Protein Hydrogel Microbeads for Selective Uranium Mining from

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Protein Hydrogel Microbeads for Selective Uranium Mining from Seawater Songzi Kou, Zhongguang Yang, and Fei Sun ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b15968 • Publication Date (Web): 06 Jan 2017 Downloaded from http://pubs.acs.org on January 8, 2017

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ACS Applied Materials & Interfaces

Protein Hydrogel Microbeads for Selective Uranium Mining from Seawater Songzi Kou, Zhongguang Yang, Fei Sun* Department of Chemical and Biomolecular Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong ABSTRACT: Practical methods for oceanic uranium extraction have yet to be developed in order to tap into the vast uranium reserve in the ocean as an alternative energy. Here we present a protein hydrogel system containing a network of recently engineered super uranyl binding proteins (SUPs) that is assembled through thiol-maleimide click chemistry under mild conditions. Monodisperse SUP hydrogel microbeads fabricated by a microfluidic device further enable uranyl (UO22+) enrichment from natural seawater with great efficiency (Enrichment index, K = 2.5×103) and selectivity. Our results demonstrate the feasibility of using protein hydrogels to extract uranium from the ocean.

KEYWORDS: green mining, heavy metal, soft matter, protein material, microfluidics

Uranium fission remains to be a major source of low carbon energy in an age when climate change has become the greatest threat to humanity and at a time when we are in dire need of alternative energies to replace fossil fuels. To date, land deposits provide nearly all uranium supplies for nuclear power generation, which is unsustainable because the terrestrial uranium is limited and improper mining is also detrimental to the environment. There is, however, an enormous uranium reserve in the ocean, 1,000 times that on land,1 waiting to be tapped. But large-scale extraction of uranyl (UO22+), the dominant form of uranium in the ocean, has been extremely challenging due to a very low uranyl concentration (~13.7 nM) and an excess of other ionic species such as calcium, magnesium and carbonate present in seawater.2 An ideal extraction technology has to be able to quickly process large volumes of seawater in order to obtain sufficient amounts of uranium materials. These challenges necessitate uranyl adsorbents with not only high binding affinity and selectivity but also rapid kinetics and large capacity. Various polymers,3-7 microspheres,810 hydrogels,11,12 beads,13,14 chitin fibers15 and metal-organic frameworks16,17 have thus far been developed to recover uranyl from groundwater and seawater, where the uranyl ligands derived from amidoximes, organic carboxylates and phosphates are most commonly used. In addition to these polymeric chelating scaffolds, several other materials including magnetic cobalt ferrite/multi-walled carbon nanotube (CoFe2O4/MWCNTs) hybrids,18 layered metal sulfides,19 melanin pigments20 and DNAzyme-conjugated gold nanoparticles21 have also been explored for their potential use in uranyl adsorption/remediation from aqueous solutions. Most of the existing uranyl adsorbents possess a low affinity and poor selectivity and thus are unsuitable for practical use.22 To

meet these challenges, significant efforts to engineer protein molecules for uranyl binding have been made in the past few years, which have led to the creation of several protein/peptide molecules with superior uranyl binding affinity and selectivity. Specifically, metalloproteins such as calmodulins23 and the nickel (II)binding protein NikR24 with an altered specificity toward UO22+ have been successfully engineered. Another intriguing approach that combines computational design and directed evolution has culminated in a super uranyl binding protein (SUP) with a remarkable selectivity and unprecedented femtomolar affinity toward UO22+.25 A following study showed that the SUP’s uranyl binding affinity and selectivity are determined by three factors, including the nature of the amino acid residues in its binding site, the integrity and strength of the second-sphere hydrogen bond network, and the number of water molecules in the first coordination sphere and that a single mutation of Glu-64 to Asp in the SUP binding site led to a further improved binding and selectivity toward UO22+.26 We envisioned that a better system for oceanic uranyl extraction can be developed by integrating the intrinsic advantage of the SUP protein in selectivity and affinity with that of conventional polymeric adsorbents in kinetics and capacity. In this sense, covalently stitching the SUP proteins into high-order molecular architectures could provide a solution for this challenge.27 In this study we demonstrate the synthesis of a type of new uranyl adsorbents featuring monodisperse protein hydrogel microbeads using a combination of thiol-maleimide click chemistry and microfluidic technologies. We further show that the resulting absorbents are able to enrich uranyl from seawater, suggesting the feasibility of protein materials for uranium mining from the ocean. The crystal structure of the super uranyl binding protein SUP revealed two surface-exposed cysteine residues, Cys-3 and Cys57, at a distance from the uranyl binding site (Figure 1).25 We hypothesized that the reaction of these two cysteine residues with the chemical crosslinker 4-arm PEG-maleimide (PEG-MAL4) (Figure 1A) could lead to the formation of a hydrogel comprising a network of immobilized SUP proteins while retaining their super uranyl binding capabilities. However, the recombinant His6tagged SUP protein obtained from Escherichia coli expression exhibited a modest solubility in water and phosphate-buffered saline (PBS, pH 8.0) buffer and therefore is unsuitable to make hydrogel materials. In order to obtain highly soluble proteins for the hydrogel formation, we genetically fused both termini of the SUP protein with elastin-like polypeptides (ELPs) consisting of repeating pentapeptides (VPGXG) 15 where X represents either valine or glutamate at a ratio of 4:1 (Figure S1). This particular ELP construct was chosen for its high solubility under physiological conditions.28,29 Using an E. coli expression system, we obtained considerable amounts of the recombinant ELP-SUP-ELP (E-SUP-E, MW 28.6 kDa) protein with high purity (Figure S2).

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Figure 1. Formation of super uranyl-binding protein (SUP) hydrogels. (A) Chemical structure of four-arm PEG-maleimide. (B) Structure of the ELP-SUP-ELP protein reveals two surface-exposed residues, Cys-3 and Cys-57 that are distal from the uranyl binding site.25 (C) Schematic illustrating the formation of a SUP hydrogel through a thiol–maleimide click chemistry. PEG-MAL4, four-arm PEG-maleimide. E-SUP-E, ELP-SUP-ELP. ELP, elastin-like protein. An SEM image of a SUP hydrogel (10 wt %) after lyophilization is shown. The inset is a photograph of a SUP hydrogel (10 wt %) cured between two glass slides with 1 mm gap at room temperature. Moreover, the lyophilized E-SUP-E protein powder could readily be dissolved in PBS buffer to make a 10 wt % solution. By mixing the resulting protein solution with the crosslinker PEG-MAL4 (5 wt % in PBS buffer, MW 2.0 kDa) at a 2:1 molar ratio, we indeed observed the formation of a gel-like material after an overnight reaction at room temperature (Figure 1C). A subsequent scanning electron microscopy (SEM) analysis revealed a porous network structure in the lyophilized sample resulting from a 72-h reaction of E-SUP-E + PEG-MAL4 (Figure 1C), while such a structural feature is absent in the E-SUP-E protein alone (Figure S3A) and the freshly mixed sample (Figure S3B). The SUP hydrogel swells only slightly in water and PBS buffer, as we observed no obvious volume change in excess of water or PBS buffer after 24 h, and less than two-fold volume increase in excess of water even after 72 h (Figure S4). We performed rheology tests in the dynamic time-, frequencyand strain- sweep modes to determine mechanical properties of the materials resulting from the reaction of E-SUP-E + PEGMAL4. The dynamic time sweep was conducted at a constant strain (5 %) and frequency (1 rad/sec). Both storage (G’) and loss (G”) moduli were monitored upon mixing the E-SUP-E protein solution with the PEG-MAL4 crosslinker at room temperature. It turned out that the gelation was a slow process, in which G’ and G” reached ~1.6 kPa and ~85 Pa after 24 h, respectively (Figure S5). The dynamic frequency sweep was performed on a 72-h cured gel at a constant strain of 5 %. Figure 2A shows the G’ value remains nearly constant (~1.6 - ~1.9 kPa) as the angular frequency varies from 1 to 100 rad/sec, strongly suggesting a stable, covalently crosslinked hydrogel. The strain sweep was subsequently performed at a fixed frequency of 10 rad/sec. Figure 2B shows that the storage modulus G’ of the SUP hydrogel is almost invariant as the strain increases from 0.1 to 10 %, showing the resilience of the SUP network toward the mechanical defor-

Figure 2. Rheology of SUP hydrogels. (A) Frequency sweep test on a 72 hour-cured SUP hydrogel at room temperature. The hydrogel was prepared by adding 4-arm PEG-maleimide (PEGMAL4) (5 wt %) to the ELP-SUP-ELP (E-SUP-E) protein solution (10 wt %) in PBS (pH 8.0) at a 1:2 molar ratio. The shear strain amplitude was set at 5%. The frequency varied from 100 to 1 rad/sec. (B) Strain sweep test on a 72 h-cured SUP hydrogel at room temperature. The shear frequency was set at 10 rad/sec. The strain amplitude varied from 0.1 to 100%. mation given. For an ideal covalent network resulting from the 2


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reaction of E-SUP-E + PEG-MAL4 with 100 % crosslinking efficiency, the molecular weight, Mc, between crosslinks is around 30 kDa based on the equation Mc = (MPEG + 2MSUP) / 2. Assuming that this ideal SUP network deforms in an affine manner,30,31 a theoretical storage modulus for this SUP network (~8.0 kPa) at room temperature (298 K) can further be deduced according to the equation G = ρRT/Mc, where ρ, the polymer density of the SUP hydrogel, is 0.096 g/ml. The measured storage modulus is only 1.6 kPa, much lower than the predicted value, ~8.0 kPa. The discrepancy between the measured and theoretical storage moduli may arise from significant non-affine deformation of the hydrogel as well as network defects, such as elastically ineffective loops and incomplete thiol-maleimide crosslinking. A major concern for protein materials is whether the protein molecules can retain their function after immobilization. To examine the function of the immobilized SUP proteins within the hydrogel network, we performed an Arsenazo III-based uranyl binding assay,25 in which an ELP-based Spy network hydrogel containing no SUP served as a negative control.32 It turned out that a tiny piece of SUP hydrogel (5 µl, 10 wt %) sequestered up to 90 % of uranyl ions from 1 ml of the uranyl solution (18 µM in H2O), substantially higher than the Spy network hydrogel (5 µl, 10 wt %) did under the same condition (Figure S6), confirming that the immobilized proteins remain functional within the SUP hydrogel network. Given the enormous sample volume in uranyl extraction from the ocean, simplicity and efficiency are deemed essential for prac-

creased surface area, facile separation by centrifugation or filtration, quantitative assessment in laboratory-scale studies, and flexibility in commercial packaging. In order to prepare monodisperse SUP microbeads, we adopted a concise droplet-generating microfluidic device, which has a Yshaped microfluidic channel with a width of 300 µm and depth of 100 µm and two immiscible phases - an oil phase consisting of mineral oil and two surfactants (3 % EM 90 and 0.05 % triton-X 100) as a carrier flow and an aqueous phase comprised of the ESUP-E + PEG-MAL4 gelation solution at a 2:1 molar ratio (see Materials and Methods in the Supporting Information). It turned out that slow gelation of E-SUP-E + PEG-MAL4 (Figure S5) allows sufficient time to process the aqueous samples in the microfluidic system (Figure 3A). By setting the flow rates at 10 and 21 µl/min for the aqueous and oil phase, respectively, monodispersed droplets were generated spontaneously upon injecting the gelation solution into the oil flow (Figure 3A).33 The resulting SUP droplets were first collected in a petri-dish at room temperature. After further curing at room temperature for 72 h, solid hydrogel microbeads formed. The resulting beads showed a uniform radius of 165.4 ± 3.0 µm in one of the batches, corresponding to a volume of 19 ± 0.1 nl/ bead (Figure 3B). These microbeads turned out to be stable and remained intact after washing with a large volume of H2O (Figure 3B). Such mechanical stability is important for flexible downstream operations such as stirring and centrifugation as well as a precise assessment for the performance of the materials.

Figure 3. Fabrication of protein hydrogel microbeads through a microfluidic device. (A) Schematic illustration of a Y-shaped microfluidic channel 300 µm in width and 100 µm in depth, respectively, generating the SUP microbeads. The carrier flow (yellow) contains mineral oil and two surfactants (3% EM90 and 0.05% triton-X 100). The aqueous phase (green) comprises the mixture of E-SUP-E + PEG-MAL4 at a 2:1 molar ratio. (B) Photographs of the microbeads in mineral oil (left) and water (right). The mean radius of the beads is 165.4 ± 3.0 µm. (C) Time-dependent uranyl sequestration by different amounts of the microbeads from 1 ml of Milli-Q water spiked with 10 µM uranyl nitrate. Theoretical capacities of these beads deduced from the 1:1 binding stoichiometry of SUP toward uranyl are indicated by dashed lines (right). (D) Concentration-dependent uranyl sequestration by the microbeads. The initial concentrations of uranyl nitrate in Milli-Q water (1 ml) varied from 1 to 20 µM. Theoretical sequestration percentage for these experiments are shown as dashed bars. Data are presented as mean ± SD (n = 3). tical uranyl adsorbents. We envisioned that fabrication of the SUP hydrogels into monodisperse beads would confer several advantages such as faster binding kinetics resulting from the in-

A single SUP microbead (~10 wt %) with a radius of ~165.4 µm contains approximately 64 pmol of the SUP protein, which corresponds to a theoretical capacity of 64 pmol of UO22+ per 3



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bead, assuming a 1:1 stoichiometry of the uranyl binding by SUP. In other words, a complete extraction from 1 ml of 10 µM uranyl solution (i.e., 10 nmol of UO22+) requires 157 SUP microbeads theoretically. To determine the actual binding capacities and kinetics, we first tested uranyl sequestration from a simplified system – Milli-Q water 1 ml spiked with a defined amount of uranyl nitrate (10 µM) – using various numbers of SUP microbeads in a timedependent manner. Figure 3C shows a gradual increase in uranyl uptake as the number of the SUP microbeads increases from 20 to 160 and the incubation time from 5 to 60 min. Within 1 h, 160 beads sequestered up to 96 % of uranyl from the solution (Figure 3C), consistent with the theoretical estimate of 157 beads. This result also points to fast adsorption kinetics of these SUP microbeads, of which the maximum uranyl binding takes less than 1 h. We also examined the effects of uranyl concentration on the performance of the SUP microbeads (Figure 3D). In the cases where the amounts of uranyl are limited, such as the 10 µM uranyl solution (1 ml) with 160 beads (Figure 3C) or the 1 µM solution with 20 and 40 beads (Figure 3D), we observed a nearly 100% uranyl extraction. When the amounts of uranyl (5, 10, 15 and 20 µM in 1 ml of H2O) surpassed the theoretical capacities of the microbeads added, i.e., 64 pmol per bead × number of beads, these microbeads exhibited a uranyl binding capacity (~100 pmol/bead) that exceeds their theoretical maximum (64 pmol/bead), which corresponds to a molar ratio of UO22+: SUP, 1.5:1, instead of 1:1. This enlarged capacity could be attributed to

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dimeric interface25 or nonspecific binding by certain aspartate or glutamate residues within the protein network. Excess of divalent cations such as Ca2+ and Mg2+ and anions such as CO32- in seawater often tampers the efficiency of uranyl absorbents due to competition effects. To test their potential for practical applications, we investigated uranyl sequestration by the SUP microbeads from natural seawater from Port Shelter, Hong Kong. With sufficient microbeads, the extraction was performed by adding excess of SUP microbeads (molar ratio of SUP : UO22+, 10:1) into the seawater sample (0.8 l) spiked with 13.7 nM uranyl. Seawater without any spiking was used as a control. According to the inductively coupled plasma mass spectrometry (ICPMS) analysis, uranyl can be enriched up to ~34 µmol (or 9.2 mg) per kilogram of the dry adsorbent from the spiked seawater, which corresponds to an enrichment index, K = [UO22+ (gel)] / [UO22+ (aq)], of 2.5 × 103. Figure S7 shows concentrations of uranyl and other major metal ions in the seawater sample determined by ICPMS. Substantially smaller enrichment indices were observed for other major metal ions (Na, Mg, Ca, K and Sr) in seawater, suggesting that uranyl sequestration by these beads is selective (Figure 4A). The apparent selectivity of the SUP microbeads toward uranyl over these metal ions in seawater was also calculated (Figure 4B). Due to the extraordinary complexity of the natural seawater sample, the selectivity of these beads toward uranyl in seawater appears lower than that of the SUP protein which was previously measured in simple buffered solutions containing only uranyl and the other metal ion of interest.25 Nevertheless, these results together demonstrate the feasibility of uranium mining

Figure 4. ICP-MS analysis of uranyl extraction from seawater by SUP hydrogel microbeads. Seawater spiked with 13.7 nM uranyl nitrate was used. The microbeads were incubated with 0.8 l of seawater at room temperature for 1 h before ICP-MS analysis. (A) Enrichment index, K = [M (gel)] / [M (aq)]. (B) Selectivity = K (uranyl)/ K (M). a secondary uranyl binding site possessed by SUP at the protein

from the ocean with these protein materials. 4


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In summary, we have developed super uranyl-binding proteinbased hydrogel microbeads through a combination of thiolmaleimide click chemistry and microfluidic technologies. The resulting materials retained the function of the immobilized proteins and showed remarkable efficiency in sequestering uranyl from seawater. This protein-based uranyl extraction system can readily be improved through judicious protein engineering and material design. Given their efficiency, robustness and evolvability, our protein hydrogel microbeads represent promising alternatives to existing uranyl adsorbents.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Materials and Methods and Figures S1-S8 (PDF).

AUTHOR INFORMATION Corresponding Author *[email protected]

Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT Fei Sun thanks the funding support from the Research Grants Council of Hong Kong SAR Government (Grants 26103915 and AoE/M-09/12). Fei Sun and Songzi Kou are grateful to the Department of Chemical and Biomolecular Engineering, HKUST for the faculty startup fund.

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Title: Protein Hydrogel Microbeads for Selective Uranium Mining from Seawater


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Protein Hydrogel Microbeads for Selective Uranium Mining from

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