OD600 1.45ml 3.55ml 0.65ml 0.65 SUV M-PAM9 P. aeruginosa* 1R 1.45ml 4.20 ml 0 SUV M-PAM9 1RR 0 5.65 ml 0.65ml 0† M-PAM9 P. aeruginosa* 2S 1.45ml 3.55ml 0.65ml 0.12/1.2** NP-SLB M-PAM9 P. aeruginosa 2R 1.45ml 4.20 ml 0 NP-SLB M-PAM9 3S 1.45ml 3.55ml 0.65ml 0.64 SUV/BAP M-PAM9 P. aeruginosa 3R 1.45ml 4.20 ml 0 SUV/BAP M-PAM9 4S 1.45ml 3.55ml 0.65ml 0.56/1.5** NP-SLB/BAP M-PAM9 P. aeruginosa 4R 1.45ml 4.20 ml 0 NP-SLB/BAP M-PAM9 * The amount of culture media taken after 24 hours ** For the NP-SLBs and NP-SLBs/BaP samples, there was some precipitate. For these samples, the first number was obtained from the supernatant and the second after the sample was shaken, so that the precipitate was included. † The small amount of added cells of P. aeruginosa precipitated/died 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391

These experiments show that P. aeruginosa can use lipids in the forms of vesicles and supported bilayers, and both with incorporated BaP, as the sole carbon sources. While more detailed investigations are planned, these preliminary results show great potential for bioremediation by a common soil/water bacterium to remove BaP (or other persistent, strongly sorbed organic contaminants4, 41) from the environment once lipid extraction of these materials occurs through hydrophobic interactions. Supporting Information Available Details of bacterial growth studies and supplemental figures as referred to in text are available free of charge via the Internet at http://pubs.acs.org. References 1. (a) Harvey, R. G., Polycyclic Aromatic Hydrocarbons. Wiley: New York, 1997; (b) Fetzer, J. C., The Chemistry and Analysis of the Large Polycyclic Aromatic Hydrocarbons. Wiley: New York, 2000. 2. (a) Bradley, L. J. N.; Magee, B. H.; Allen, S. L., Background levels of polycyclic aromatic hydrocarbons (PAHs) and selected metals in New England urban soils. Journal of Soil Contamination 1994, 3 (4), 1-13; (b) Mauro, D. M.; A. Coleman, A.; Sirivedhin, T. Survey of the distribution and sources of PAHs in urban surface soils.; 2006; pp 513-521; (c) Teaf, C. M., Polycyclic aromatic hydrocarbons (PAHs) in urban soil: A Florida risk assessment perspective. International Journal of Soil, Sediment, and 11 ACS Paragon Plus Environment


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Nanoparticle-Supported Lipid Bilayers as an In Situ Remediation

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