Repeated and Folded DNA Sequences and Their Modular Ag10

Article Cite This: J. Phys. Chem. C 2018, 122, 4670−4680

pubs.acs.org/JPCC

Repeated and Folded DNA Sequences and Their Modular Ag106+ Cluster Jeffrey T. Petty,*,† Mainak Ganguly,† Ian J. Rankine,† Elizabeth J. Baucum,† Martin J. Gillan,† Lindsay E. Eddy,† J. Christian Léon,‡ and Jens Müller‡ †

Department of Chemistry, Furman University, Greenville, South Carolina 29613, United States Westfälische Wilhelms-Universität Münster, Institut für Anorganische und Analytische Chemie, Corrensstraße 28/30, 48149 Münster, Germany

‡

S Supporting Information *

ABSTRACT: Molecular silver clusters are optical chromophores, and species with distinct spectra form with DNA strands. One such hybrid chromophore is a violet cluster bound to repeated C2X sequences where X ≠ C. We varied the number of C2X repeats and the X nucleobase and consider three observations. First, different lengths of (C2A)y and (C2T)y strands with y = 3−12 identify a minimal (C2X)6 scaffold that forms a specific Ag10 adduct. This cluster has a +6 oxidation state, absorbs between 400−450 nm, and folds its DNA host. Second, different X nucleobases alter the (C2X)6 binding site. The natural nucleobases preferentially form the Ag106+ cluster and yield strong circular dichroism. These ligands coordinate via their heteroatoms, and the N3 of thymine was identified via cluster fluorescence that varies with pH. In contrast, abasic sites and imidazole substitutions suppress circular dichroism and diminish the number of silver adducts. These observations suggest that a (C2X)6 coordinates Ag106+ via multiple nucleobases. Third, beyond the minimal (C2X)6 binding site, longer strands still form Ag106+ but can also coordinate additional Ag+ adducts. The added Ag+ do not perturb the Ag0 and their spectra and thus may partition to open C2X subunits outside the core (C2X)6−Ag106+ complex. Thus, these modular complexes distinguish oxidized and reduced silvers. Collectively, these three observations suggest that the DNA and silver cluster play complementary roles: a repeated C2X sequence stabilizes the Ag106+ cluster, while the cluster folds its host. We specifically suggest that the Ag+ within Ag106+ cross-links remote C2X subunits and the Ag0 coordinate with mismatch sites in a hairpin-like secondary structure. Distinct roles for Ag+ and Ag0 within a cluster are considered in light of the X-ray spectra of related complexes.

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fluorescence quantum yields as large as ∼90%.32−34 Furthermore, cluster emission jumps via sequential two-photon excitation.35−37 Third, they can be structurally switched. When single- and double-stranded forms of DNA interconvert, the cluster adducts are driven between dark and bright states with up to 500-fold changes in fluorescence.38−40 Fourth, they are flexible. DNA strands wrap and assemble around silver clusters and thereby protect their reactive metallic cargo against precipitation and degradation.38,40−45 Reaction conditions and time impact the cluster formation, and the primary sequence and the secondary structure of a DNA scaffold encode the cluster color and photophysics.25,32,38,46−50 However, this relationship is still empirical. To better understand these hybrid DNA−silver chromophores, we are motivated by one of their key characteristics: a polymeric DNA anchors a silver cluster via its nucleobases. We hypothesize that its sequence and structure organize the nucleobase ligands and thereby favor a cluster with specific spectra.23,25,32,46,49,51−54 We focus on repeated DNA sequences because they limit the types and numbers of nucleobases and may thus delineate key characteristics of cluster binding sites within a DNA. Furthermore, these

INTRODUCTION Noble metal clusters with ∼10 atoms are optical chromophores that are more similar to organic dyes than to the bulk metal or nanoparticles.1−3 Specifically, silver clusters have sparse manifolds of valence electronic states with rich spectra and distinct photophysics.4 These chromophores absorb across the optical region with spectra that are prescribed by cluster size, charge, and shape.5−10 Molecular noble metals were discovered in gaseous and cryogenic matrix environments but can be synthesized in solution when they are guarded against agglomeration and degradation.11−14 For example, nascent clusters develop when oxidized metals are chemically reduced and then captured by thiols and phosphines that coordinate the cluster surface.12,13,15−21 Furthermore, such ligands control the stoichiometries, charges, and atomic and electronic structures of their embedded clusters.16,22−24 Molecular silver clusters can also be trapped by DNA strands, and these oligomers offer several advantages as ligands.25−27 First, they are monodisperse. Strands with precise lengths between 10−30 nucleotides locally concentrate specific numbers of silvers and thus constrain the cluster sizes.25,28−31 Second, they can be programmed. Strand sequence and structure encode the cluster color and brightness, and these chromophores absorb across the ultraviolet to near-infrared with extinction coefficients of ∼105 M−1cm−1 and with © 2018 American Chemical Society

Received: December 18, 2017 Revised: February 14, 2018 Published: February 14, 2018 4670

DOI: 10.1021/acs.jpcc.7b12351 J. Phys. Chem. C 2018, 122, 4670−4680

Article

The Journal of Physical Chemistry C

measurements of the separated species were made using the SPD-M20A and RF-10XL, respectively. For the thymine oligonucleotides dT10, dT15, dT20, and dT30, the averages and standard deviations of the retention times were linearly correlated to the hydrodynamic radii, from which the radii of the cluster conjugates were determined using standard error propagation methods. Continuous variation analysis was conducted by removing DNA from the solution and replacing it with an equivalent amount of Ag+.59 The total concentration of Ag+ and C2A was constant at 36 μM, which is >100-fold larger than the dissociation constant of ∼2 × 10−7 M for Ag+ with DNA.41 The ellipticities at 260 nm were plotted as a function of the mole fraction of DNA to determine the complex stoichiometry. Mass spectra were collected using Q-TOF G2-S (Waters) and analyzed with MassLynx V4.1, as described previously.41,45,56 We used the negative mode because the phosphate backbone of a DNA strand is ionized at neutral pH and thus makes the overall complex anionic.60,61 Excision. Uracil DNA Glycosylase (UDG) was obtained from New England BioLabs (M0280S) and stored at −20 °C in 10 mM Tris-HCl, 50 mM KCl, 1 mM DTT, 0.1 mM EDTA, 0.1 mg/mL BSA, and 50% Glycerol, pH 7.4. The reaction used 15 μL of 1 mM oligonucleotide, 7.5 μL of enzyme (3.5 units), and 5 μL of 10× reaction buffer (from supplier but without DTT) in a total volume of 50 μL. Slow pipetting mixed the solution to prevent enzyme denaturation. The resulting solution was incubated at 37 °C for ∼12 h and subsequently dialyzed against water to remove the reaction buffer. The resulting samples were sufficiently purified for mass spectral analysis and silver nanocluster synthesis. The extinction coefficient for the resulting stand was calculated by the nearest-neighbor method after accounting for the excised nucleobases.

templates yield spectrally diverse chromophores and thus control the electronic structure of their molecular silver adducts. For example, C4X-based strands produce fluorescent silver clusters with blue absorption and green emission that is strongest with X = adenine and thymine.55 The contiguous cytosines elongate this cluster, and this shape contrasts with the compact structure of its dim counterpart.56 C3X sequences form far-red/near-infrared chromophores, and the X nucleobases control both the cluster spectra and photophysics.29,30,33,42,47,57 In this paper, we focus on oligomeric C2X templates that form a molecular silver chromophore with violet spectra. The binding site for this cluster depends on the number and sequence of the C2X subunits, and we consider three questions. First, what is the minimal number of repeats for this cluster? Two sets of oligonucleotides with 3−12 C2X repeats vary the length of the DNA template, and systematic changes in the cluster binding sites are signaled by the optical and mass spectra. Size exclusion chromatography shows that not only DNA length but also shape favor this adduct. Second, which nucleobases bind the cluster? The X nucleobases were modified and eliminated, and corresponding changes in the binding sites were signaled by the electronic and mass spectra of the cluster moieties. Third, what is the role of ancillary repeats? The minimal sequence for the violet cluster was extended, and their Ag106+ complexes were reacted with Ag+. Mass spectrometry determined both the stoichiometry and oxidation states of these higher order complexes. From these observations, we suggest that the DNA and cluster mutually contribute to the overall structure of the complex. The polymeric DNA establishes the binding site through its length and sequence, and the cluster molds this flexible scaffold through silver-nucleobase crosslinks. We consider these interactions in light a segregated structure that was deduced from the X-ray absorption spectra of related complexes.

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RESULTS Our experiments were guided by two characteristics of DNAbound silver clusters. First, these clusters are molecules with ∼10 atoms. They bind with single DNA strands, and these complexes are preserved by electrospray ionization mass spectrometry.34,61,62 During negative electrospray, the phosphate backbone binds varying numbers of H+, and the net masses of these monodisperse oligonucleotide ions give the cluster stoichiometries. Furthermore, the numbers of phosphate-bound H+ diminish in proportion to the charge of the cationic cluster, and the indirectly derived oxidation states agree with those measured by near-edge X-ray absorption spectra.45 The mass spectra yield the empirical silver stoichiometries, and we refer to the resulting complexes as molecular clusters for two reasons. The silvers are in close proximity because they are bound to a DNA strand with a hydrodynamic radius of ∼1 nm.41 Furthermore, extended X-ray absorption fine structure studies identify a network of silver−silver bonds within these complexes. For example, Ag106+ adducts with both single- and double-stranded DNA hosts yield scattering paths that are attributed to bonding between reduced and oxidized silvers.45,56 However, it is important to acknowledge that the DNA host could form strong bonds with their silver adducts and ultimately alter the cluster structure, as seen for gold clusters with different thiol ligands.63 Second, molecular silver clusters have sparse electronic states. In this study, the chromophores not only absorb in the 400−450 nm region but also exhibit circular dichroism, possibly due to their chiral DNA hosts.64 The inherent circular dichroism changes with the DNA-cluster

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EXPERIMENTAL SECTION Synthesis. Commercial oligonucleotides from Integrated DNA Technologies were purified by desalting by the manufacturer and dissolved in deionized water. The resulting DNA concentrations were determined from the molar absorptivities based on the nearest-neighbor approximation. The imidazole strands were synthesized as reported previously and characterized by mass spectrometry ((C2IC2T)3: calcd for [M + H]+: 5059 Da, found: 5058 Da; (C2mIC2T)3: calcd for [M + H]+: 5101 Da, found: 5099 Da).58 These oligonucleotides formed the silver clusters via the following procedure. First, the DNA strands were combined with Ag+ at a 1:8 relative ratio, respectively, with a DNA concentration of 30 μM in either water or a 20 mM ammonium acetate buffer at pH 7. An aqueous solution of BH4− was added to give a final concentration of 4 BH4−:oligonucleotide, and the resulting solution was vigorously shaken for 1 min. The samples were then place in a high-pressure reactor from Parr with 400 psi O2 for ∼3 h to favor the Ag106+ cluster.47 Characterization. Absorption spectra were acquired on a Cary 50 from Varian, and emission spectra were acquired on a Fluoromax-3 from Jobin-Yvon Horiba. Size exclusion chromatography used a 300 mm, 7.8 mm inner diameter (id) column (BioSep, Phenomenex) on a high performance liquid chromatography (HPLC) system (Prominence, Shimadzu) using a 10 mM citrate buffer at pH 7 with 40 mM NaClO4 to minimize matrix adsorption. Absorbance and fluorescence 4671


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Figure 1. Absorption (A), circular dichroism (B), and fluorescence (C) spectra (with λex = 440 nm) of (C2A)4 (dotted blue), (C2A)5 (solid green), (C2A)6 (solid black), (C2A)7 (solid red), and (C2A)8 (solid blue) oligonucleotides with silver clusters. Arrows indicate a progressively favored environment for violet cluster as DNA length increases. (D) Mass spectra of (C2A)4−7 oligonucleotides with silver clusters following the color scheme for panels A−C. The (C2A)6 strand is emphasized because it establishes a threshold that favors a Ag10 cluster with λ ∼ 440 nm in the absorption and circular dichroism spectra and λ ∼ 535 nm in the emission spectrum.

coordination and was derived from the anisotropy g = ΔA/A, where ΔA is the difference in the absorption of left vs right circularly polarized light, and A is the ordinary absorbance.65,66 Fluorescence also characterizes DNA binding sites that change with sequence and pH. Using these experimental techniques, we now discuss how the number of C2X repeats and the X nucleobase develop a particular silver-based chromophore. Minimal DNA Length Develops Ag106+. The number of C2X repeats dictates the cluster environment, as shown by the X = adenine derivatives. (C2A)y sequences with y = 3 and 4 bind 5−6 silver and yield cluster chromophores with broad and diffuse absorptions, low ellipticities, and weak emission (Figures 1 and S1). Thus, these optical and mass spectra suggest that shorter strands suppress cluster formation and thus are poor cluster scaffolds. In contrast, strands with y = 5, 6, and 7 improve the environment and ultimately develop a specific cluster (Figure 1). (C2A)5 preferentially binds higher numbers of 6−8 silvers, while (C2A)6 and (C2A)7 preferentially produce

a 10 silver adduct with single absorption, excitation, and emission bands (Figures 1A and C and S2A).45,47 The emission spectra with excitation spanning 300−600 nm overlap with λmax,en = 535 nm, and this correspondence suggests that a single chromophore develops in a favored binding site (Figure S2B). Furthermore, these spectra match those of the clusters with (C2A)4 and (C2A)5 and thus suggest that the same cluster forms with all the strands. We subsequently suggest that the larger Ag10 cluster harbors smaller subsets of chromophoric silvers (Figures S2C and D). Additionally, the longer (C2A)5, (C2A)6, and (C2A)7 strands progressively strengthen the inherent circular dichroism with respective anisotropies of 0.7, 0.9, and 1.1 × 10−3 (Figure 1B). Similar values for other silver and gold cluster complexes with chiral ligands support a favorable interaction between the cluster and C2A repeats.67,68 A circular dichroism transition at 315 nm is masked in the absorption spectrum, but its ellipticity tracks the changes in its neighboring peak. So, we suggest that these two electronic 4672


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Figure 2. Absorption (A) and circular dichroism (B) spectra of (C2T)4 (dotted blue), (C2T)5 (solid green), (C2T)6 (solid black), (C2T)7 (solid red), and (C2T)8 (solid blue) oligonucleotides with silver clusters. (C) Mass spectra of (C2T)4−7 oligonucleotides with silver clusters following the color scheme for panels A and B. The (C2T)6 strand is emphasized because it establishes a threshold length that favors a Ag106+.

stranded thymine oligonucleotides.69−72 These references adopt random coil shapes and show that the native 18nucleotide (C2A)6 elutes as a dT17±3 and thus has no innate secondary structure. In contrast, its cluster-laden counterpart elutes as a smaller dT12±2 oligonucleotide, so the cluster adduct contracts its host, possibly via metal-mediated cross-links.73 Second, besides DNA shape, sequence also controls the cluster binding site (Figure S4). Relative to (CCA)6, the permuted (CAC)6 strand shifts the spectrum and quenches the emission. To further probe the preferred sequence for the violet cluster, (CAC)6 was appended with a 5′ terminal C to yield C(CAC)6. However, this sequence can be rewritten as (CCA)6C, and this modification recovers the favored (C2A)6 sequence and the associated strong violet absorption. Relative to the core (C2A)6 scaffold, the appended (C2A)6C yields a cluster with λmax that is more similar to the spectra with (C2A)y with y ≥ 7 (Figures 1A and S1A). This suggests that (C2A)6 is a minimal scaffold for the Ag106+ cluster and that additional nucleobases optimize the binding site and electronic environment of this cluster. Third, the cluster oxidation state was deduced from the mass spectra

transitions arise from the same Ag10 species. Longer (C2A)y strands with y = 8, 10, and 12 still favor Ag10 with the same spectra and strong anisotropies g ∼ 1 × 10−3, but two observations signal changes in the cluster environments. First, longer strands diminish the cluster absorbance, ellipticity, and emission in relation to their (C2A)6 and (C2A)7 counterparts (Figures 1A and B and S1A and B). Second, these strands bind not only 10 but also 6 silvers. These two observations suggest that the longer strands harbor a (C2 A) 6 subset that preferentially develops Ag10 and that the extraneous C2A repeats form competing clusters. We subsequently discuss these additional repeats as Ag+ binding sites. The (C2A)6 strand is a minimal sequence for a Ag10 chromophore with violet absorption and circular dichroism and green emission, and we further studied three characteristics of this complex: its global structure, DNA sequence, and cluster charge. First, the overall structure is dominated by the relatively larger DNA host and was studied by size exclusion chromatography (Figure S3). Shifts in elution times reflect changes in DNA shape that were interpreted using single4673


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Figure 3. Absorption (A) and circular dichroism (B) spectra of (C2DC2T)3 (black), (C2IC2T)3 (red), (C2mIC2T)3 (blue), and (C2G)6 (green) oligonucleotides with silver clusters. (C) Mass spectra of (C2T)4−7 oligonucleotides with silver clusters following the color scheme for panels A and B. The first three strands are distinguished because they produce smaller Ag6 and the larger Ag10 clusters and have weak circular dichroism spectra.

strands are poor cluster templates. Like its adenine analog, (C2T)6 marks a transition: it preferentially develops Ag106+ with a sharp absorption band at λ ∼ 420 nm and strong anisotropy g ∼ 1 × 10−3 (highlighted spectra in Figure 2). The longer oligonucleotides (C2T)y with y = 7, 8, 10, and 12 more fully develop the Ag106+ binding site, as signaled by absorption and circular dichroism peaks that sharpen at 405 nm and with g = 0.4−0.6 × 10−3. The y = 10 and 12 strands also develop a transition at ∼510 nm, and we are investigating this new transition. In summary, both sets of (C2A)y and (C2T)y oligonucleotides reveal a break in the cluster environment: strands with ≳6 repeats develop Ag106+ clusters with sharp and strong absorption and circular dichroism bands. Multiple Nucleobases Coordinate Ag106+. DNA strands stabilize molecular silver clusters via their nucleobases, and we considered the types and sequences of the nucleobase ligands in a range of other (C2X)6 hosts. Cytosines coordinate the cluster, as indicated by a permuted sequence that alters the cluster environment (Figure S4). The X nucleobases also complex the cluster, as suggested by (C2X)6 sequences with X = A, T, and G that produce Ag106+ clusters with distinct spectra (Figures 1−3). The X nucleobases were also deprotonated, eliminated, and substituted to further interrogate the cluster binding site. Natural nucleobases stabilize silver clusters via one or more of their heteroatoms, and we investigated the acidic N3 site in thymine.53,54 This heteroatom within (C2T)6 was selectively

(Figure S5). A DNA-cluster ion has different isotopologues due to its natural isotope abundances, and these distributions are dominated by silver with 51.8% 107Ag and 42.8% 109Ag. The masses and intensities of these envelopes can be modeled using the molecular formulas. For example, C168H205O100N66P17Ag10−6 predicts the masses and intensities for the set of peaks at m/z ∼ 1059. In contrast with the formula C168H211O100N66P17−6 for the native (C2A)6, the DNA-cluster complex has 6 fewer H+, so this difference suggests that a + 6 charged cluster drives off 6 additional H+ from the phosphate backbone. The same comparison of the ligated and native DNA strands for the −4, −5, and −7 charge states yields the same +6 oxidation state for the cluster. (C2T)y oligonucleotides mirror their adenine counterparts and reveal a similar threshold for Ag106+ (Figures 2 and S6). The shorter strands weakly bind silver. (C2T)3 yields chromophores with a broad, structure-less absorption at λmax ∼ 450 nm and with multiple circular dichroism transitions between 300 and 600 nm, and the isolated oligonucleotide dominates the mass spectrum. These observations indicate a weak oligonucleotide-cluster affinity, so larger nanoparticles may develop with DNA-induced circular dichroism.74 (C2T)4 and (C2T)5 are similarly poor templates. (C2T)4 binds no silvers, (C2T)5 favors the Ag6 species, and both cluster complexes absorb with multiple transitions between 350−550 nm but no observable circular dichroism. Thus, these shorter 4674


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Figure 4. (A) Mass spectra of the −6 charge state of the (C2A)6−Ag106+ cluster without and with 4 added equivalents of Ag+:(C2A)6 followed by 100-fold dilution and dialysis. The star marks the expected position of the Ag117+cluster. (B and C) Mass spectra of the −6 charge state of the (C2A)8−Ag106+ cluster with 0, 2, and 4 added equivalents of Ag+:(C2A)8 followed by 100-fold dilution and dialysis and the associated circular dichroism spectra. The optical spectra do not significantly change, but the mass spectra show higher order complexes (C2A)8−Ag106+, −Ag117+, −Ag128+, and −Ag139+. Thus, added Ag+ do not perturb the Ag0 chromophore. (D) Proposed hairpin-like structure with 6 C−Ag+−C base pairs and two X−X mismatches that are proposed binding sites for the two Ag2-based clusters.

deprotonated in basic solutions because its pKa ∼ 9.7 is distinct from the pKa ∼ 4.5 for the N3 of cytosine.50,54,60 Resulting changes in the cluster environment were signaled by fluorescence (Figure S7). Neutral pH yields poor emission, but more basic solutions develop stronger emission that rises sharply between pH 9.2 and 10.2, a range that brackets the pKa for the thymine N3. These fluorescence changes can be reversed: strong fluorescence at pH 10.2 quenches at pH 8.5 but recovers at pH 10.1. Collectively, these experiments suggest that the cluster and H+ compete, and the cluster binds when the thymine N3 deprotonates. The (C2T)6−cluster complex emits with λex/λem = 470/560 nm, which is distinct from the clusters with (C 2 A) 6 but similar to adducts with the homooligonucleotide dT12.54 These observations suggest that the thymines within (C2T)6 specifically bind the cluster and control its emission. This similarity between (C2T)6 and the homooligonucleotide T12 further suggests that the spectral changes

can be attributed to changes in the protonation state of the thymine. X nucleobases within (C2X)6 were also eliminated and substituted (Figure 3). Three nucleobases in alternating repeats were enzymatically excised to yield (C2DC2T)3 with the abasic sites D. Like its intact (C2X)6 relatives, this 15-nucleobase strand also yields Ag106+ with a strong, sharp absorption at 420 nm but with one key distinction: the circular dichroism anisotropy is suppressed by ∼10-fold relative to that of the (C2A)6 and (C2T)6 complexes. Furthermore, this strand also yields a competing 6 Ag adduct. Analogously, imidazole (I) and 2-methyl-imidazole (mI) were substituted into (C2IC2T)3 and (C2mIC2T)3, respectively, and these modified strands also diminish the circular dichroism and produce the alternate adduct. Thus, abasic sites and imidazole nucleobases similarly compromise the minimal (C 2 X) 6 scaffold for Ag 10 6+ . Collectively, the deprotonated thymines, the abasic sites, the 4675


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Minimal DNA Length Develops Ag106+. Only (C2X)y strands with a sufficient number of repeats produce the violet cluster. Because (C2A)y and (C2T)y follow similar paths to this cluster, we suggest that DNA length and not sequence establish the favored binding site. Shorter strands with y = 3 and 4 weakly bind silvers and yield chromophores with diffuse and unstructured absorptions, low circular dichroism, and poor emission. The y = 5 and 6 oligonucleotides progressively favor the Ag106+ chromophore with a single and sharp violet absorption. This same species develops with sequences with up to y = 12 repeats, and this plateau indicates that longer strands harbor core (C2X)6 binding sites for Ag106+. The length of this 18-nucleobase strand may favor Ag106+ in two ways. First, the oligonucleotide is a polymer, and its length sets the number of nucleobase ligands. In support, other DNA strands also form violet and chiral Ag106+ chromophores, but only when the number of nucleobases exceeds ∼18.45 Second, DNA length controls the flexibility and folding of the host strand. We focused on (C2A)6−Ag106+ that has a hydrodynamic radius ∼30% smaller than that of the native (C2A)6 and thus propose that Ag106+ intramolecularly cross-links its single-stranded and pliable DNA host. In support, prior studies establish that silver clusters do not passively bind to single-stranded DNA but reshape their host by not only folding but also assembling DNA strands.30,41,42,57 For example, silver clusters with near-infrared spectra cross-link repeated C3X strands, and these intermolecular dimers develop at concentrations as low as 300 nM oligonucleotide. Thus, these observations highlight complementary interactions within the (C2X)6−Ag106+ complex: the length of the DNA establishes the minimal binding site for the cluster, while the cluster cross-links and folds its DNA host. Multiple Nucleobases Coordinate Ag106+. DNA binds silver clusters via its nucleobases, and the interaction between Ag106+ and its (C2X)6 host was probed by altering the DNA sequence and modifying the X nucleobase. Permuted sequences suggest that the cytosine sequence sets the cluster environment because (CCA)6 yields single absorption and emission bands for its cluster, whereas (CAC)6 produces multiple and shifted absorption bands and quenches emission. The X nucleobases within a (C2X)6 also control the cluster environment, as shown by deprotonating, excising, and substituting these ligands. A single-stranded oligonucleotide anchors silver clusters via the heteroatoms in its nucleobases, and we studied the thymine N3 in (C2T)6. This acidic heteroatom deprotonates in basic solutions with pH ≳ pKa ∼ 9.7 and consequently becomes an open coordination site for a fluorescent cluster, as supported by earlier studies.50,54 The resulting spectrum matches that for a dT12-silver cluster complex, which suggests that the six thymines in (C2T)6 coordinate the cluster at high pH and thus control its emission.54 Strands with missing and alternate nucleobases further signal how the DNA coordinates the cluster. (C2DC2T)3 preserves the phosphodiester backbone and favored DNA length for the Ag106+ adduct but has three abasic sites (D) that interrupt the nucleobase sequence. The three missing nucleobases compromise the cluster environment, as indicated by a 10-fold drop in the circular dichroism relative to intact strands. Additionally, an alternate Ag6 cluster forms. The analogous strands (C2IC2T)3 and (C2mIC2T)3 with imidazoles (I) and 2-methyl-imidazoles (mI), respectively, may behave like the interrupted strand because the smaller imidazole nucleobases have only one coordination site. Furthermore, these ligands weakly stack with their neighboring nucleobases, thereby altering their conformation and possibly the cluster

imidazole substitutions, and the permuted cytosine sequence suggest that multiple nucleobases within (C2X)6 coordinate Ag106+. Longer Strands Add Ag+. Both (C2A)6 and (C2T)6 strands mark a plateau where oligonucleotides with ≳6 repeats form the same cluster chromophore. To illustrate, (C2A)8 behaves like (C2A)6 and forms Ag106+, but this longer scaffold has unsaturated sites that can acquire additional Ag+ (Figure 4). The (C2A)6 and (C2A)8 complexes with Ag106+ were first formed by reacting the native oligonucleotides with 8 Ag+:4 BH4−:oligonucleotide, and this substoichiometric amount of silver yielded only the Ag106+ cluster with a single absorption at 440 nm. The reactions were conducted in 20 mM ammonium acetate solutions because this salt enables electrospray-based mass spectrometry and the NH4+ inhibits ionic Ag+ binding by screening the phosphates.75,76 The DNA-cluster conjugates were then purified by diluting 100-fold to dissociate weakly bound silvers and dialyzing against a 2.5 kDa cutoff filter to pass these silvers as well as borohydride byproducts.77 The retained species were then combined with 2 and 4 additional equivalents of Ag+:oligonucleotide and analogously purified to dissociate and eliminate weakly bound Ag+-DNA adducts. The two complexes react differently. (C2A)6−Ag106+ binds no additional Ag+ (Figures 4A and S9). In contrast, (C2A)8−Ag106+ recruits more Ag+ to form (C2A)8−Ag117+, (C2A)8−Ag128+, and (C2A)8−Ag139+ (Figures 4B and C and Figure S8). These formulas were derived from the mass spectra and show that the new complexes only expand the number of Ag+ without perturbing the reduced silvers, as also reflected in the unchanging optical spectra. A longer C2T strand forms analogous higher-order complexes (Figure S10). The binding sites for these additional Ag+ are suggested by their stoichiometry. The (C2A)8−Ag128+ complex is most favored with higher Ag+ concentrations, and we propose that this complex has two parts: a core (C2A)6−Ag106+ with two added DNA−Ag+ complexes. The binding sites were further studied by reacting native (C2A)6 with Ag+ without a chemical reductant. This single-stranded DNA selectively binds Ag+ via its nucleobases, and its circular dichroism spectra yield the Ag+:DNA stoichiometry via continuous variation analysis (Figure S11).78−80 (C2A)6 is a polymer, so we used the concentration of C2A subunits to more clearly resolve the stoichiometry of the complex.81 Linear extrapolation from the two concentration extremes yielded an empirical stoichiometry of 1.2 ± 0.1 Ag+:C2A.80 On the basis of this stoichiometry, we suggest that the (C2A)8−cluster complex is a core (C2A)6− Ag106+ flanked by two 1:1 C2A−Ag+ adducts. Thus, the added Ag+ and chromophoric silvers partition to different parts of their oligomeric DNA host. We subsequently suggest that the Ag+ and Ag0 within a (C2X)6−Ag106+ complex also segregate through their interaction with the DNA scaffold.

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DISCUSSION

DNA oligonucleotides produce molecular silver clusters with distinct spectra, and we hypothesize that the types and organization of the nucleobase ligands define specific binding sites. We studied repeated C2X sequences that develop a Ag106+ cluster with violet spectra. These templates limit the numbers and types of nucleobases, and we comprehensively interrogated the DNA−silver coordination by varying the DNA length and sequence. Three observations suggest how the DNA host and its molecular silver adduct are organized. 4676


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cluster. This structure further suggests binding sites for the Ag0. The folded DNA has two mismatches, and three observations suggest that these opposing nucleobases coordinate the Ag0. First, abasic sites and smaller imidazole nucleobases may quench the violet circular dichroism because these modifications block or compromise DNA coordination with the chromophoric silvers. Second, different X nucleobases shift the absorption spectra and control the fluorescence spectra and intensities, thus signaling different types of X−Ag0 complexes. Third, two X−X mismatch sites could bind silver molecules with stable electronic configurations.2,11,91 A (Ag0)2-based cluster with two valence electrons has a stable electronic configuration, and the two proximal X−X sites in the proposed hairpin could coordinate two dimeric Ag0 clusters. Within the folded, condensed DNA template, these two smaller clusters could be structurally linked via intervening C−Ag+−C base pairs. Similarly small clusters such as Ag3+ have been proposed based on electronic spectra and theoretical calculations, and these species have spectra that are similar to those of the (C2X)6−Ag106+ complexes.50 A proximal arrangement of two discrete molecular clusters been previously suggested for kernel-like gold clusters and an octahedral-like silver cluster.45,92 In summary, we propose that the Ag106+ cluster binds with its (C2X)6 host via 6 C−Ag+−C base pairs and 2 X− (Ag0)2−X complexes. This model suggests that the cluster disperses within its DNA scaffold and is consistent with earlier studies.10,34,50,68,93 Theoretical studies support thread-like clusters with collective longitudinal excitations that explain how the electronic spectra of silver clusters vary with cluster size. We suggest that these extended structures develop because of the Ag+ within the clusters. Silver clusters bound to singlestranded oligonucleotides are largely oxidized, and their Ag+ could structurally anchor the DNA. These adducts have strict coordination requirements and preferentially linearly coordinate only two nucleobases, so the Ag+ within Ag106+ might require multiple nucleobase ligands within a sufficiently long DNA strand. Because many DNA-bound silver clusters are highly oxidized, Ag+-linked base pairs may provide a useful tool to structurally mold and spectrally tune DNA binding sites for chromophoric silver clusters.

circular dichroism. Imidazoles in duplex DNA strongly coordinate Ag+, but repeated C2X sequences could disrupt this coordination because their secondary structure differs.82 In summary, these modified strands suggest that most, if not all, of the 18 nucleobases in the (C2X)6 binding site coordinate and preferentially stabilize the Ag106+ cluster. Longer Strands Add Ag+. Longer C2X strands are modular because they expand the number of Ag+ adducts without disrupting the Ag0 chromophore. To illustrate, (C2A) 8−Ag106+ adds Ag+ and favors the (C2A)8−Ag128+ complex, but the two additional Ag+ adducts do not alter the Ag106+ spectrum. We propose that such higher-order complexes have two parts: a core (C2X)6 scaffold that coordinates the violet Ag106+ chromophore and unsaturated nucleobases that bind additional Ag+. Specifically, (C2A)8−Ag128+ may be decomposed as an embedded (C2A)6−Ag106+ with two ancillary C2A subunits that bind one Ag+ each, and the proposed C2A− Ag+ complexes are supported by circular dichroism studies. The exciton-coupled circular dichroism of stacked nucleobases changes when Ag+ binds, and continuous variation analysis with different concentrations of native (C2A)6 and Ag+ reveal a break at ∼1 Ag+:C2A. Thus, open trinucleotide sequences in longer scaffolds may selectively bind additional Ag+ and thereby protect and preserve the chromophoric Ag0 within the Ag106+ cluster. Furthermore, we suggest that C2X−Ag+ complexes organize Ag106+ within its minimal (C2X)6 binding site. Because the 6 C2X repeats matches the +6 cluster change, we suggest that the 6 Ag+ within the cluster partition to the DNA and separate from the reduced Ag0. This Ag+/Ag0 segregation is a significant finding of our work, and two chemically distinct forms of silver have also been distinguished via the X-ray spectra of other DNA−Ag106+ complexes.45,56 These spectra identified silver−silver bonds with lengths of ∼2.75 Å that indicate metal-like bonds, thus suggesting that the Ag0 cluster together. Additionally, silver-DNA complexes with bond lengths of 2.1−2.2 Å support segregated Ag+ complexes with the N/O heteroatoms in the nucleobases. This model is consistent with gold and silver-thiolate complexes that also separate into cation-thiol complexes with staple-like motifs around a reduced and compact metal-like core.83−85 DNAbased complexes are distinct because the covalently linked backbone organizes the types and arrangement of nucleobases, and the DNA flexibility further refines the coordination environment and ultimately the cluster shape.34,56 Summary and Structural Model. Our key observations are minimal (C2X)6 strands develop a specific silver cluster Ag106+ with violet spectra, this cluster adduct folds its DNA host, multiple nucleobases coordinate this cluster, and Ag+ and Ag0 within the cluster are chemically distinct. We suggest complementary roles for the DNA and cluster in which the minimal (C2X)6 scaffold anchors the Ag106+ cluster and the cluster folds its flexible, polymeric scaffold. We first consider the cluster cross-links and are guided by Ag+ that are anchored by cytosine mismatches.86−88 Ag+ develops specific coordination complexes with nucleobases, as exemplified by its linear coordination complexes with opposing, mismatched cytosines in canonical duplexes.50,89,90 These metal-based bonds are stronger than hydrogen-bonded pairs, so we suggest that analogous C−Ag+−C base pairs cross-link remote cytosines and create a (C2X)6 hairpin (Figure 4D). This folded (C2X)6 structure would be saturated with 6 C−Ag+−C base pairs, which agrees with the measured empirical stoichiometry of ∼1 Ag+:C2X and also matches the number of Ag+ in the Ag106+

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CONCLUSION Repeated C2X sequences and a Ag106+ cluster form a hybrid chromophore that is founded on two interactions: multiple nucleobases in the DNA strand coordinate and stabilize the cluster, while this molecular adduct cross-links and intramolecularly folds its DNA host. We propose that the cluster segregates into oxidized and reduced silvers with Ag+ that linearly coordinates distant nucleobases in the oligonucleotide host. The resulting folded structure thereby creates binding sites for the Ag0-based cluster. This segregated structure may provide a platform to better understand how the sequence and structure of a DNA scaffold can tune and harness the novel spectra and photophysics of molecular silver chromophores.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.7b12351. Electronic and mass spectra of (C2A)3, (C2A)10, and (C2A)12 strands with silver; the excitation and emission spectra of clusters with (C2A)x strands; size exclusion 4677


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chromatograms of (C2A)6 and (C2A)6−Ag106+ with thymine size standards; electronic spectra of clusters with permuted (C2A)6 sequences; isotopic analysis of the mass spectra of the −4 to −7 charge states of (C2A)6/ Ag106+; electronic and mass spectra of (C2T)3, (C2T)10, and (C2T)12 strands with silver; fluorescence spectra of (C2T)6−Ag106+ complexes at different pH values; isotopic analysis of the mass spectra of (C2A)8−Ag106+, −Ag117+, −Ag128+, and −Ag139+ complexes; electronic spectra of (C2A)6−Ag106+ before and after adding 4 equiv of Ag+; mass spectra of (C2T)10−Ag106+, −Ag117+, −Ag128+, and −Ag139+; and continuous variation analysis of the circular dichroism spectra for the (C2A)6−Ag+ reaction (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: jeff[email protected]; Phone: 864-294-2689. ORCID

Jeffrey T. Petty: 0000-0003-0149-5335 Mainak Ganguly: 0000-0002-5315-7381 Jens Müller: 0000-0003-4713-0606 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the National Science Foundation (Grant 1611451), the National Institutes of Health (Grant 1R15GM102818), and the Deutsche Forschungsgemeinschaft (GRK 2027). E.J.B. and M.J.G. were supported by fellowships from the Furman Advantage Program.

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