Article pubs.acs.org/Langmuir

Interactions between Rotavirus and Natural Organic Matter Isolates with Different Physicochemical Characteristics Leonardo Gutierrez and Thanh H. Nguyen* Department of Civil and Environmental Engineering, Safe Global Water Institute, University of Illinois at Urbana−Champaign, Urbana, Illinois 61801, United States S Supporting Information *

ABSTRACT: Interaction forces between rotavirus and Suwanee River natural organic matter (SRNOM) or Colorado River NOM (CRNOM) were studied by atomic force microscopy (AFM) in NaCl solutions and at unadjusted pH (5.7−5.9). Compared to CRNOM, SRNOM has more aromatic carbon and phenolic/carboxylic functional groups. CRNOM is characterized with aliphatic structure and considerable presence of polysaccharide moieties rich in hydroxyl functional groups. Strong repulsive forces were observed between rotavirus and silica or mica or SRNOM. The interaction decay length derived from the approaching curves for these systems involving rotavirus in high ionic strength solution was significantly higher than the theoretical Debye length. While no adhesion was observed for rotavirus and SRNOM, attraction was observed between CRNOM and rotavirus during approach and adhesion during retraction. Moreover, these adhesion forces decreased with increasing ionic strength. Interactions due to ionic hydrogen bonding between deprotonated carboxyl groups on rotavirus and hydroxyl functional groups on CRNOM were suggested as the dominant interaction mechanisms between rotavirus and CRNOM.



NOM interactions with viruses have been studied in field, column, and batch experiments. While electrostatic forces were proposed to dominate the interaction between viruses and mineral surfaces, NOM has been suggested to hinder the deposition of rotavirus, bacteriophages PRD1, λ, MS2, and ϕX174 to mineral surfaces due to competition for adsorption sites.9−12 Hydrophobicity was also proposed to control the interaction between PRD1 or MS2 and NOM.13 Steric interactions arising due to the complex polymeric properties of NOM have also been suggested to explain interactions observed for SRNOM and rotavirus or MS2 bacteriophage.14,15 These studies have also reported stronger interaction of MS2 and rotavirus with NOM in the presence of divalent cations compared to those in the presence of monovalent cations due to complexation of divalent cations with deprotonated carboxylic groups on both NOM and viruses.14,16,17 From these studies it has been clearly observed that, along with solution chemistry, the interactions between NOM and viruses were highly dependent on the characteristics of NOM and viruses. Nevertheless, to the best of our knowledge, there has been no research regarding direct measurement of intermolecular forces to elucidate the very specific dominant interaction

INTRODUCTION

Natural organic matter (NOM) is a highly heterogeneous mixture of decayed organic compounds and functionalities ever-present in soils and natural and engineered water systems. NOM is considered a major constituent of the carbon cycle, and its essential bio/geochemical role in every aquatic environment is undeniable.1,2 However, the structural and chemical characteristics of NOM are highly dependent on their origin.3 Previous characterization studies have shown significant differences (e.g., aromaticity/aliphaticity, elemental composition, molar ratios, and major functional groups) between NOM isolates collected from a variety of natural water sources.4 Results from previous extensive NOM characterization studies indicate that NOM has highly heterogeneous characteristics. Although NOM could be classified into humic and nonhumic substances, in reality NOM isolates often contain a mixture of those.5 Humic substances have a high content of aromatic/ phenolic carbon, high ratios of C/H, C/O, and C/N, and carboxyl and phenol as main functional groups.4,6 Nonhumic substances are characterized by a high content of nitrogen and aliphatic carbon and a low content of aromatic/phenolic carbon. In addition, polysaccharides, amides, bases, and alkyl alcohols comprise strongly hydrophilic NOM species.4,7,8 Rigorous and detailed characterization of NOM has played a central role in understanding NOM interaction with other ubiquitous components in natural/engineered water systems.1,4 © 2013 American Chemical Society

Received: July 29, 2013 Revised: October 15, 2013 Published: October 23, 2013 14460

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filament current 15 mA) at an operating pressure of 20 for every solution condition) were described by log-normal distribution.38 The minimum detectable adhesion force included in this statistical analysis was defined as 0.05 nN (i.e., detection limit), as previously suggested.38 Adhesion forces of magnitude lower than 0.05 nN were taken into account for discussion but not quantified. The mean (μ) and variance (σ) were determined by fitting the measured adhesion forces, or adhesion distance, or adhesion energy to log-normal density function. Surfaces and Probe Preparation for Atomic Force Microscopy Experiments. Silica surfaces was obtained from Q-Sense (Sweden) and cleaned following the procedure previously described.14 Briefly, silica surfaces of approximately 0.7 cm2 in area were first immersed in 2% Hellmanex (Hellma Analytics, Müllheim, Germany) solution for 30 min and subsequently rinsed in excess in DI water. Then, 400 μL of 98% sulfuric acid with 30 g/L nochromix solution was pipetted on top of the silica surfaces and removed after 24 h of exposure. The silica surfaces were then rinsed in excess with DI water, dried with ultrapure N2, and finally oxidized in an ozone/UV chamber



RESULTS AND DISCUSSION Electrophoretic Mobility (EPM) Analysis for NOM Isolates. The EPM of silica particles was negative at the whole range of ionic strength tested (Figure 1) and became less negative with increasing salt in solution (from −2.3 ± 0.3 to −0.3 ± 0.1 μm cmV−1 s−1 at 1 mM NaCl and 100 mM NaCl,

Figure 1. EPM of (a) bare silica particles (1.6 μm), CRNOM-coated silica particles, SRNOM-coated silica particles, and (b) PLL-coated silica particles as a function of ionic strength (ambient pH, 25 °C). The different EPM magnitudes obtained for SRNOM and CRNOM were indicative of their dissimilar surface characteristics. Shown are average and standard deviation of at least three replicates. 14462

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respectively). As reported in previous investigations,30 PLL reversed the charge of silica particles. PLL-coated silica particles became less positively charged with increasing ionic strength (from 4.5 ± 0.1 to 2.2 ± 0.1 μm cmV−1 s−1 at 1 mM NaCl and 100 mM NaCl, respectively). SRNOM or CRNOM adsorbed on PLL-coated silica particles caused another charge reversal. The EPM of NOM-coated particles was negative at the whole range tested and also decreased with increasing ionic strength (from −2.7 ± 0.3 at 1 mM NaCl to −0.7 ± 0.1 μm cmV−1 s−1 at 100 mM NaCl for SRNOM, and from −1.7 ± 0.1 at 1 mM NaCl to −0.5 ± 0.2 μm cmV−1 s−1 at 100 mM NaCl for CRNOM) as previously observed for other charged colloids.27,39,40 This decrease in EPM was due to compression of the diffuse double layer associated with increased concentration of Na+ ions in solution. Na+ ions have been suggested to only weakly interact with NOM molecules via outer-sphere association.41 At the pH of the experiments, the charge displayed by both isolates is a product of ionized carboxylate groups as a dominant acidic functional group.41 The more negative EPM exhibited by SRNOM would be the result of a larger presence of deprotonated carboxylate groups on its structure. The EPM of both isolates did not seem to reach a finite lower limit associated with limited charge screening at high salt concentration in solution, as observed in previous studies.27,42 NOM-Coating Completeness of Silica Surfaces. Control experiments were first conducted to assess NOM-coating completeness of the silica surfaces following protocols previously detailed.14 A SiNi tip of approximately 20 nm in radius of curvature was used instead of a 1 μm colloidal probe for this control to obtain higher spatial resolution data. At pH 8.3 in 1 mM NaHCO3 solution, repulsion forces were detected when the SiNi tip was approaching the silica surface, indicating electrostatic repulsion originated by the negative charge of the tip and the silica surface. Interaction force decay lengths of 9.1 ± 0.4 nm (n = 17), calculated based on the approaching curves, closely followed the theoretical Debye length of 9.6 nm at 1 mM ionic strength, suggesting the dominant role of electrostatic forces. Attractive forces were detected when the negatively charged SiNi tip was approaching the positively charged PLL-coated silica surface; adhesion was detected when the tip was retracting from the PLL-coated surface. Thus, the silica surface was coated by PLL relative to the length-scale of the radius of the SiNi tip of approximately 20 nm. Finally, repulsive forces were detected between the SiNi tip and SRNOM-coated silica surfaces, indicating successful modification of the PLL-coated silica surface by the adsorbed NOM isolate relative to the radius of curvature of the SiNi tip. Interaction Forces between Rotavirus and Mica or Silica Surface. Interaction forces between silica probe and mica surface were first measured as a control experiment to validate the experimental setup. The measured interaction decay length (i.e., 9.2 ± 0.2 nm, 3.2 ± 0.2 nm, and 1.5 ± 0.1 nm, in 1, 10, and 100 mM NaCl solutions, respectively, number of analyzed curves n = 10 per solution condition) was in good agreement with the theoretical Debye length (i.e., 9.6 nm, 3.0 nm, and 0.96 nm, in 1, 10, and 100 mM NaCl solutions, respectively). This agreement between the measured interaction decay length and the theoretical Debye length suggest an increased charge screening at high ionic strength, controlling electrostatic repulsion between silica probe and mica surface (Figure 2). On the other hand, the interaction force decay lengths calculated from force profiles collected when rotavirus-

Figure 2. Interaction force decay length determined between rotavirus-coated silica colloidal probe and mica surface or silica surface or SRNOM-coated silica surface or SAM-COOH (n = 20, 20, 25, and 25, per solution condition, respectively), and between mica surface and silica colloidal probe (n = 10 per solution condition). The decay lengths were calculated from the approaching curve profiles at a 500 nm/s rate (pH 5.7, 25 °C). Error bars represent standard deviations.

coated probes approached mica or silica surfaces showed no significant statistical difference (two-tailed t test, α = 0.05) at all the ionic strengths tested (1, 10, and 100 mM NaCl, n = 20 per solution condition) (Figure 2). In 1 mM NaCl solution, these decay lengths closely followed the predicted Debye length (i.e., 8.4 ± 0.4 nm and 7.9 ± 0.5 nm for mica and silica surfaces, respectively, versus 9.6 nm as the theoretical Debye length). In 10 mM and 100 mM solutions, however, the observed decay length was significantly larger than the theoretical Debye length (Figure 2). Similar deviation observed between rotavirus-coated silica probe and silica surface has been reported previously.14 This deviation from the theoretical Debye length, clearly originating from rotavirus, indicates the presence of an additional interaction force in this system besides electrostatic double-layer interaction for perfectly smooth hard surfaces.76,77 If electrostatic interaction is the only dominant force, increasing ionic strength is expected to compress the double layer, leading to a smaller decay length equal to the theoretical Debye length. The observed higher decay length for rotavirus compared to the theoretical Debye length expected at 100 mM ionic strength may be due to steric interaction that prevents the rotavirus particles from approaching the surface. Similar steric interaction has already been reported for bacteria or oocysts.35,40,43 Interaction Forces between Rotavirus and SRNOMCoated Silica Surface. Repulsive forces were recorded between rotavirus and SRNOM at the entire ionic strength range tested (i.e., 1, 10, and 100 mM NaCl solutions). The interaction force decay length calculated between rotavirus and SRNOM (i.e., 8.7 ± 1.9 nm) (Figure 3) closely followed the theoretical Debye length at 1 mM NaCl solutions. However, the decay length was significantly larger than the predicted Debye length at 10 and 100 mM NaCl solutions (i.e., 7.5 ± 1.6 nm and 5.6 ± 1.5 nm, respectively, number of analyzed curves n = 25 for every solution condition). At 10 mM NaCl, the difference between the decay length values was not significant for rotavirus−SRNOM and rotavirus−mica (7.5 ± 1.6 nm vs 6.0 ± 0.5 nm, two-tailed t test, α = 0.05). The higher standard deviation obtained for rotavirus on the SRNOM surface is probably due to the heterogeneity of both rotavirus and SRNOM surfaces. There was no significant statistical difference (two-tailed t test, α = 0.05) between the decay lengths obtained 14463

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the scope of this study to identify the origin of this steric and/ or hydration interaction. Interaction Forces between Rotavirus and the CRNOM-Coated Silica Surface. The interaction forces between rotavirus and CRNOM were significantly different from those exhibited between rotavirus and SRNOM. Specifically, at every ionic strength tested from 1 mM to 100 mM, not only were repulsive forces absent, but the AFM cantilever was observed to “jump” onto the surface because of the presence of strong attractive forces exceeding the cantilever spring constant (Figure 3a). This phenomenon is referred to as jump-in to contact instability in AFM measurement. Because of the heterogeneity of both CRNOM and rotavirus, 20 force curves at different locations were collected. The magnitudes of the forces of the jump-in to contact between CRNOM and rotavirus were measured and statistically analyzed. Probability density function fitted to log-normal distribution was used to describe all collected interaction forces (Figure 3b−d). The interaction forces of the jump-in to contact decreased with increasing ionic strength. Specifically, the mean and variance values were 0.4 nN and 0.3, 0.2 nN and 0.3, and 0.1 nN and 0.5 for 1, 10, and 100 mM NaCl, respectively. In addition to jump-in to contact observed with the approaching force curves, adhesion forces were detected for the retracting force curves (Figure 4a). The maximum adhesion

Figure 3. (a) Representative approaching curves between rotaviruscoated silica colloidal probe and CRNOM-coated silica. Probability density functions (log-normal fit) describing the interaction force distributions between rotavirus and CRNOM during approach at (b) 1 mM NaCl, (c) 10 mM NaCl, and (d) 100 mM NaCl solutions (n = 20 per solution condition). The mean (μ) and variance (σ) values obtained by fitting to the log-normal distribution function are also shown.

from the force measurement between rotavirus-coated probe and silica or mica or SRNOM at 100 mM NaCl solutions. Interaction decay lengths higher than the theoretical Debye length and decay length independent of ionic strength observed for rotavirus approaching mica, bare silica, or the SRNOMcoated silica surface were similar to the observation reported for Cryptosporidium oocyst interaction with a silica surface.43 Steric interaction due to the presence of a weakly charged carbohydrate outer layer of the oocysts was proposed to explain the detection of a long decay length for oocysts.43 No adhesion forces were recorded between rotavirus and SRNOM even at high ionic strength (e.g., 100 mM NaCl solution). Furthermore, the retracting force versus distance profiles closely mirrored approaching force curves, as similarly reported in a previous investigation for rotavirus and SRNOM.14 The strong repulsive forces observed between rotavirus and SRNOM and the absence of adhesion forces even at high ionic strength suggest the role of nonelectrostatic interactions. This absence of strong adhesion between rotavirus and SRNOM has been previously observed during deposition and aggregation kinetics experiments (i.e., using quartz crystal microbalance and time-resolved dynamic light scattering techniques, respectively).14 Previous studies have attributed NOM strong repulsive forces to the steric stabilization of nanoparticles coated with NOM.44−46 Long range repulsive forces closely following exponential decays observed for rotavirus and SRNOM have been reported previously between surface-grafted poly(ethylene glycol) polymers and the AFM tip.47 Strong repulsive interaction at high salt concentration was already observed for protein molecules and was attributed to steric and hydration forces.48−50 Because the capsid of rotavirus is essentially made of proteins,51 we also suggest that the strong repulsion force independent of interaction decay length with ionic strength has a steric and/or hydration nature. It is beyond

Figure 4. (a) Representative retracting curves between the rotaviruscoated silica colloidal probe and the CRNOM-coated silica surface measured at 1, 10, and 100 mM NaCl solutions and at pH 5.7. (b and c). Probability density functions (log-normal fit) describing maximum adhesion force distributions between rotavirus and CRNOM during retracting at (b) 1 mM NaCl, (c) 10 mM NaCl, and (d) 100 mM NaCl solutions (n = 20 per solution condition). The mean (μ) and variance (σ) values obtained by fitting to the log-normal distribution function are also shown.

forces between CRNOM and rotavirus, determined based on the maximum force measured before total detachment between the rotavirus-coated probe and the CRNOM-coated silica surface, were described with probability density functions fitted to log-normal distributions (Figure 4b−d). A decrease in maximum adhesion forces with increasing ionic strength was observed. Specifically, the mean and variance values were 3.3 nN and 0.2, 2.2 nN and 0.1, and 1.3 nN and 0.3 at 1, 10, and 14464

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100 mM NaCl solutions, respectively. Similarly, long adhesion distances were recorded at every single retracting curve recorded, and these distances also decreased with increasing ionic strength. Specifically, the mean and variance values were 209 nm and 0.3, 148 nm and 0.8, and 142 nm and 0.6 at 1, 10, and 100 mM NaCl solutions, respectively (Figure 2Sa−c, Supporting Information). Note that these distances were longer than the diameter of a rotavirus particle or a CRNOM molecule, suggesting a possible detachment (pull-off) occurring at the substrate or AFM probe, as suggested in previous studies.14,52 In addition, multiple detachments were also observed, indicating multiple discrete adsorption sites occurring between the CRNOM-coated surface and the rotavirus-coated colloidal probe.53 Similar to the decrease of maximum adhesion forces and maximum adhesion distances with increasing ionic strength, calculated adhesion energies between CRNOM and rotavirus also decreased with increasing ion concentration in solution. Specifically, the mean and variance values were 308 × 10−18 J and 0.78, 107 × 10−18 J and 0.71, and 90 × 10−18 J and 0.01 at 1, 10, and 100 mM NaCl solutions, respectively (Figure 3Sa−c, Supporting Information). Evidently, the dominant interaction mechanism between CRNOM and rotavirus in NaCl solutions was inversely correlated to the addition of ions in solution, and this high affinity was clearly observed for both approaching and retracting force curves. The observed strong adhesion between rotavirus and CRNOM and the strong repulsion observed between SRNOM and rotavirus may be due to the dominant hydroxyl and carboxylate groups present in CRNOM and SRNOM isolates, respectively. Further investigation on rotavirus interaction with surfaces containing either carboxylate or hydroxyl groups is described below. Interactions between Rotavirus and Self-Assembled Monolayers of 16-Mercapto-1-hexadecanol (SAM-OH) or 16-Mercaptohexadecanoic Acid (SAM-COOH). The chemical structures of SAM-COOH and SAM-OH were confirmed by surface chemical analysis by XPS. The C 1S spectrum of SAM-COOH (Figure 4Sa, Supporting Information) was fitted into three components. The peak at 285 eV originates from aliphatic carbon (C−C/C−H), which is the major carbon species detected. The shoulder centered at 289.3 eV indicates carboxylic carbon (OC−O), while the shoulder at 286.5 eV corresponds to C−COO.54 The presence of oxygen is indicated by the peak at 532.5 eV (Figure 4Sb, Supporting Information). The O 1S spectrum was fitted into two components found at 531.9 eV (CO) and 533.3 eV (C− O).55,56 The peak of the carboxylic carbon was absent in the SAM-OH spectrum (Figure 5Sa, Supporting Information), while the peak at 286.5 eV corresponds to hydroxyl.57 Finally, the O S1 spectrum was fitted to one peak centered at 532.8 eV, which is attributed to the oxygen from the hydroxyl group (Figure 5Sb, Supporting Information).58 Contact angles measured between water (probe solution) and the previously cleaned gold (Au) surface, Au SAM-OH, and Au SAM-COOH indicate a modification of the originally hydrophobic gold surface (Table 2S, Supporting Information). Repulsion forces following an exponential decay were observed between the rotavirus-coated colloidal probe and SAM-COOH (Figure 5a) in approaching force profiles. These repulsive forces increased with decreasing distance and were evident even at high ionic strength (100 mM NaCl solutions). The carboxyl group on SAM-COOH is expected to be deprotonated at the unadjusted pH of the experiments (5.7−

Figure 5. (a) Model approaching curves for rotavirus (RV)-coated colloidal probe and 16-mercapto-1-hexadecanol SAM (SAM OH) or 16-mercaptohexadecanoic acid SAM (SAM COOH). Probability density functions describing maximum adhesion force distributions between rotavirus and SAM-OH during retracting at (b) 1 mM NaCl, (c) 10 mM NaCl, and (d) 100 mM NaCl solutions (n = 25 per solution condition). The mean (μ) and variance (σ) values obtained by fitting to the log-normal distribution function are also shown.

5.9). Rotavirus was negatively charged under the same conditions (Figure 1a). Therefore, electrostatics is expected to influence the interactions between rotavirus and SAMCOOH. However, the interaction force decay lengths determined from the force profiles recorded when rotavirus approached SAM-COOH in 100 mM ionic strength solution were higher than the theoretical Debye length (Figure 2). When the rotavirus-coated probe was retracting from the SAMCOOH surface, no significant adhesion was observed (Figure 6Sa−c, Supporting Information). Because the SAM-COOH surface is chemically homogeneous, in addition to electrostatic interaction, steric and/or hydration interaction may be responsible for the observed large decay length for rotavirus on this SAM-COOH surface. The interaction between rotavirus and SAM-OH significantly differed from SAM-COOH (Figure 5a) but closely resembled that of rotavirus−CRNOM (Figure 3a). A jump-in to contact was observed for all recorded approaching force curves (n = 25 per solution condition) (Figure 5a; Figure 7Sa−c, Supporting Information). High adhesion forces were evident from the retracting force curve recorded for experiments conducted at 1 mM NaCl. In addition, the magnitude of the adhesion force decreased with increasing ionic strength, similar to the observation of rotavirus interaction with CRNOM (Figure 5b−d). We suggest that this strong adhesion of rotavirus to SAM-OH and CRNOM is due to the ionic hydrogen bonding formed between hydroxyl and carboxylates, as illustrated in Figure 6. The deprotonated carboxylate functional groups present on the rotavirus surface at pH 5.7−5.9 form hydrogen bonding with the OH groups of CRNOM or SAM-OH. Similar strong adhesion due to ionic hydrogen bonding has been studied by chemical force microscopy using functionalized SAM.25,59 Ionic hydrogen bonds among ions and molecules have been shown to play an essential role in processes involving biomolecules.60 14465

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CONCLUSION Results from this investigation indicate the importance of NOM physicochemical characteristics during interactions with rotavirus. Specifically, strong repulsion likely due to electrostatic, steric, and hydration forces was observed for rotavirus interaction with carboxylate-functionalized thiols SAM and SRNOM, which contain phenolic and carboxylic functional groups. On the other hand, deprotonated carboxyl groups on rotavirus with high affinity to hydroxyl groups on CRNOM and hydroxyl-functionalized SAM through ionic hydrogen bonding explained the strong adhesion observed between rotavirus. In a natural aquatic environment, the structural and chemical characteristics of NOM are highly dependent on their origins3,4 and the presence of other components such as multivalent cations.17,41 Rotavirus interactions with NOM in various aquatic systems might differ significantly. Thus, the results presented here suggested that the nature of the dominant interaction mechanisms between NOM and viruses would be also highly dependent on the surface properties (i.e., protein capsid) of the specific virus selected. Other properties, such as hydrophobicity and molecular weight, may also influence virus fate and transport. On the basis of this study, predictive models of the fate and transport of viruses in aquatic systems should consider the chemical functional groups of NOM and of viruses. ASSOCIATED CONTENT

S Supporting Information *

Additional information as noted in the text. This material is available free of charge via the Internet at http://pubs.acs.org.



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Figure 6. Schematic of ionic hydrogen bonding occurring between deprotonated carboxyl groups on rotavirus and hydroxyl functional groups on CRNOM or SAM-OH.



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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This work was partially supported by Safe Global Water Institute, and the USDA NIFA grant 2013-67017-21221. We also acknowledge Dr. Jean-Philippe Croue, Dr. Scott McLaren, Dr. Rick Haasch, Youngsung Byun, Hanting Wang, and the Frederick Seitz Materials Research Laboratory. We also thank Dr. Howard Fairbrother from Johns Hopkins University for advice on XPS experiments. 14466

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dx.doi.org/10.1021/la402893b | Langmuir 2013, 29, 14460−14468

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dx.doi.org/10.1021/la402893b | Langmuir 2013, 29, 14460−14468

Interactions between rotavirus and natural organic matter isolates with different physicochemical characteristics.

Interaction forces between rotavirus and Suwanee River natural organic matter (SRNOM) or Colorado River NOM (CRNOM) were studied by atomic force micro...
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