Dissolved Organic Matter Adsorption to Model Surfaces: Adlayer

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Dissolved Organic Matter Adsorption to Model Surfaces: Adlayer Formation, Properties, and Dynamics at the Nanoscale Antonius Armanious, Meret Aeppli, and Michael Sander* Institute of Biogeochemistry and Pollutant Dynamics (IBP), Department of Environmental Systems Science, Swiss Federal Institute of Technology, ETH Zurich, 8092 Zurich, Switzerland S Supporting Information *

ABSTRACT: Adlayers of dissolved organic matter (DOM) form on many surfaces in natural and engineered systems and affect a number of important processes in these systems. Yet, the nanoscalar properties and dynamics of DOM adlayers remain poorly investigated. This work provides a systematic analysis of the properties and dynamics of adlayers formed from a diverse set of eight humic and fulvic acids, used as DOM models, on surfaces of self-assembled monolayers (SAMs) of different alkylthiols covalently bound to gold supports. DOM adsorption to positively charged amine-terminated SAMs resulted in the formation of water-rich adlayers with nanometer thicknesses that were relatively rigid, irreversibly adsorbed, and collapsed upon air drying, as demonstrated by combined quartz crystal microbalance and ellipsometry measurements. DOM adlayer thicknesses varied only slightly with solution pH from 5 to 8 but increased markedly with increasing ionic strength. Contact angle measurements revealed that the DOM adlayers were relatively polar, likely due to the high water contents of the adlayers. Comparing DOM adsorption to SAM-coated sensors that systematically differed in surface charge and polarity characteristics showed that electrostatics dominated DOM−surface interactions. Laccase adsorption to DOM adlayers on amine-terminated SAMs served to demonstrate the applicability of the presented experimental approach to study the interactions of (bio)macromolecules and (nano)particles with DOM.

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INTRODUCTION Dissolved organic matter (DOM) makes up a significant fraction of the total organic carbon pool in terrestrial, aquatic, and marine environments. DOM is also present in engineered systems including water treatment facilities and water reservoirs. In all of these systems, DOM adsorbs to waterexposed surfaces, resulting in the formation of DOM adlayers. DOM adsorption is of interest for a number of reasons. First, adsorption alters the stability and the composition of DOM. Adsorption to mineral surfaces protects DOM from degradation by extracellular enzymes and thus contributes to the sequestration of organic carbon in soils and sediments.1−4 Preferential adsorption of DOM subfractions alters the chemical composition of the DOM that remains dissolved.5−8 Second, surfaces coated with DOM exhibit physicochemical properties and hence reactivities that differ substantially from those of the bare, uncoated surfaces. For instance, DOM adsorption to suspended particles may alter both particle− particle and particle−collector interactions and, hence, the coagulation and deposition dynamics of the particles. Such effects have been reported for minerals as well as engineered nanoparticles.9−11 DOM adsorption to membrane surfaces triggers fouling and hence diminishes membrane performance.12−15 Finally, the surfaces of the DOM adlayers interact with cells, (bio)macromolecules, (nano)particles, and organic © XXXX American Chemical Society

and inorganic pollutants in solution, thereby altering their fates and activities.16−29 For these reasons, there is considerable interest in obtaining a detailed understanding of the factors governing DOM adsorption to surfaces and of the properties and dynamics of the formed DOM adlayers.8,30 DOM adsorption to surfaces has a number of energetic contributions. Because DOM is a negatively charged polyelectrolyte, it experiences electrostatic attraction to positively charged and electrostatic repulsion from negatively charged surfaces.31−33 Electrostatic interactions are strongly dependent on solution chemistry because pH and ionic strength (I) affect the charges of the DOM and the sorbent surfaces and the extent of charge shielding in solution. DOM adsorption is facilitated both by specific DOM−surface interactions, including ligand exchange reactions and H-bonding between the DOM and polar sites on the surfaces,3,29,34−36 and by nonspecific van der Waals interactions. The hydrophobic effect may facilitate DOM adsorption to apolar surfaces.5,37,38 Finally, adsorption has unfavorable entropic contributions,30 as it lowers the conformational freedom of the DOM. While several Received: June 3, 2014 Revised: July 14, 2014 Accepted: July 15, 2014

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dx.doi.org/10.1021/es5026917 | Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Environmental Science & Technology

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extents, and reversibility of the adsorption of eight different humic acids (HAs) and fulvic acids (FAs) as a function of solution pH (5.0−8.0) and ionic strength (10−500 mM; adjusted by NaCl) to chemically well-defined SAM surfaces using QCM-D. DOM adsorption was primarily studied to positively charged amine-terminated SAM surfaces, reflecting the importance of electrostatic attraction in DOM adsorption to positively charged mineral surfaces in natural systems. The HAs and FAs were chosen such that they spanned a wide range of physicochemical properties and originated from both terrestrial and aquatic sources. Information on the wet adlayer masses and thicknesses obtained by QCM-D were complemented by ellipsometry and contact angle measurements to determine the thicknesses of DOM adlayers after drying and the wettability characteristics of wet and dry DOM adlayers, respectively. To meet the second objective, we measured the kinetics, extents, and reversibility of laccase adsorption to selected DOM adlayers and model surfaces under different solution conditions.

of these interactions may act simultaneously during DOM adsorption to a given surface, electrostatics are considered to play a major role. For instance, electrostatic attraction contributes to the particularly strong association of DOM with the surfaces of positively charged minerals in soils and sediments.3,5−7,29,31−33,35−45 Adsorption of DOM depends on solution chemistry and forms adlayers with nanometer thicknesses30,46 and masses of 10−50 ng·cm−2.35,39 Desorption of the DOM from the surfaces is often kinetically slow because it requires that numerous DOM−surface bonds are broken simultaneously. Macroscopically, slow desorption manifests itself as sorption hysteresis.8,35,37 A systematic investigation of the nanoscalar properties and dynamics of DOM adlayers, however, remained missing from the literature, partly reflecting that these characteristics are not easily determined by traditional solution depletion methods. In contrast, in situ surface techniques offer the possibility to directly monitor the formation and dynamics of DOM adlayers on various surfaces. Among these techniques, quartz crystal microbalance with dissipation monitoring (QCM-D) is unique in that it senses DOM adlayer-associated water and hence allows measuring the masses, thicknesses, and viscoelastic properties of wet DOM adlayers. This feature is important in light of the polyelectrolytic character and the high water contents of DOM adlayers (i.e., 70−90 mass %).16−18 QCM-D measures changes in the masses adsorbed onto the surfaces of sensors by monitoring the resulting changes in the resonance frequencies of piezoelectric quartz resonators embedded into these sensors. QCM-D was previously used to study the adsorption of selected DOMs to aluminum oxide coated sensors40−42 and to positively charged polyelectrolytes (e.g., poly-L-lysine) immobilized on silica sensors.16−28 However, positively charged weak polyelectrolytes form loops and tails in adsorbed states47−52 and hence result in uneven surfaces that may lead to enhanced DOM adsorption compared to flat surfaces. Furthermore, because the conformation of adsorbed polyelectrolytes is dependent on solution chemistry,48,49 these surfaces are ill-suited to selectively study the effects of solution pH and I on DOM adlayer formation and dynamics. In contrast to polyelectrolytes, self-assembled monolayers (SAMs) of alkylthiols (i.e., HS−(CH2)n−R) on gold supports spontaneously form flat, stable, and rigid surfaces by covalent binding of the sulfur in the headgroup (HS−) to the Au atoms on the gold surfaces.53 The alkyl chains (i.e., −(CH2)n−) self-assemble into densely packed formations with the functional groups (− R) oriented toward the solution. The SAM approach allows altering the surface chemistries of the SAM by using alkylthiols with different functional groups. For instance, SAM surfaces formed from alkylthiols with amine (SAM−NH+3 ), carboxyl (SAM−COO−), hydroxyl (SAM−OH), and methyl (SAM− CH3) functional groups can be used to assess the role of electrostatic attraction and repulsion, H-bonding, and the hydrophobic effect on DOM adsorption, respectively. Furthermore, the conformation of SAMs is independent of solution pH and I. This work had two major objectives. The first objective was to systematically study the formation, dynamics, and properties of DOM adlayers at the nanoscale as a function of DOM type and solution chemistry. The second objective was to demonstrate that DOM adlayers on amine-terminated SAM surfaces can be used to investigate the interactions of (bio)macromolecules and (nano)particles with DOM adlayer surfaces. To meet the first objective, we measured the kinetics,

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MATERIALS AND METHODS DOM Samples, Laccase, and Chemicals. Standard HAs and FAs of Leonardite (LHA), Elliot soil (i.e., ESHA and ESFA), Pahokee peat (i.e., PPHA and PPFA), and Suwannee River (i.e., SRHA and SRFA), and natural organic matter from Suwannee River (i.e., SRNOM) were obtained from the International Humic Substances Society (IHSS). Selected physicochemical properties and ordering information of the DOMs are provided in section S1, Supporting Information (SI). Laccase from Trametes versicolor (T. versicolor; 22.4 U· mg−1) was obtained from Fluka. All other chemicals used were of analytical grade and are listed in section S2, SI. All materials were used as received. Solutions. All solutions were prepared in Milli-Q water (resistivity ≈ 18.2 MΩ·cm; Barnstead NANOpure Diamond) and pH buffered using acetic acid (pH 5), bis(2-hydroxyethyl)aminotris(hydroxymethyl)methane (pH 6 and 7) and tris(hydroxymethyl)aminomethane (pH 8). We did not use 4-(2hydroxy-ethyl)-1-piperazineethanesulfonic acid as it interfered with DOM adsorption to amine-terminated SAM surfaces. The solution pH and total ionic strength, I, were adjusted with NaOH and HCl (each 1 M) and sodium chloride, respectively. Solutions of DOM (50 μgDOM·mL−1) and laccase (500 μg· mL−1) were prepared as detailed in section S2, SI. Formation of SAMs on Gold. SAMs were formed on thoroughly cleaned gold-coated QCM-D sensors (QSX 301, QSense). The cleaning protocol is described in section S2, SI. The cleaned sensors were transferred into polypropylene tubes containing an alkylthiol solution (0.5−2.0 mM) in anhydrous ethanol and left to react for at least 12 h, all in an O2-free glovebox (N2) to rule out thiol oxidation. The SAMs were formed from cysteamine (SAM−NH3+), 11-Amino-1-undecanethiol, 11-mercaptoundecanoic acid (SAM−COO−), 1dodecanethiol (SAM−CH3), and 11-mercapto-1-undecanol (SAM−OH). After SAM formation, the sensors were rinsed with ethanol, sonicated in ethanol for 2 min, and again rinsed with ethanol to remove unbound alkylthiols. The sensors were then dried under an N2 stream and used in adsorption experiments on the same day. Proper formation of SAMs on the Au surfaces was confirmed by ellipsometry measurements (see section S2, SI, for details) and by contact angle measurements, as detailed below. B



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SAM−NH3+ surfaces at pH 5 and I = 10 mM, as measured by QCM-D. All other tested DOMs had comparable adsorption profiles. At the onset of the experiment (t < 0 min), the SAM− NH3+ surfaces were rinsed with DOM-free buffer solutions leading to stable Δf 9/9 and ΔD9 values. Switching to DOMcontaining solutions (t = 0 min) resulted in DOM adsorption, as evidenced from decreasing Δf 9/9 values. Initial fast adsorption was followed by a transitional phase with slower adsorption that ultimately plateaued at well-defined final adsorbed masses, which were larger for ESHA than SRFA. Subsequent rinsing with DOM-free solutions resulted in only small increases in Δf 9/9, demonstrating that ESHA and SRFA were irreversibly adsorbed. Fast initial adsorption, a sharp transition into an adsorption plateau, and no desorption upon rinsing suggest strong electrostatic attraction of the DOMs to the SAM−NH3+ surfaces. DOM adsorption stopped when DOM saturated the SAM−NH3+ surfaces. Extensive coverages of the positively charged SAM−NH3+ surfaces by DOMs were confirmed in control experiments in which solutions containing poly(acrylic acid) (PAA), a negatively charged polyelectrolyte, were run over ESHA adlayers and over bare SAM−NH3+ surfaces (section S3, SI). While PAA adsorbed extensively to the oppositely charged SAM−NH3+ surfaces, it did not adsorb to the ESHA adlayers. In the subsequent discussion, we use the term “monolayer” to describe the final DOM adlayer at surface saturation. We deliberately use this term to account for the fact that DOM has both polyelectroyte and micellar properties.54−56 Masses and Thicknesses of DOM Adlayers. Figure 1b shows selected adsorption profiles of the eight tested DOM samples onto SAM−NH3+ surfaces. Adsorption is expressed both in terms of adsorbed mass and averaged adlayer thicknesses. The adsorbed masses were calculated from Δf values using the Sauerbrey equation (eq 1), which was applicable as the adlayers were relatively rigid (i.e., relatively small ratios of dissipation to frequency changes, as detailed in section S4, SI). Comparable adsorbed masses were obtained using the Voigt model and hence by accounting for the viscoelastic properties of the DOM adlayers (section S4, SI). We note that the adlayer thicknesses were calculated based on the simplifying assumption that the adsorbed DOM was equally distributed over the entire SAM−NH3+ surfaces. Because this assumption was best met upon saturation of the surfaces by the DOMs, we will subsequently discuss only the thicknesses of final adlayers after adsorption plateaued. However, it is important to note that the final adlayers had nonuniform thicknesses due to the polydispersity of the adsorbing DOMs37,57 and the fact that saturation of surfaces by polyelectrolytes (including DOM) occurs below 100% surface coverage. We independently confirmed the effect of polydispersity on adlayer thicknesses by adsorbing two ESHA size fractions obtained by centrifugation of an ESHA solution through a 2 kDa cutoff membrane filter. The adsorption of the filtrate (2 kDa) (section S5, SI). The adsorption profiles of all DOMs were similarly shaped but differed in the initial rates and the final extents of adsorption (Figure 1b). In fact, the initial rates and the final extents of adsorption were linearly correlated (section S6, SI). Larger DOMs thus delivered more mass to the SAM−NH3+ surfaces in initial stages of adsorption and resulted in heavier and thicker adlayers in final stages of adsorption. The final adlayer masses and thicknesses of the different DOMs from all adsorption experiments are compiled in Figure 1c and in a table

QCM-D Experiments. DOM adsorption was measured using a QCM-D (Q-Sense E4 system; Q-Sense AB) equipped with four flow-through cells. Adsorption to and desorption from a QCM-D sensor surface is measured by monitoring the changes in the resonance frequencies (Δf n) and energy dissipation values (ΔDn) of the fundamental tone (n = 1) and several overtones (n = 3−13) of an oscillating piezo-quartz crystal in the sensor. Two approaches were used to convert the changes in frequency and dissipation values to adsorbed masses. The first approach relied on the Sauerbrey equation which is valid for nondissipative to weakly dissipative adlayers: Δm = C

−Δfn n

(1)

where Δm (ng·cm−2) is the areal mass density of the wet adlayer, C (=17.7 ng·cm−2·Hz−1) is the sensor-specific mass sensitivity constant, and Δf n (Hz) is the frequency shift of the nth overtone. The data from the 7th or the 9th overtone were used for calculations and plotting. In the second approach, the Voigt model in the QTools instrument software was used to describe the data. This model accounts for the adlayer viscoelasticity to calculate adsorbed masses. For both approaches, an adlayer density of 1050 kg·m−3 was used to convert final adsorbed masses to adlayer thicknesses.16−18 The adlayer density is slightly larger than that of bulk water, reflecting the high water contents of DOM adlayers. The thicknesses have to be considered estimates as the calculation is based on the simplifying assumption that the DOM adlayers were perfectly homogeneous in density and distribution on the SAM−NH3+ surfaces. QCM-D experiments were conducted at a constant flow rate of 20 μL·min−1 using a peristaltic pump. A typical DOM adsorption experiment consisted of three consecutive steps: (i) equilibration of the mounted sensors to DOM-free pH-buffered solutions to obtain stable baseline readings; (ii) introduction and continuous delivery of DOM solutions (50 μgDOM·mL−1) over the sensors; (iii) rinsing with DOM-free solutions. All steps were conducted at constant pH and I. The laccase adsorption experiments included two additional steps: (iv) introduction and continuous delivery of laccase solutions (500 μg·mL−1) over the DOM adlayers; (v) rinsing with laccase-free solutions. Ellipsometry. The thicknesses of air-dried SAMs and of DOM adlayers on the SAM−NH3+ surfaces were measured by spectroscopic ellipsometry (M-2000F system; J.A. Woollam Co. Inc.) over a wavelength range of 370−995 nm and at an incident angle of 70°. Details on the measurements and thickness calculations are provided in section S2, SI. Contact Angle Measurements. The wettability characteristics of the model surfaces and DOM adlayers were determined by measuring the contact angles (i) of sessile water drops (volume of 3 μL) on these surfaces after they were dried under an N2 stream and (ii) of captive air and octane bubbles (volume of 2 μL) on inverted surfaces under pH 5 and I = 10 mM solutions using a DSA 100 system (Krüss GmbH). Additional information is provided in section S2, SI.

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RESULTS AND DISCUSSION Formation of DOM Adlayers on Amine-Terminated SAM Surfaces. Figure 1a shows the shifts in the frequency and dissipation values of the 9th overtone (i.e., Δf 9/9 and ΔD9, respectively) during adsorption of ESHA and SRFA onto C



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Figure 1. Adsorption of dissolved organic matter (DOM) to the surfaces of self-assembled monolayers (SAMs) of cysteamine on gold (Au) at pH 5 and ionic strength (I) of 10 mM: (a) Adsorption profiles of Elliot soil humic acid (ESHA) and Suwannee River fulvic acid (SRFA), expressed as changes in the frequency and dissipation values of the ninth oscillation overtone (i.e., Δf 9/9 and ΔD9); (b) adsorption profiles and corresponding masses and final thicknesses of eight DOM adlayers calculated using the Sauerbrey equation; (c) compiled adlayer masses and thicknesses for eight tested DOMs (mean values ± standard deviations); (d) thicknesses of DOM adlayers in water and after drying in air, as measured by QCM-D and ellipsometry, respectively (the thicknesses of the dried DOM adlayers were corrected for the thicknesses of the underlying amine-terminated SAMs of 0.46 nm); (e) contact angles of sessile water drops on dried DOM adlayers and model surfaces; (f) captive bubble contact angles of octane on inverted DOM adlayer surfaces and model surfaces in buffered solutions (pH 5 and I = 10 mM). The model surfaces included SAM−COO−, SAM− OH, SAM−NH3+, bare Au, and SAM−CH3.

adsorbed states.60,61,63 Larger sizes of HAs than FAs have been ascribed to HAs having larger molecular weights, lower charge densities, and lower polarities and hence increased cohesion in HA assemblies due to the hydrophobic effect. An interdependence of DOM polarity and size is supported by the QCM-D data which show that the final adlayer thicknesses tended to increase with increasing molar C/(O + N + S) ratios and hence increasing apolar character16,18 of the DOMs (section S8, SI). A large part of the volume of DOMs, in both dissolved58,64 and adsorbed states,16−18 is occupied by water. The DOM adlayers are therefore expected to collapse and to become thinner upon drying. This was confirmed by ellipsometry measurements which showed that the wet DOM adlayers lost about 40% of their thicknesses upon drying (Figure 1d). The linear correlation between the wet and dry thicknesses

in section S7, SI. The DOM adlayers were very thin with thicknesses that ranged from 0.5 nm for PPFA to 2.3 nm for ESHA, corresponding in lengths to those of alkyl chains with only 3−15 carbon atoms. While the DOMs likely changed their conformation upon adsorption and flattened on the surface, the measured thicknesses are in general agreement with previously reported sizes of dissolved and adsorbed DOM estimated by other techniques.46,57−62 The diverse set of DOMs studied in this work allows identifying trends between adlayer properties and types of DOM. For instance, when comparing HAs and FAs that were extracted from the same source material, the adlayer masses and thicknesses were higher for the HAs than FAs (Figure 1c). These differences were more pronounced for terrestrial (i.e., Elliot soil and Pahokee peat) than for the aquatic (i.e., Suwannee River) DOMs. Larger sizes of HAs than FAs have previously been reported for dissolved but not for D



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amine groups in the SAM−NH3+ surfaces deprotonate at pH ≥ 7.0).72−74 Increasing the pH from 5 to 8 did not result in systematic changes in the adlayer masses and thicknesses of the different DOMs. This finding is consistent with previous studies that showed small pH effects on the sizes of selected DOMs in solution58 and adsorbed onto mica surfaces.75 The observed slight decrease in ESHA adlayer masses with increasing pH may have resulted from more stretched conformations of ESHA assemblies in solution (due to increasing densities of negatively charged moieties and hence intra-ESHA electrostatic repulsion) with increasing pH and, hence, flatter adlayers upon adsorption at high than at low pH. In contrast to pH, increases in solution I from 10 to 500 mM at constant pH 5 resulted in significant increases in DOM adlayer masses and thicknesses. A similar trend was previously reported for the adsorption of selected DOMs to mineral surfaces.32,33 The increase in final adlayer masses with increasing I likely resulted from DOM adsorbing in more condensed states due to shielding of electrostatic repulsion within each DOM both in solution and in adsorbed states and between DOM adsorbed onto the SAM−NH3+ surfaces. The adsorption profiles of ESHA at I = 10−100 mM had similar shapes with initial fast adsorption followed by transitions into well-defined adsorption plateaus (Figure 2b), consistent with the formation of ESHA monolayers of different thicknesses. In contrast, ESHA adsorption at I = 250 mM and 500 mM (not shown in Figure 2b) showed an initial phase of fast adsorption followed by a second phase of slower adsorption that continued until rinsing with ESHA-free solutions was initiated. Replotting the adsorption profiles by relating changes in the adsorbed masses to changes in dissipation values revealed that the adlayers formed in the second phases were much more dissipative than the adlayers formed in the first phases (section S12, SI). We note that adsorption into the second phase was observed only at high I and was pronounced only for ESHA and LHA (section S12, SI), the most apolar and least charged DOMs tested (section S1, SI). Based on these findings, we ascribe the second phase to adsorption in excess of a monolayer, which required high I to shield DOM−DOM electrostatic repulsion and apolar DOMs with favorable contributions from the hydrophobic effect to DOM−DOM interactions. Effect of Sorbent Surface Chemistry on DOM Adsorption. Tailoring the Au sensors with different SAMs allows assessing the relative contributions of different DOM− surface interactions to DOM adsorption. Figure 2d shows selected adsorption profiles of ESHA to SAMs terminated with carboxyl (SAM−COO−; negatively charged), methyl (SAM− CH3; apolar), and hydroxyl (SAM−OH; polar) groups in addition to SAM−NH3+ and bare gold surfaces. The experiments were conducted at pH 7 and I = 10 mM to ensure high negative charge densities on the SAM−COO− surfaces.76 All results are compiled in section S13, SI. A comparison of ESHA adsorption to the different tested surfaces reveals that electrostatics dominated ESHA−surface interactions: while electrostatic attraction to SAM−NH3+ surfaces resulted in ESHA monolayer adsorption, electrostatic repulsion of ESHA from like-charged SAM−COO− completely inhibited adsorption. Very little ESHA adsorbed to the SAM−OH surface, suggesting only minor energetic contributions from H-bonding to ESHA adsorption. It is likely that H-bond interactions between ESHA and the SAM−OH surfaces were competitively suppressed by strong interactions of H2O with both polar

measured by QCM-D and ellisometry suggests comparable water contents of the adlayers formed from the different tested DOMs. DOM Adlayers on Different Positively Charged Surfaces. Adsorption of DOM to SAM−NH3+ and SAMs formed from 11-amino-1-undecanethiol (i.e., two and eleven carbons in the alkyl chain, respectively) resulted in very similar adsorption profiles and final DOM adsorbed masses (section S9, SI). The length of the alkyl chain of the aminoalkylthiol therefore did not affect DOM adsorption. Conversely, DOM adlayer masses were significantly smaller on the SAM−NH3+ surfaces (this work) than on poly-L-lysine (PLL) immobilized on silica sensors (previous work)16 (section S10, SI). Smaller DOM adlayer masses on SAM−NH3+ than PLL were independently confirmed by adsorbing two DOMs, SRNOM and SRFA, to both surfaces (section S10, SI). The larger adlayer masses on the PLL surfaces likely resulted from DOM adsorption to tails and loops of PLL that extended from the silica surfaces into solution. This explanation is supported by the positive correlation in DOM adlayer masses on the SAM− NH3+ and PLL surfaces (section S10, SI), because tails and loops are expected to enhance adsorption of both small and large DOMs. Based on these findings we recommend the use of smooth, rigid, and planar amine-terminated SAM surfaces rather than dynamic, flexible, and uneven polyelectrolyte surfaces in future studies on DOM adsorption as well as on the adsorption of (bio)macromolecules and (nano)particles to DOM adlayers, as highlighted below for laccase adsorption. Wettability Characteristics of DOM Adlayers. Sessile water drops had comparable contact angles (30°−45°) on all DOM adlayers (Figure 1e), suggesting that they had similar wettability characteristics. Contact angles of water drops covered a much wider range on the Au and SAM model surfaces, and increased from the most polar SAM−COO− surface to the most apolar SAM−CH3 surface (Figure 1e). All measured contact angles are compiled in section S11, SI. The angles on the model surfaces were in good agreement with literature values.65−68 The captive bubble contact angles were measured on inverted DOM adlayers under solution and were therefore not susceptible to potential drying-induced changes in the DOM adlayers (e.g., adlayer collapse, Figure 1d).69−71 While air bubbles did not stick to most of the DOM adlayers, octane bubbles had comparable contact angles on all tested DOM adlayers (i.e., 27°−44°; Figure 1f). The contact angles of octane bubbles covered a much larger range on the model surfaces (Figure 1f and section S11, SI). Given that the contact angles of water drops and octane bubbles on the DOM adlayers were comparable to the respective angles measured on the polar SAM−OH and SAM−NH3+ surfaces, the DOM adlayer surfaces were relatively polar. The polarity of the DOM adlayer surfaces suggests that the adlayer associated water, in addition to the polarity characteristics of the DOM backbones, largely contributed to the interfacial energies determined by microlitersized drops/bubbles used in the contact angle measurements. Effect of Solution Chemistry on DOM Adlayers. Figure 2 shows the effects of solution pH and I on the final adlayer masses and thicknesses of ESHA, ESFA, SRHA, and SRFA. These four DOMs were selected to allow comparing DOMs from terrestrial (ES) and aquatic (SR) sources and, for both sources, HAs to FAs. From pH 5 to 8, DOM adsorption to SAM−NH3+ surfaces was extensive (Figure 2a), consistent with electrostatic attraction under these pH conditions (i.e., the E



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Figure 2. Effects of solution pH, ionic strength (I), and sorbent surface chemistry on adsorption of DOM: (a) Effect of pH on final adlayer masses and thicknesses of humic and fulvic acids from Elliot soil (i.e., ESHA and ESFA) and Suwannee River (i.e., SRHA and SRFA) on positively charged self-assembled monolayer surfaces (SAM−NH3+; all experiments were conducted at I = 10 mM with NaCl as the background electrolyte); (b) adsorption profiles of ESHA to SAM−NH3+ at I = 10, 50, 100, and 250 mM, all at pH 5; (c) effect of I on the masses and thicknesses of ESHA, ESFA, SRHA, and SRFA adlayers on SAM−NH3+ surfaces, all at pH 5 (the § symbol indicates that the use of the Sauerbrey equation underestimated the adsorbed masses due to high energy dissipation in the respective adlayers); (d) Adsorption profiles of ESHA to SAM−NH3+, SAM−CH3, Au, SAM−OH, and SAM−COO− surfaces, all at pH 7 and I = 10 mM.

details provided in section S14, SI). Increasing from pH 5 to 8 increases the negative charges and decreases the positive charges on the laccase surface due to deprotonation of ionizable amino acids. However, the laccase surface still has negatively charged patches (red in Figure 3a) below its IEP and positively charged patches (blue in Figure 3a) above its IEP. Proteins with nonuniform surface charge distributions are susceptible to patch-controlled electrostatic attraction (PCEA) to charged sorbent surfaces.17,18,80,81 A representative adsorption profile of laccase to an LHA adlayer at pH 5 and I = 10 mM is shown in Figure 3b. Initial fast adsorption was followed by a sharp transition into an adsorption plateau. Subsequent rinsing with laccase-free solutions resulted in only slight desorption of laccase. These features are consistent with strong laccase−LHA electrostatic attraction and the formation of a monolayer of laccase on the LHA surface. Monolayer adsorption is supported by similar adsorption profiles of laccase to ESHA, ESFA, SRHA, and SRFA with comparable final adsorbed masses (i.e., 400−450 ng·cm−2) and overall irreversible adsorption (Figure 3c and section S15, SI). At pH 5 and I = 10 mM laccase also adsorbed extensively and irreversibly to both negatively charged SAM−COO− and to positively charged SAM−NH3+ surfaces (Figure 3c). These results point toward PCEA of laccase in that it adsorbed via

ESHA moieties and the hydroxyl groups on the SAM−OH surfaces. The use of more apolar SAM−CH3 and Au surfaces resulted in intermediate ESHA adsorption, suggesting a contribution from the hydrophobic effect to adsorption. Also, the finding that ESHA adsorbed much slower and less extensively onto the uncoated Au surface (i.e., the surface with the highest density and polarizability and hence propensity to undergo van der Waals interactions) suggests that DOM adsorption to charged surfaces had comparatively small contributions from van der Waals interactions as compared to electrostatic interactions. Weak van der Waals interactions involving DOM can be rationalized on the basis of the high water contents of DOM. Overall, these data demonstrate that SAMs on gold supports provide a viable experimental platform to assess the relative importance of different DOM−surface interactions to DOM adsorption. Laccase Adsorption to DOM Adlayers. To meet the second objective of this work, we studied the adsorption of laccase from T. versicolor to DOM adlayers. Laccase was chosen because it oxidizes polyphenolic structures in DOM and lignin and is one of the key enzymes involved in organic matter oxidation in soils, sediments, and wetlands.77−79 While the used laccase has an estimated isoelectric point (IEP) = 5.9, it has a highly nonuniform surface charge distribution, as revealed by modeling of its electrostatic isopotential surfaces (Figure 3a; F



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Figure 3. Adsorption of laccase from T. versicolor to DOM adlayers: (a) Crystallographic structure of laccase with negative (red) and positive (blue) grids above the laccase surface representing the −1 kBT/e and +1 kBT/e isopotential surfaces, calculated for pH 5−8 and ionic strength of 10 mM from the distribution of ionizable amino acids on the laccase surface; (b) adsorption profiles of LHA to SAM−NH3+ surface and subsequent adsorption of laccase to the LHA adlayer, all at pH 5 and I = 10 mM; (c) final adsorbed masses of laccase on selected DOM adlayers (i.e., LHA, ESHA, ESFA, SRHA, and SRFA) and model surfaces (i.e., SAM−COO− and SAM−NH3+) following adsorption (solid bars) and rinsing with laccase-free solutions (dashed bars), all at pH 5 and I = 10 mM; (d) changes in the adsorbed masses of laccase on LHA adlayers at pH 5−8 (I = 10 mM) during the adsorption step and during rinsing with laccase-free solutions of the same pH and I; (e) changes in the adsorbed masses of laccase on LHA adlayers during adsorption at pH 5, followed by rinsing with laccase-free solutions at pH 5 and, subsequently, for three of the four cells, with solutions of pH 6, 7, and 8. At the end of the experiment, all surfaces were again rinsed with pH 5 solutions. A constant I = 10 mM was maintained throughout the experiments.

Following the formation of laccase monolayers, the cells were rinsed with laccase-free solutions of pH 5 and I = 10 mM and, after approximately 40 min, of pH 6, 7, and 8 in three of the four cells. Increasing the pH of the rinsing solution resulted in increased desorption of laccase from the LHA adlayers and hence weakening of laccase−LHA interactions, consistent with increasing negative surface charges on both laccase and LHA adlayers with increasing pH. Panels d and e of Figure 3, however, show that rinsing with pH 6−8 solutions resulted in more extensive desorption to smaller final adsorbed masses for laccase that was adsorbed at pH 5 (panel e) as compared to laccase that was adsorbed at pH 6−8 (panel d). This finding implies that the solution pH in the adsorption step affected the orientations in which laccase adsorbed: a significant fraction of laccase molecules that were adsorbed onto the LHA surfaces at

positively and negatively charged patches on its surface to the SAM−COO− and SAM−NH3+ surfaces, respectively. PCEA was supported by the pH dependency of laccase adsorption to and desorption from LHA adlayers (Figure 3d,e). Increasing the pH from 5 to 8 resulted in decreasing initial kinetics and final extents of laccase adsorption to LHA adlayers (Figure 3d). This pH dependency can be ascribed to increasing negative charges on the laccase and LHA surfaces and hence a decreasing number of favorable adsorption sites with increasing pH. At the same time, extensive and irreversibly adsorption of net-negatively charged laccase to like-charged LHA at pH 7 and 8 strongly suggests that laccase adsorbed via positively charged patches on its surface. Figure 3e shows the results of complementary experiments in which laccase was adsorbed to LHA at pH 5 and I = 10 mM in four parallel flow cells. G



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icochemical properties of DOM samples and adlayers, and laccase adsorption experiments. This material is available free of charge via the Internet at http://pubs.acs.org/.

pH 5 in favorable orientations desorbed upon rinsing with higher pH solutions because many of the orientations became (electrostatically) unfavorable. Conversely, laccase adsorption at pH 6−8 selected for orientations that remained favorable also during rinsing at these higher pH values.

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Corresponding Author

IMPLICATIONS This study provides direct evidence that DOM adsorption to positively charged surfaces results in nanometer thick, waterrich, yet relatively rigid, and irreversibly adsorbed adlayers, consistent with strong DOM−surface electrostatic attraction. These nanoscalar adlayer characteristics provide an explanation for the macroscopic observation that DOM adsorbed to positively charged mineral surfaces in soils and sediments is protected from degrading enzymes: compared to DOM in solution, irreversible adsorption into thin and rigid adlayers lowers the flexibility of the DOM backbone and hence the probability that proper enzyme−substrate complexes are formed. The DOM adlayers contain significant amounts of water which cause the adlayers to shrink upon drying and to have high surface polarities. We propose that the polarity characteristics of DOM adlayers are strongly dependent on the measurement scale: micrometer-sized objects, such as the drops and bubbles used in contact angle measurements, integrate over large areas and thus sense the high water contents of the adlayers. DOM adlayers may therefore be relatively polar for objects that interact with the adlayers on length scales of hundreds of nanometers to micrometers. Conversely, low molecular weight organic pollutants and small proteins interact with the DOM over much smaller areas and hence are much more sensitive to the polarity characteristics of the DOM backbone.18 Particles with sizes of several tens to hundreds of nanometers, including viruses and engineered nanoparticles, may sense intermediate adlayer polarities. This work provides direct evidence for the dominant role of electrostatics in DOM adsorption, whereas H-bond interactions, van der Waals interactions, and the hydrophobic effect had smaller energetic contributions to adsorption. Based on the effects of solution chemistry on DOM adsorption to the SAM− NH3+ surfaces, stronger modulating effects of I than pH are expected for DOM adsorption to positively charged minerals in soils and sediments. In natural systems with low to intermediate I, DOM adsorption is expected to plateau in monolayer coverages. In systems with high I such as marine sediments, DOM adsorption may proceed beyond monolayer coverages, resulting in larger amounts of adsorbed DOM than in terrestrial and freshwater aquatic systems. From a methodological perspective, this work presents a versatile experimental approach using SAMs to systematically study DOM adsorption to various surfaces as a function of solution chemistry. Moreover, the use of QCM-D allows determination of the viscoelastic properties of DOM adlayers that are not accessible by in situ optical techniques. We propose that future studies on the interactions of (bio)macromolecules and (nano)particles with DOM adlayers employ the approach described herein instead of using polyelectrolyte polymers to form DOM adlayers.

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AUTHOR INFORMATION

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the Swiss National Science Foundation, SINERGIA Project CRSI22_127568, for funding, Prof. Nicholas Spencer, Cathrein Hückstädt, Olof Sterner, and Adrienne Nelson for access to and help with the ellipsometry and contact angle instruments, and Melanie Münch for help with selected QCMD experiments.

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REFERENCES

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S Supporting Information *

Additional information and data on the preparation of solutions, sensor cleaning, ellipsometry measurements, physH



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Dissolved Organic Matter Adsorption to Model Surfaces: Adlayer

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