DNA Facilitates the Sorption of Polycyclic Aromatic Hydrocarbons on

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DNA facilitates sorption of polycyclic aromatic hydrocarbons on montmorillonites Chao Qin, Wei Zhang, Bing Yang, Xuwen Chen, Kang Xia, and Yanzheng Gao Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05174 • Publication Date (Web): 08 Feb 2018 Downloaded from http://pubs.acs.org on February 15, 2018

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Environmental Science & Technology

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DNA facilitates sorption of polycyclic aromatic hydrocarbons on montmorillonites

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Chao Qin,† Wei Zhang,‡ Bing Yang,† Xuwen Chen,† Kang Xia,§ and Yanzheng Gao†,*

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†

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Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R. China.

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‡

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Program, Michigan State University, East Lansing, Michigan 48824, United States.

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§

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United States.

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*Corresponding author: Yanzheng Gao, Address: Weigang Road 1, Nanjing 210095, China.

Institute of Organic Contaminant Control and Soil Remediation, College of Resource and

Department of Plant, Soil and Microbial Sciences, and Environmental Science and Policy

Department of Crop & Soil Environmental Sciences, Virginia Tech, Blacksburg, VA 24060,

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Tel: +86-25-84395019. E-mail: [email protected].

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TOC ART

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ABSTRACT: The sorption of polycyclic aromatic hydrocarbons (PAHs) to montmorillonites is

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largely influenced by their interactions with dissolved organic matter (DOM). However, the role

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of DOM rather than humic and fulvic acids (e.g., extracellular DNA) in the PAH sorption to soil

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clays is little known. Here we demonstrated that extracellular double-stranded salmon testes

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DNA substantially increased the sorption of phenanthrene and pyrene to Na-, Ca-, and

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Fe-modified montmorillonites. All PAH sorption isotherms fitted the linear and Freundlich

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models reasonably well (R2 = 0.918–0.999). Distribution coefficients were increased from

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0.0458–0.103 and 0.0493–0.141 L/g at 0 mg/L DNA to 0.413–0.589 and 0.385–0.560 L/g at 10

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mg/L DNA for phenanthrene and pyrene, respectively. Spectroscopic and computational

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chemistry analyses confirmed that PAHs were first inserted into DNA by binding with the

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nucleobases via van der Waals and π-π electron donor-acceptor interactions. Compared to PAHs,

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the DNA-PAH complex can be more easily sorbed to cation-modified montmorillonites by

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complexation between DNA phosphate and exchangeable cations, in addition to intercalation

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into clay interlayers. This work highlights the importance of understanding the control on

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contaminant sorption by many organic compounds that are ubiquitous in soils but not

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represented by humic and fulvic acids.

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INTRODUCTION

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Polycyclic aromatic hydrocarbons (PAHs) are important hydrophobic organic contaminants,

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due to their carcinogenic and mutagenic effects to exposed human populations.1 PAHs are

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commonly found in soils with varying concentrations (e.g., 0.45–4560 mg/kg).2, 3 Sorption of 2 ACS Paragon Plus Environment

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PAHs to soils, which is largely controlled by the content and composition of soil organic matter

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(SOM) and clay minerals,4-7 greatly influences their accumulation, transport, transformation, and

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bioavailability in the environment,8-11 and has thus been extensively investigated in the past. As

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clay minerals, particularly montmorillonite (a predominant clay type in many soils), provide

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major sorptive surfaces in soils,12, 13 their sorption affinity to PAHs has often been studied.

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Distribution coefficients between PAHs and montmorillonite were reported in the approximate

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range of 0.01–0.8 L/g, depending on clay sources and exchangeable cations.4, 14 Indeed, in

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natural soils clay surfaces are often coated with SOM15, 16 or bound with cations such as Na+,

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Ca2+, and Fe3+,17 which control the sorption of PAHs to clays via mechanisms such as

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partitioning18 and π-π electron donor-acceptor (EDA)5 interactions between PAHs and SOM, and

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cation-π interaction between bound cations and PAHs enriched with delocalized π electrons.4, 19

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It is now known that the sorption of PAHs to montmorillonite increases with increasing strength

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of cation-π interaction between PAHs and exchangeable cations (e.g., tetra-alkyl ammonium,

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Na+, Ba2+, Mg2+, Cs+, and Ag+).4, 19, 20 In contrast, while it is recognized that the PAH sorption to

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montmorillonite is significantly influenced by SOM that is either coated on the clay surface or

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dissolved in water phase,6, 7 our understanding on the role of organic matter rather than humic

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and fulvic acids extracted from soils by an alkaline (NaOH or KOH) extraction21, 22 is still very

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limited.

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Earlier studies on the interactions of PAHs with dissolved organic matter (DOM)

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predominantly used humic and fulvic acids.23-25 However, the question on whether the 3 ACS Paragon Plus Environment


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alkaline-extracted humic substances could truly represent SOM is an ongoing debate.22, 26 It is

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certain that they cannot truly represent DOM, because the extreme pH used in the alkaline

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extraction is unlikely for typical natural soils.22 DOM can include simple sugars, amino acids,

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small organic acids, as well as more complex carbohydrates (polysaccharides), peptides, proteins,

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nucleic acids, fatty acids, and large organic acids with aromatic rings at various levels.26

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Although the earlier studies using humic and fulvic acids provided valuable insight on the

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interactions of PAHs with carboxylic, phenolic, and carbonyl functional groups of DOM through

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complexation or hydrophobic binding,11 there is clearly a knowledge gap on the interactions of

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PAHs with other types of DOM, and the impact of these interactions on the PAH sorption to

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soils.

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Deoxyribonucleic acid (DNA) is one important group of organic matter in DOM that has

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been inadequately studied in this regard. Extracellular DNA released from prokaryotic and

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eukaryotic cells is abundant in soils and sediments, with reported concentration of 0.08–80 µg/g

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in soils, 0.2–44 µg/L in sea water, and 0.5–70 µg/L in freshwater.27-30 The persistence of

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extracellular DNA in soils likely results from the sorption of DNA to soil minerals (e.g., clay)

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that offers protection from enzymatic degradation.27, 30, 31 DNA is a macromolecule formed by

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repeating units of nucleotides made of nitrogenous nucleobase, sugar deoxyribose and phosphate

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group,29 and is thus enriched with sites of negative charge (i.e., phosphate groups) and

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π-electrons (i.e., nucleobases). In particular, the hydrophobic intercalating sites between adjacent

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nucleobases may allow for binding with PAHs of wide molecular sizes,32-35 and the DNA 4 ACS Paragon Plus Environment

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phosphate groups may link with cations by complexation.36-38 Therefore, the functional moieties

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such as adenine (A), thymine (T), cytosine (C), guanine (G), pentose and phosphate groups in

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DNA can result in totally different interaction mechanisms with PAHs, compared with those in

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humic and fulvic acids. The binding of PAHs with DNA, on one hand, may alter its structure and

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genetic function.39, 40 On the other hand, it may change the sorption of PAHs to soil clays

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through previously unrecognized mechanisms. However, the previous investigations mainly

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focused on the interactions in the binary PAHs-DNA,32-35 PAHs-clays,4, 14 and DNA-clays

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systems.41-43 There has been little studies on the DNA-PAHs-clays ternary systems, which is a

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critical knowledge gap in understanding the persistence of both PAHs and DNA in soils.

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Therefore, this study aimed to mechanistically explore the influence of dissolved DNA on

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the sorption of PAHs to montmorillonite. Batch sorption experiments of PAHs to Na+-, Ca2+-, or

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Fe3+-modified montmorillonite with and without dissolved DNA were performed, in

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combination with atomic force microscopy (AFM), field-emission scanning electron microscopy

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(FESEM), laser scanning confocal microscopy (LSCM), and X-ray diffraction (XRD). The

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binding sites and reaction mechanisms were further confirmed by X-ray photoelectron

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spectroscopy (XPS) and Fourier transform infrared spectroscopy (FTIR), and corroborated by

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molecular computational modeling. By investigating the role of DNA on the sorption of PAHs to

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soil clays, this study explores how contaminant sorption is impacted by natural organic matter

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not represented by humic and fulvic acids.

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MATERIALS AND METHODS 5 ACS Paragon Plus Environment


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Chemicals. Montmorillonite K10, phenanthrene (97%), and pyrene (99%) were purchased

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from Sigma-Aldrich (St. Louis, MO, USA). The montmorillonite had a specific surface area

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(SSA) of 220–270 m2/g, and a cation exchange capacity of 76.4 cmol/kg, as reported by the

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vendor. The montmorillonite also had minor fraction of cristobalite and quartz, as characterized

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by the XRD (Figure S1). Double-stranded salmon testes DNA was obtained from Shanghai

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Ruicong Scientific and Technological Co., Ltd., and has an average molar mass of 1.3 × 106 Da

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(~2000 bp) and %G-C content of 41.2%. This DNA was selected because it has previously been

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used as a model DNA to investigate the aggregation and sorption behaviors of extracellular

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DNA.36, 44, 45 Phenanthrene and pyrene stock solution were prepared in methanol at 1.0 g/L and

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further diluted to 50 mg/L by methanol prior to use. DNA stock solution of 1 g/L was prepared

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by dissolving 0.1 g DNA in 100 mL of Tris-HCl buffer solution (10 mM, pH 7.0), and stored at

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4 °C in a refrigerator before use. All solutions were prepared with ultrapure water (18.25

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MΩ·cm). Other chemicals are described in Supporting Information S1.

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Clay minerals. Montmorillonites saturated with Na+, Ca2+, or Fe3+ were prepared following

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the approach in a previous study,46 as detailed in Supporting Information S1. The original and

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modified clays were ground, passed through a 160-mesh sieve (98 µm), and labeled as MMT,

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Na-MMT, Ca-MMT, and Fe-MMT, respectively. N2-SSA, pore volume, and pore size of these

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montmorillonites were measured by the N2 gas adsorption isotherms, and are provided in Table

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S1. The measured N2-SSA ranged from 56.6 m2/g for MMT to 74.0 m2/g for Fe-MMT, much

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lower than the SSA (220–270 m2/g) specified by the vendor. This discrepancy was because N2 6 ACS Paragon Plus Environment

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could not fully penetrate into the clay interlayers,47 thus resulting in lower N2-SSA than

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calculated SSA as also observed by Hundal et al.14

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Interactions of PAHs with DNA. Microtitration was used to determine the interactions of

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PAHs with DNA nucleobases as per the approach of Kang et al.39 Briefly, 100 mg/L DNA

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solution was prepared by diluting 1 g/L stock solution with Tris-HCl (10 mM, pH 7.0), and 100

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µg/L phenanthrene or pyrene solution was obtained by diluting 50 mg/L phenanthrene or pyrene

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stock solution with ultrapure water. Then, 100 mg/L DNA solution was gradually titrated into 20

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mL of each PAH solution by a chromatographic injector at a titration volume of 50 µL, followed

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by stirring for 20 min at 160 rpm, pH 7.0, and 25 °C. The fluorescence intensity of a 2-mL

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sample in a 4-mL quartz cuvette (1-cm path length) was measured at excitation (EX) wavelength

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of 250−310 nm and emission (EM) wavelength of 300−550 nm at a wavelength resolution of 2

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nm (F96PRO, Leng Guang, China). The maximal fluorescence intensity was obtained at EX/EM

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of 271/364 nm for phenanthrene and 332/375 nm for pyrene, respectively. The peak fluorescence

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intensity was averaged from two measurements. Fluorescence quenching can occur through

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either dynamic or static quenching. Dynamic quenching occurs due to molecular collision rather

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than actual binding, whereas static quenching involves the excitation of the complex formed by

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the fluorescent molecule and the quencher at the ground state. For the dynamic quenching, the

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peak fluorescence intensity versus the quencher (here DNA) concentrations can be described by

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the Stern-Volmer equation:

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F0 F

=1+Kq τ0 Q=1+KSV [Q]

(1) 7 ACS Paragon Plus Environment


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where F0 and F are the fluorescence intensity of phenanthrene or pyrene before and after

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quenching, Kq is the bimolecular quenching rate constant, τ0 is the average lifetime of the

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fluorophore in the absence of quencher, [Q] is the concentration of the quencher, and Ksv is the

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quenching constant.

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For the static quenching, we also calculated the binding constant (KA) and the number of

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binding sites (b) via:

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Log

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=LogKA + b Log[Q]

F0 -F F

(2)

From the measured fluorescence intensities, the F0/F or Log

values were calculated

F0 -F F

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and then plotted against [Q] or Log [Q], followed to by the linear regression to estimate Kq, Ksv,

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KA, and b, respectively.

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Sorption experiments. Batch sorption experiments were conducted to explore the effect of

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DNA on the sorption of PAHs to the montmorillonites. For the DNA-free sorption experiments,

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0.05 g of Na-MMT, Ca-MMT or Fe-MMT were placed in 20-mL amber EPA vials equipped

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with Teflon-lined screw caps, followed by the addition of 20 mL Tris-HCl (10 mM, pH = 7.0).

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Then, a series of initial PAH concentrations (0–120 µg/L) were obtained by adding appropriate

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volume of 50 mg/L stock solution of phenanthrene or pyrene. After that, the vials were shaken

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vigorously at 250 r/min and 25 °C for 72 h until reaching the sorption equilibrium.14 Finally, the

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mixtures were centrifuged at 3500 r/min for 30 min, and the supernatants were collected for

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measurements of PAH concentrations by high performance liquid chromatography (HPLC) as

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described in Supporting Information S1. While typical concentrations of phenanthrene (7–9 µg/L) 8 ACS Paragon Plus Environment

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and pyrene (2–4 µg/L) in pore water of contaminated soils were located at the lower end of our

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initial concentration range,3 our highest initial concentration was still lower than that in a

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previous study by 8 folds.14 The levels of PAH initial concentrations were selected to ensure the

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accurate isotherm measurements and the coverage of possible high PAH concentrations in

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heavily contaminated soils.

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For the sorption experiments in the presence of DNA, a series of 20 mL DNA solutions of 0.5,

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1, 5, or 10 mg/L was prepared in 10 mM Tris-HCl, followed by adding appropriate volume of

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phenanthrene or pyrene stock solution (50 mg/L) to obtain the desired initial PAH concentrations

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of 0–120 µg/L. After mixing for 24 h, 0.05 g of Na-MMT, Ca-MMT or Fe-MMT were added

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into the vials, followed by shaking at 250 r/min and 25 °C for 72 h. The final mixtures were

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again centrifuged at 3500 r/min for 30 min to collect the supernatants for measuring the PAH

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concentrations by the HPLC. The sorbed PAH amount to the clays was then calculated by the

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difference in the initial and final PAH concentration in the solution. The sorption experiments

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were conducted in triplicates. In these experiments, the effect of DNA on the sorption of PAHs to

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the montmorillonites was evaluated when DNA and PAHs co-existed in the solution phase (i.e.,

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exclusively for the effect of DOM on the PAH sorption). The scenario in which DNA is coated

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on clay surfaces is also important, but was not investigated in this study.

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The sorption data were fitted to the linear and Freundlich models (Eq. 3 and 4) by the Origin

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8.5.1 software. While the Freundlich model is frequently used to fit the sorption isotherms of

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PAHs to clays,5, 14 we also employed the linear model, following the principle of parsimony in 9 ACS Paragon Plus Environment


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choosing appropriate models. The linear model is a special case of the Freundlich model, and

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allows for calculation of distribution coefficients (Kd, L/g) quantifying the sorption affinity

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between sorbents and sorbates.

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qe = K C e

(3)

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qe =KF Cne

(4)

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where qe is the amount of PAH sorbed by the clays (µg/g), Ce is the equilibrium concentrations

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of phenanthrene or pyrene (µg/L) in the solution phase, KF is the Freundlich coefficient (Ln

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µg1-n/g), and n is an empirical constant for isotherm nonlinearity.

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d

The DNA sorption experiments were also conducted to measure the amounts of DNA sorbed

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on Na-MMT, Ca-MMT, or Fe-MMT, as described in Supporting Information S1. The DNA

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sorption isotherms were fitted to the Freundlich model.

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Microscopic and spectroscopic analyses. To elucidate the mechanisms responsible for the

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effect of DNA on the sorption of PAHs to the montmorillonites, an array of microscopic and

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spectroscopic methods were used to thoroughly characterize the montmorillonites, and sorbed

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PAHs and DNA. The montmorillonite surfaces with sorbed PAHs and DNA were characterized

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by AFM, FESEM, LSCM and XRD. Furthermore, XPS and FTIR were conducted to analyze

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possible binding sites for elucidating the binding mechanisms of DNA and metal cations in the

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montmorillonites, as well as the binding mechanisms between PAHs and DNA. Detailed

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characterization procedures are provided in Supplementary Information S1.


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Model Computation. We also used computational chemistry to elucidate possible binding

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mechanisms. Detailed model computation procedure was given in Supplementary Information

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S1.

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RESULTS AND DISCUSSION

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Interactions of PAHs with DNA. Based on the Stern-Volmer plots (Figure 1a, R2 > 0.995),

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the Kq values for phenanthrene ([0.766–24.5] × 1014 L/mol/s) and pyrene ([0.469−15.0] × 1013

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L/mol/s) were much higher than typical maximal value of 2.00 × 1010 L/mol/s,48 suggesting the

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occurrence of the static quenching due to the formation of DNA-PAH complex. The estimated

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fluorescent lifetime (τ0) for phenanthrene ([0.400−12.9] × 10−8 s) and pyrene ([0.400−12.8] ×

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10−8 s) fell in the typical τ0 range for the PAH-organic matter chromophores, i.e., (0.400–12.8) ×

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10−8 s.49-51 The greater Ksv value for phenanthrene (9.91 × 106 L/mol) than that for pyrene (6.00 ×

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105 L/mol) indicates that the 3-ring phenanthrene was more prone to the fluorescence quenching

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by DNA than the 4-ring pyrene, probably due to greater steric hindrance for pyrene that limited

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its insertion into the DNA double helix structure. Figure 1b further demonstrated the static

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quenching for phenanthrene and pyrene by DNA (R2 > 0.999). The binding strength (Log KA) of

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phenanthrene to DNA (8.3 L/mol) was greater than that of pyrene (5.3 L/mol), which agreed with

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our previous results,35 but was opposite to the findings of another study on the interactions of

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pyrene and phenanthrene crystals with calf-thymus DNA.52 We speculate that the high pyrene

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concentration at the pyrene and DNA interface in that study might contribute to the higher

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pyrene binding by overwhelming any steric hindrance associated with pyrene. The b values 11 ACS Paragon Plus Environment


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estimated for phenanthrene (1.19) and pyrene (0.933) were very close to 1, suggesting that one

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molecule of phenanthrene or pyrene probably binds to one binding site in the double-stranded

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chromosomal DNA.53 This was also observed in our previous study on the PAH binding with

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double-stranded plasmid DNA,35 suggesting similar interactions of PAHs with both

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chromosomal and plasmid DNAs.

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It is well known that PAHs can bind with DNA nucleobases and thus form complexes with

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DNA through van der Waals interaction, hydrogen bonding, and π-π EDA interactions.5, 32, 33 The

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PAH-DNA interactions were also revealed by the highest occupied molecular orbitals (HOMO)

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and the lowest unoccupied molecular orbitals (LUMO) between the bases (adenine, thymine,

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cytosine, guanine) and phenanthrene (Figure 1c) or pyrene (Figure 1d). As the positive and

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negative phases of electronic wave function were found for the interactions of cytosine and

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guanine with phenanthrene (Figure 1c), the probable binding sites of DNA for phenanthrene

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should be located on cytosine and guanine. Similarly, the possible binding sites of DNA for

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pyrene should be located on adenine, thymine and guanine (Figure 1d). Furthermore, due to their

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largest positive potentials, guanine and cytosine are most likely the binding sites (Figure 1c and

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d). In contrast to the preference to GC bases for unsubstituted PAHs such as phenanthrene and

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pyrene, the intercalation of substituted PAHs to DNA is strongly influenced by function groups

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attached to the aromatic rings, due to their steric hindrance, electrostatic interaction, or hydrogen

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bonding with DNA moieties.32, 33 For example, piperazinecarbonyloxyethyl- and

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piperazinecarbonyloxy-2-propyl-substituted anthracene and pyrene showed a preferential 12 ACS Paragon Plus Environment

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intercalative binding to AT over GC, due to the steric hindrance between the piperazinium tail

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and the exocyclic amino groups of guanine in the GC minor groove.32 However, the binding of

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hydroxylated PAHs to DNA had no selectivity with base pairs, likely due to strong hydrogen

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bonding occurring for both AT and GC pairs.34

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Sorption of PAHs by montmorillonites. The sorption isotherms of phenanthrene and

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pyrene to the montmorillonites in the absence of DNA are presented in Figure S2. The sorption

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of phenanthrene and pyrene to the montmorillonites could be best fitted with the linear model

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(Figure S2 and Table 1), supported by the excellent linearity in the sorption isotherms of

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phenanthrene to Na-, K-, and Ca-saturated reference Wyoming, Panther Creek, White, and Cheto

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montmorillonites in a previous study (Freundlich n = 0.82–1.18).14 The sorption of phenanthrene

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and pyrene to the montmorillonites increased in the order of Na-MMT < Ca-MMT < Fe-MMT,

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with their Kd values ranging from 0.0458 L/g and 0.0493 L/g for Na-MMT to 0.103 L/g and

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0.141 L/g for Fe-MMT, respectively (Table 1). These values were within the typical range of Kd

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values (0.01–0.8 L/g) for PAH sorption to cation-saturated montmorillonites.4, 14 Additionally,

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the modification by cations appeared to cause the swelling of the montmorillonite, and the

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montmorillonite layers appeared more wrinkled and open (Figure S3). Thus, Ca-MMT and

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Fe-MMT had larger interlamellar spacing than Na-MMT (Figure S4), and the pore volume

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increased in the order of Na-MMT < Ca-MMT < Fe-MMT (Table S1). The greater interlamellar

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spacing and pore volume could lead to greater accessibility of the interlayer space to the PAH

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molecules, which may be partly responsible for the above PAH sorption trend. As the cation-π 13 ACS Paragon Plus Environment


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bonding is less favorable for hard cations (such as Na+, Mg2+, Ca2+, Al3+) than intermediate (e.g.,

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Fe2+, Fe3+, Zn2+, Cu2+, and Pb2+) and soft (e.g., Ag+ and Cd2+) cations,14, 54 it may also contribute

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to the higher PAH sorption to Fe-MMT. Indeed, the presence of softer Pb2+ and Cd2+ enhanced

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the phenanthrene adsorption to clays.55

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DNA-enhanced sorption of PAHs by montmorillonites. The sorption of phenanthrene and

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pyrene to Na-MMT, Ca-MMT, and Fe-MMT increased with increasing DNA concentrations

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(Figure S5). The isotherms could be well fitted with the linear and Freundlich models (R2 =

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0.918–0.999, Table 1 and Table S2). With the addition of DNA, the Kd value of phenanthrene

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was increased from 0.0458 to 0.465 L/g for Na-MMT, from 0.0985 to 0.413 L/g for Ca-MMT,

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and from 0.103 to 0.589 L/g for Fe-MMT (Table 1). Similarly, the Kd value of pyrene was

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increased from 0.00493 to 0.385 L/g for Na-MMT, from 0.0919 to 0.432 L/g for Ca-MMT, and

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from 0.141 to 0.560 L/g for Fe-MMT. Interestingly, the Freundlich n values for phenanthrene

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and pyrene decreased with increasing DNA concentrations (Table S2), suggesting lower linearity

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of the isotherms. The n values of phenanthrene on Na-MMT ranged from 0.915 to 0.986 that are

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very close to 1,5, 11 indicating a good linearity of the isotherms. The decreased linearity with

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increasing DNA concentrations was also showed by lower R2 values in the presence of DNA in

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the fitting results of the linear model (Table 1). Thus, there is probably a chemical sorption

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mechanism of DNA-PAH complex to cation-modified montmorillonites. The same nonlinear

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isotherms of PAHs sorbed on humic acid-associated minerals (goethite, hematite, Cu2+- and


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Ca2+-montmorillonite) were also reported.56, 57 Overall, it is clear that that DNA facilitates the

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sorption of PAHs to montmorillonites.

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Sorption of DNA to montmorillonites. To probe the mechanisms responsible for the

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DNA-facilitated sorption of PAHs to the modified montmorillonites, we further examined the

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sorption of DNA-PAH complex by the montmorillonites using AFM, LSCM and batch sorption

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experiments (Figure S6). Figure S6a-c shows the LSCM images of DNA-PAH complexes sorbed

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on Na-MMT (a), Ca-MMT (b) and Fe-MMT (c). The blue parts showed the DAPI-stained DNA

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sorbed on the montmorillonites. The AFM images in Figure S6d-f illustrated that the filamentous

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DNA was tightly attached to the surface of the Na-MMT (d), Ca-MMT (e) and Fe-MMT (f). The

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sorption of DNA on the montmorillonites followed the order of Fe-MMT > Ca-MMT >

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Na-MMT in the absence of PAHs, and the sorption isotherms were well fitted with the

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Freundlich model (Figure S6g and Table S3). Considering the molar concentrations of the sorbed

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DNA nucleobase pairs (e.g., ~0.02 mM) were about two orders of magnitude greater than the

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sorbed PAH molar concentrations (e.g., ~0.0001 mM) on the montmorillonites, the sorbed DNA

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could fully carry the sorbed PAH molecules. It is recognized that the DNA used here varies from

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environmental extracellular DNAs in concentrations, polymer size, type (chromosomal and

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plasmid DNA), and sequence structure (%G-C). Nonetheless, it could serve as a model system

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for exploring interaction mechanisms among extracellular DNAs, PAHs, and soil clay,

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recognizing that the actual magnitude of these interactions may vary in natural environment.



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Microscopic and spectroscopic analyses. Furthermore, we used microscopic and

291

spectroscopic techniques to identify the sorption sites of the montmorillonites for DNA and

292

PAHs. As revealed by the XRD patterns of Na-MMT, Ca-MMT, and Fe-MMT after the sorption

293

of PAHs, DNA, and PAH-DNA complex, the interlayer spacing was increased after the sorption

294

of the PAHs (Figure S4a-c), indicating that the PAHs were intercalated in the clay interlayers,

295

probably facilitated by cation-π interactions.5, 19, 58 Similarly, the interlayer spacing generally

296

increased after the sorption of DNA, supporting the intercalation of DNA. Additionally, the

297

negatively charged phosphate groups on the outer surface of DNA may easily complex with the

298

positively charged exchangeable cations in the montmorillonites, thus forming a stable

299

cation-phosphate complexes.

300

Further molecular evidences were identified on the linkages between cations, DNA

301

phosphate group, and DNA-PAH complexes. Formation of cation-phosphate (DNA-Ca and

302

DNA-Fe) complexes was verified by the XPS analysis, as shown in Figure 2. The XPS spectra of

303

oxygen (Figure 2a) showed that the peak assigned to the O 1s spectrum of the DNA phosphate

304

groups59 shifted from 532.58 eV for the unmodified MMT without sorption of PAHs or DNA to

305

532.38 eV, 532.28 eV, and 532.48 eV for Na-MMT, Ca-MMT, and Fe-MMT in the presence of

306

PAHs and DNA (Figure 2a). However, there was no change for the peaks assigned to the N 1s

307

spectra (402.7 eV)60 and P 2p spectra (133.7 eV)61 of DNA (Figure 2b and 2c). Therefore, it was

308

likely that the DNA-PAH complex interacted with Na-MMT, Ca-MMT and Fe-MMT through

309

the O atom in the DNA phosphate group. 16 ACS Paragon Plus Environment

Page 17 of 31


310

Additionally, the binding energy of Na (Figure 2d), Ca (Figure 2e), Fe (Figure 2f) on the

311

Na-MMT, Ca-MMT, and Fe-MMT were also detected by XPS in the presence (black solid line)

312

and absence (red solid line) of DNA. The blue dashed line represents the standard binding energy

313

of each element. The binding energy of Na was only increased from 1072 eV62 to 1073.18 eV in

314

Na-MMT, but there was little change occurred after the DNA sorption (Figure 2d). This

315

phenomenon indicates no formation of chemical bond between Na and the O in the DNA

316

phosphate group. In the presence of DNA, the peak energy levels for the spectra of Ca 2p was

317

increased by 5.48 eV from the reported values of 346.6 eV63 (Figure 2e). In the absence of DNA,

318

the energy shift was 5.88 eV. The difference of 0.4 eV in the energy shift indicated that Ca2+

319

probably complexed with the O in the DNA phosphate group. Similarly, the peak energy level

320

for the spectra of Fe 2p was increased by 5.18 eV from the reported values of 719.9 eV64 to

321

725.18 eV in the presence of DNA (Figure 2f), whereas the energy shift was 5.88 eV in the

322

absence of DNA. This observation again suggests that Fe complexed with the O in the DNA

323

phosphate groups. Thus, Ca and Fe could serve as cation bridges between the hydroxyl groups

324

on the montmorillonite surface and the phosphate groups of DNA.

325

The FTIR spectra of MMT, DNA-MMT, PAH-MMT, and DNA-PAH-MMT (Figure 3) were

326

further used to identify the binding sites. For the montmorillonites with DNA, the vibrational

327

bands at 1691, 1649, 1605, and 1492 cm−1 are assigned to nucleobases including guanine (G),

328

thymine (T), adenine (A), and cytosine (C), respectively.59 The bands near1531, 1420 and 1488,

329

1369 cm−1 are attributed to imidazole ring, guanine and DNA structure, respectively. The 17 ACS Paragon Plus Environment


Page 18 of 31

330

absorption bands near 1236 cm−1 indicate the dissymmetrical stretch vibration of PO2−. Bands at

331

1080 and 1053 cm−1 separately represent the symmetrical stretch vibration of phosphate

332

functional groups and stretch vibration of P-O or C-O. The bands of 950−970 cm−1 indicate the

333

DNA backbone.65 The band of FTIR spectra less than 900 cm−1 is attributed to the “fingerprint”

334

zone caused by the functional groups such as phosphate. Because there was no change at the

335

bands of 1691, 1649, 1605, and 1492 cm−1, there was on binding of metal cations to nitrogenous

336

bases. However, the Ca-MMT and Fe-MMT with sorbed DNA had weaker absorption peaks at

337

1053 and 1236 cm−1 that represent the symmetrical and dissymmetrical stretch vibration of

338

phosphoric acid group. Additionally, the absorption spectra of DNA was obviously changed for

339

Ca-MMT and Fe-NMT, presumably by complexation between DNA and metal cations. Thus, it

340

was again confirmed that the most possible binding sites of DNA with the modified MMT are

341

located in the phosphate groups.

342

Based on the results of FTIR and XPS, we modeled the interactions of metal atoms (Na, Ca,

343

Fe) and the DNA phosphate groups (Figure 4). The HOMO is related to the outermost higher

344

energy orbital serving as an electron donor, whereas the LUMO is an electron acceptor.66, 67

345

Frontier molecular orbital energies and their energy gaps between the HOMO and LUMO are

346

displayed to show the stability of chemical bonding.68 The calculated energy gap was the lowest

347

for the Na-phosphate interaction (0.01077 eV, Figure 4a), the intermediate for the Ca-phosphate

348

interaction (0.04980 eV, Figure 4b), and the highest for the Fe-phosphate interaction (0.12626

349

eV, Figure 4c). Therefore, Fe3+ can form the strongest bond with the DNA phosphate group, 18 ACS Paragon Plus Environment

Page 19 of 31


350

followed by Ca2+, whereas Na+ is unlikely to complex with the phosphate group. This trend was

351

in agreement with the existing literature reporting that the binding strength of metal cations with

352

DNA increased with the valence of positive charged cations.37, 38, 44 Thus, in addition to Ca2+ and

353

Fe3+, we expect that other cations such as Al3+ could also form strong complexes with the DNA

354

phosphate groups, as supported by our previous report that environmental-relevant

355

concentrations of Al(III) species including Al3+, Al(OH)2+, and Al(OH)2+ could facilitate DNA

356

aggregation by complexing with the DNA phosphate group.36 This is particularly interesting

357

because hard cation Al3+-saturated montmorillonite may have lower cation-π bonding for the

358

PAH sorption,14, 54 the DNA-facilitated PAH sorption could then play an important role in

359

Al-rich soils such as Oxisols and Spodosols. Additionally, soils contain variable levels of

360

inorganic and organic phosphate compounds such as orthophosphate and phytate that may

361

compete with the DNA phosphate group for the exchangeable cations in clays. About 10% of

362

organic phosphate bound in SOM is from nucleic acids in mineral soils, and DNA may account

363

for up to 53% of extracted phosphorus in wetland soils.30 Thus, the DNA phosphates can still

364

play a significant role in the binding of DNA and DNA-associated contaminants to soils.

365

Mechanisms of DNA-enhanced PAH sorption by montmorillonites. We identified novel

366

mechanisms responsible for the enhanced sorption of PAHs to the montmorillonites facilitated

367

by DNA. DNA acts as a vehicle for small-sized PAH molecules, and the sorption of DNA-PAH

368

complexes increase the overall sorption of PAHs by the montmorillonites. In detail, the

369

nucleobases of DNA bind with PAHs via van der Walls, hydrogen bonding, and π-π EDA 19 ACS Paragon Plus Environment


Page 20 of 31

370

interactions to form the DNA-PAH complexes, followed by chemical bonding between DNA

371

phosphate groups and exchangeable metal cations in the montmorillonites (i.e., cation bridging).

372

Additionally, the DNA-PAH complexes can also be intercalated in the interlayers of the

373

montmorillonites, thus enhancing the PAH sorption.

374

It is known that humic and fulvic acids can bind with PAHs and further enhance their

375

sorption to soils through hydrophobic binding and complexation.69 However, DNA has

376

nitrogenous nucleobases, sugar deoxyriboses and phosphate groups distinct from the functional

377

groups in humic and fulvic acids. Thus, studying the interactions of PAHs with other types of

378

DOM rather than humic and fulvic acids in the environment (such as DNA) would provide key

379

information about how DOM influences the sorption of hydrophobic organic compounds in soils.

380

This study is limited in using a double-stranded model DNA in the Tris-HCl buffer solution (10

381

mM, pH 7.0), because DNA sorption to soils (specifically clay) may depend on DNA polymer

382

size, ionic strength, and pH.41-43 The binding of PAHs to DNA is controlled by substitution of

383

functional groups on benzene rings and the %G-C and chirality of DNA structure.32-34 Future

384

studies could be directed to more diverse structures of DNA (e.g., molecular weight and %G-C),

385

PAHs, or proteinaceous compounds to improve our understanding on environmental behaviors of

386

PAHs under natural conditions.

387

ASSOCIATED CONTENT

388

Supporting Information


Page 21 of 31


389

S1. Supplemental methods including MMT preparation and characterizations, and model

390

computation; S2. Supplemental results including MMT characterization data, sorption isotherms

391

and fitting results, and SEM-EDX and XRD spectra of MMTs.

392

Supporting Information is available free of charge on the ACS Publications website at DOI:

393

AUTHOR INFORMATION

394

Corresponding Author

395

*Weigang Road 1, Nanjing 210095, China. Tel: +86-25-84395019. E-mail:

396

[email protected].

397

Notes

398

The authors declare no competing financial interest.

399

Acknowledgments

400

The work was supported by Jiangsu Provincial Key Research and Development Plan, China

401

(BE2017718), the Special Fund for Agro-Scientific Research in Public Interest, China (No.

402

201503107), and the National Science Foundation of China (41771523).



Page 22 of 31

403

References

404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440

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583


Page 27 of 31

584 585


Table 1. Fitting linear isotherm parameters of phenanthrene and pyrene sorption to Na-MMT, Ca-MMT, and Fe-MMT. DNA (mg/L)

Na-MMT

0

0.0458

0.5

Ca-MMT

Fe-MMT

586 587

a

Phenanthrene

Sorbents

Pyrene Kd (L/g)

R2

0.992

0.0493

0.985

0.110

0.974

0.171

0.980

1

0.217

0.989

0.234

0.994

5

0.351

0.993

0.301

0.996

10

0.465

0.996

0.385

0.994

0

0.0985

0.995

0.0919

0.950

0.5

0.159

0.959

0.149

0.944

1

0.215

0.978

0.272

0.950

5

0.309

0.976

0.366

0.918

10

0.413

0.941

0.432

0.822

0

0.103

0.972

0.141

0.996

0.5

0.117

0.997

0.182

0.984

1

0.187

0.990

0.303

0.977

5

0.394

0.965

0.383

0.958

10

0.589

0.932

0.560

0.934

Kd (L/g)

a

R

2

Kd is the distribution coefficients.



588 589 590 591 592 593 594 595 596 597

Page 28 of 31

Figure 1. Interactions of DNA with phenanthrene and pyrene probed by DNA-induced fluorescence quenching: (a) Stern-Volmer plot and (b) Plot of Log [(F0-F)/F] vs Log [Q]. Comparison of the molecular orbitals between (adenine, thymine, cytosine, guanine)-phenanthrene (c) and (adenine, thymine, cytosine, guanine)-pyrene (d) in HOMO orbital and LUMO orbital analyses by the GaussView 5.0. The C, H, O and N in adenine, thymine, cytosine, and guanine are colored in gray, white, red and blue, respectively. Larger brown and green spheres represent the positive and negative phases of electronic wave function, respectively.


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Figure 2. XPS analysis of O (a), N (b), and P (c) of DNA on the surface of montmorillonites. And XPS analysis of Na (d), Ca (e), and Fe (f) on the Na-MMT, Ca-MMT, and Fe-MMT, respectively, with and without sorbed DNA or PAHs. The black lines in panel d, e, and f represent the montmorillonites in the presence of 10 mg/L DNA and 120 µg/L PAHs and the red lines in panel d, e, and f represent the montmorillonites in the presence of 120 µg/L PAHs.



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Figure 3. Comparison of FTIR spectra of DNA sorbed on Na-MMT (a, a’), Ca-MMT (b, b’), and Fe-MMT (c, c’) with and without DNA, PAHs, or DNA-PAH complexes. The circled regions in panel a, b and c are enlarged in panel a', b', and c'. Phe represents phenanthrene, and pyre represents pyrene.


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Figure 4. Computation results of the interactions between the DNA phosphate group and Na+ (a), Ca2+ (b), or Fe3+ (c). The C, H, O and P in DNA are colored in gray, white, red, and yellow, respectively. The added metal atoms are colored in purple (Na), green (Ca), and pink (Fe). Larger brown and green spheres near metal atoms represent the positive and negative phases of electronic wave function, respectively.


DNA Facilitates the Sorption of Polycyclic Aromatic Hydrocarbons on

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