Ammonia clathrate as new phases for Titan, , and other planetary systems

Kyuchul Shina, Rajnish Kumarb, Konstantin A. Udachina, Saman Alavia, and John A. Ripmeestera,1

aSteacie Institute for Molecular Sciences, National Research Council of Canada, Ottawa, ON, Canada K1A 0R6; and bNational Chemical Laboratory, Council of Scientific and Industrial Research, Pune 411008, India

Edited by Mark H. Thiemens, University of California San Diego, La Jolla, CA, and approved July 26, 2012 (received for review April 12, 2012)

There is interest in the role of ammonia on ’s moons Titan Results and Enceladus as the presence of , , and ammonia As a first step in this study we show that in the presence of other under temperature and pressure conditions of the surface and in- clathrate forming substances, ammonia indeed can be terior make these moons rich environments for the study of phases incorporated in cages within the clathrate lattice. Incorporation formed by these materials. Ammonia is known to form solid hemi-, of ammonia in a phase was accomplished by mono-, and dihydrate phases under conditions consistent freezing a solution of the well known clathrate hydrate former with the surface of Titan and Enceladus, but has also been assigned tetrahydrofuran (THF) and approximately 5% aqueous ammonia a role as water- antifreeze and methane hydrate inhibitor which with an approximate THF:water mole ratio of 1∶17 at −10 °C. is thought to contribute to the outgassing of formed were harvested after a few days and those suita- hydrates into these moons’ atmospheres. Here we show, through ble for diffraction were identified and mounted on a diffract- direct synthesis from solution and vapor deposition experiments ometer at low temperatures. The above experimental conditions under conditions consistent with extraterrestrial planetary atmo- can be compared with those in the study of Dong et al. (15, 16) spheres, that ammonia forms clathrate hydrates and participates who used THF:water ratios of about 1∶63 with up to 5% ammo- synergistically in clathrate hydrate formation in the presence of nia to study methane hydrate formation in the presence of methane at low temperatures. The binary structure II tetra- ammonia. In their experiments, Dong et al. (15, 16) did not use

hydrofuran + ammonia, structure I ammonia, and binary structure sufficient THF to lead to the direct formation of the binary CHEMISTRY I ammonia + methane clathrate hydrate phases synthesized have THF þ NH3 clathrate hydrate and ammonia hydrate formation been characterized by X-ray diffraction, molecular dynamics simu- was not observed. lation, and Raman spectroscopy methods. Structural data were recorded at 100 K (see Materials and Methods). The structure was shown to be the usual cubic structure ice ∣ single crystal X-ray diffraction ∣ bonding ∣ II (sII) clathrate hydrate (28), space group Fd-3m with a unit cell hydrate inhibitors ∣ ethane edge of 1.71413(6) nm. The THF occupy the large cages, as expected, and 39% of the small cages are filled with am- mmonia has long been seen as a key species in extraterres- monia molecules (Fig. 1). This measured small cage occupancy is Atrial space, both interstellar and on outer , moons, likely to be a function of the starting composition. Whether small and and the interplay of ammonia, methane, and water cages could be completely filled with a more ammonia-rich liquid has been the subject of a considerable number of studies and is uncertain and should be studied separately. One of the water speculation (1–8). The main role assigned to ammonia has been molecules in the small cages which encapsulate the ammonia guests has moved out of its normal position, 0.118 nm inward into that of an antifreeze for ice and clathrate hydrate formation, ⋯ modifying the stability region of the solid ice and methane clath- the small cage thus forming H2O H-NH2 hydrogen bonds (0.267–0.272 nm) with NH3 (as suggested by hydrogen positions rate hydrate phases as a thermodynamic inhibitor (2, 5, 9). How- ⋯ ever, ammonia is a methane-sized , thus based on size on the ammonia guest). The formation of HOH NH3 hydrogen alone it has the potential for being a suitable guest for clathrate bonding could also lead to this water displacement. This displace- ment breaks the of this water molecule with hydrate cages. Issues that may have prevented ammonia from ⋯ being considered as a suitable clathrate guest molecule include another water from an adjacent large (or small) cage (O O dis- tance 0.393 nm), thus distorting both large and small cages. The the notion that guest species need to be hydrophobic in order to equivalent O⋯O distance in the undistorted edges of the water be incorporated into clathrates, and the observation of a number polyhedra is 0.279 nm. It should be noted that the minimum heavy of stoichiometric nonclathrate phases of ammonia and water atom N⋯O distance in the clathrate hydrate is smaller than in the obtained upon cooling aqueous ammonia solutions (2). Previous ammonia hydrates, where the more uniform local environment of experimental work on the water-ammonia and water-methane- the NH3 molecule results in N⋯O distances of 0.305 to 0.330 nm. ammonia systems had not shown evidence for the enclathration Because structural evidence for the mixed THF þ NH3 sII of ammonia (5, 10–19). Close inspection, however, shows that the hydrate showed that it is possible to incorporate ammonia into low pressure ammonia dihydrate (18) and the high pressure phase II of ammonia monohydrate (19) have structural features in com- mon with canonical clathrate and semiclathrate structures. Author Contributions: R.K., K.S., and J.A.R. performed the vapor deposition experiments; Recent structural analysis and molecular simulations have K.S., K.A.U., and J.A.R. did the powder and single-crystal XRD experiments; S.A., K.S., and shown that some guest molecules which form strong hydrogen J.A.R. performed the molecular dynamics simulations; and J.A.R., S.A., and K.S. wrote the manuscript. bonds with the water framework of the clathrate hydrate lattice The authors declare no conflict of interest. may nonetheless produce stable phases (20–23). It is therefore reasonable to consider that ammonia has potential as a clathrate This article is a PNAS Direct Submission. guest molecule. Furthermore, previous experimental and com- Data deposition: The single-crystal XRD structure of the binary tetrahydrofuran and ammonia structure II clathrate hydrate has been deposited in the Cambridge Structural putational studies have shown that in the gas phase, water forms Database, Cambridge Crystallographic Data Centre, Cambridge CB2 1EZ, United Kingdom dodecahedral cages around ammonia and ammonium ions. (CSD reference no. 864781). These structures may be indicative of a geometric tendency to- 1To whom correspondence should be addressed. E-mail: [email protected]. wards clathrate hydrate structures for the ammonia and ammo- This article contains supporting information online at www.pnas.org/lookup/suppl/ nium molecules (24–27). doi:10.1073/pnas.1205820109/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1205820109 PNAS Early Edition ∣ 1of6 Downloaded by guest on September 29, 2021 Fig. 1. The large and small cages of the cubic structure II THF-ammonia binary clathrate hydrate from single crystal X-ray diffraction. The ammonia guest has moved a water molecule out of its normal position by pulling it into the small cavity by forming a H2N-H⋯OH2 or H3N⋯HOH hydrogen bond.

clathrate cages, attempts were made to form clathrate hydrates with only ammonia as guest. Pure ammonia clathrate hydrate synthesis cannot be done by simply cooling aqueous ammonia solutions, as a variety of stoichiometric hydrates of ammonia are known to form preferentially (2, 11, 18, 19). Other ways of form- ing clathrate hydrates include vapor deposition of water at low temperatures to yield , followed by exposure of the ice to a pressure of guest gas and annealing (29), or vapor code- position of water and the potential guest material at low tempera- tures, again, followed by annealing (23, 30, 31). It has been shown that below approximately 140 K ice surfaces are relatively inert unless strong hydrogen-bond donors or acceptors are present. For example, molecules normally hydrolyzed by water such as formal- dehyde will not do so when in contact with at low tempera- ture and will template clathrate hydrate lattices when amorphous ice is annealed (30). Following the latter procedure, described in detail in Materials and Methods, vapor codeposits of ammonia and water were pre- pared at T < 20 K. The codeposited crystals were harvested at 77 K and kept in liquid until appropriate measurements Fig. 2. PXRD patterns of NH3 and H2O co-deposition sample (A) recorded at could be made. A portion of each amorphous product was 100, 140, and 150 K; (B) expansion of the pattern at 150 K. Lattice parameters mounted in a low temperature cell on a powder X-ray diffract- (150 K) are: a ¼ 0.4527ð1Þ nm, b ¼ 0.5586ð1Þ nm, c ¼ 0.9767ð3Þ nm for am- 2 2 2 ¼ 0 4496ð1Þ ¼ ometer and the samples annealed stepwise, increasing tempera- monia monohydrate (space group: P 1 1 1); a . nm and c 0.7339ð1Þ nm for (space group P63∕mmc); a ¼ 1.1818ð2Þ nm for sI ture from approximately 100 K. Fig. 2 shows the transformation ¼ 0 8404ð2Þ ¼ A ammonia clathrate hydrate (space group Pm-3n); a . nm, b of the amorphous deposit upon annealing. Fig. 2 shows the pow- 0.8441ð3Þ nm, and c ¼ 5.345ð1Þ nm for ammonia hemihydrate (space group der X-ray diffraction (PXRD) pattern for amorphous ice with Pbnm); and a ¼ 0.7125ð1Þ nm for ammonia dihydrate (space group P213). traces of ices Ic and Ih at 100 K. At 140 K, the amorphous ice has largely transformed to ices Ic and Ih plus a number of other as well as cubic sI [Pm-3n, a ¼ 1.1847ð8Þ nm] and cubic sII clath- crystalline phases (the Bragg positions for Ic are omitted). These rate hydrates [Fd-3m, a ¼ 1.7161ð9Þ nm]. To observe both com- reflections continue to develop with increase of temperature to mon cubic clathrate hydrate structures is surprising. Structure I 150 K. The inset (Fig. 2B) shows a vertical expansion of the 150 K is the usual clathrate that forms for methane at low pressures pattern. For each pattern the profiles are matched to those of although metastable sII methane hydrate has been observed as known crystalline phases, including the stoichiometric ammonia well (30). A blank run for a vapor codeposit of water and methane hydrates (hemi-, mono-, and dihydrates), hexagonal ice Ih, and but without ammonia did not reveal any clathrate hydrate under clathrate hydrates. Eight reflections (shown in Fig. 2) can be as- similar conditions of annealing (Fig. S1). Further annealing of signed to the cubic structure I (sI) ammonia clathrate hydrate and the three-component codeposit at 180 K showed (Fig. 3A) that indexed to be consistent with sI clathrate hydrate, space group the sII clathrate hydrate pattern had largely disappeared, and Pm-3n, with unit cell edge 1.1818(2) nm at 150 K. reflections for the stoichiometric ammonia hydrates were absent. The interactions of ammonia with methane clathrate hydrate The transformation from mixed sI and sII hydrates to sI hydrate are also considered to be important in determining the phase was confirmed by observing methane C-H symmetric stretch equilibria on Titan and Enceladus. Several vapor deposits of frequencies around 2;905 cm−1 by Raman spectroscopy (32) methane, ammonia, and water were prepared as described in (Fig. S2). At low temperature, the deposited methane peak Materials and Methods and annealing of the vapor codeposits was appeared at 2;908 cm−1, which is close to the Raman shift of followed by PXRD. Fig. 3A shows the PXRD pattern at 112 K, dissolved methane in water (33). This peak splits into a doublet indicating the material to be mainly amorphous except for some at 160 K; one peak at 2;903 cm−1 representing the methane in crystalline Ih. At 143 K (Fig. 3A, second trace) most of the pat- the large cages and the second at 2;914 cm−1 representing tern for the amorphous deposit has transformed into plus methane in the small cages. As temperature increases, the ratio other crystalline phases that upon closer inspection suggested the of methane in the large cages to that of the guest in the small presence of both cubic sI and sII clathrate hydrates. At 160 K, this cages increases, which implies the transformation to sI phase pattern is well developed and a vertically expanded detail is given (six large cages to two small cages) which has a greater proportion in Fig. 3B. Profile matching for each powder pattern shows that a of large cages than sII (8 large cages to 16 small cages). Similar good fit is obtained by considering the presence of ices Ic and Ih, enhanced processes of CO2 clathrate hydrate formation on ice

2of6 ∣ www.pnas.org/cgi/doi/10.1073/pnas.1205820109 Shin et al. Downloaded by guest on September 29, 2021 up to 200 K and did not show signs of decomposition and cage collapse. In the molecular simulations of the sI and sII pure ammonia hydrate phases, we observe hydrogen bonding between the ammonia guest molecules and the water molecules in both the small and large clathrate hydrate cages. Cases where ammonia is the hydrogen donor (H2N-H⋯OH2) and hydrogen acceptor (H3N⋯H-OH) are both common but the latter is more frequent (Figs. S3 and S4). On the other hand, in the binary sII hydrate phases with THF or methane in the large cages, ammonia showed either no hydrogen bonding or only a small probability for hy- drogen bond formation with water molecules of the small cages (see Figs. S5 and S6). From integrating the hydrogen bonding peak in the radial distribution functions (RDF), we calculated the probability of hydrogen bonding, p, in the pure NH3 sI, sII, and binary NH3 þ CH4 sII clathrate hydrates for ammonia molecules and the results are given in Table 1. Peaks in the RDF with H2N-H⋯OH2 or H3N⋯H-OH distances less than 0.25 nm were assigned to hydrogen bonding. The areas underneath the hydrogen bond peaks in the RDF give a measure of the hydrogen bond probability (see Materials and Methods). The probability of hydrogen bonding increases with temperature, which shows that the ammonia-water hydrogen bonding in the clathrate hydrates is endothermic. The temperature dependence of the hydrogen bonding probability is evaluated using the van’t Hoff plot of ln K [where K ¼ p∕ð1 − pÞ] as a function of 1∕T (Fig. S7). The slopes of the linear plots are used to determine the enthal- pies of hydrogen bond formation for ammonia in the different CHEMISTRY environments which are also given in Table 1. The formation of hydrogen bonds in the sII clathrate hydrate is less endothermic and the more facile formation of these bonds may destabilize the sII clathrate hydrate water lattice to a greater extent than the sI case. Sample hydrogen bonded configurations of the ammonia guests in the large and small cages of the sI and sII clathrate hydrates are shown in Fig. 4. Hydrogen bond configurations Fig. 3. PXRD patterns of NH3,CH4, and H2O co-deposition sample (A)re- with ammonia acting as the proton donor and the proton accep- corded at 112, 143, 160, and 180 K; (B) expansion of the pattern at 160 K. tor (often simultaneously) are observed. The ammonia guest re- Vertical thin red lines and arrows indicate the peaks from sII hydrate and blue mains mostly in the cage but in some configurations the ammonia lines and arrows indicate the peaks from sI hydrate. Lattice parameter molecule displaces one of the water molecules from a lattice site. ¼ 0 4491ð3Þ ¼ 0 7333ð5Þ (160 K): a . nm and c . nm for Ih (space group The water molecules in the hexagonal faces of the large clathrate P63∕mmc), a ¼ 0.6361ð3Þ nm for Ic (space group Fd-3m), a ¼ 1.1847ð8Þ nm for sI hydrate (space group Pm-3n), and a ¼ 1.7161ð9Þ nm for sII hydrate hydrate cages are less hindered and may also have less stable (space group: Fd-3m). water-water hydrogen bonds which require less energy to break compared to the water molecules forming hydrogen bonds in pentagonal faces. Snapshots from the simulations show that the nanoparticles at low temperatures in the presence of hydrogen ammonia molecules preferentially hydrogen bond with the water bonding ether guest molecules have been observed (34). molecules in the hexagonal faces. Ammonia-water hydrogen To study molecular level structure and dynamics of ammonia bonding severely distorts the small and large cage structures. At containing clathrate hydrates, we performed molecular dynamics temperatures below 200 K, the hydrate phase maintains its simulations of the THF (in large cages) + NH3 (in 39% of small mechanical stability without framework collapse despite the am- cages) binary sII clathrate hydrate from 100 to 240 K. We also monia-water hydrogen bonds and the defects they induce in the simulated the pure NH3 sI and sII clathrate hydrates and binary hydrate lattice hydrogen-bonding network. As we only performed CH4 (large cages) + NH3 (small cages) sII clathrate hydrates a molecular dynamics simulation and not a full free energy cal- for temperatures in the range of 100 to 240 K. The molecular culation comparing the thermodynamic stability of the clathrate dynamics simulation methodology is described in detail in Mate- hydrate phase to the products, we cannot comment on the ther- rials and Methods. For the duration of the simulations, all the modynamic stability of the ammonia clathrate hydrate phase. By clathrates are mechanically stable at simulation temperatures mechanical stability we imply that the hydrate structure did not

Table 1. The average percent (H3N⋯H-OH) hydrogen bonding configurations calculated from RDFs and the enthalpy of hydrogen bond formation for pure sI and sII NH3 hydrates and binary sII CH4 (large cages) + NH3 (small cages) hydrate at different temperatures Δ ∕ −1 Guests 100 K 120 K 140 K 160 K 170 K HHB kJ·mol

NH3 (pure sI, large cages) 4.6 12.9 34.5 54.4 68.9 7.66 NH3 (pure sI, small cages) 1.4 2.1 15.0 32.0 49.8 8.90 NH3 (pure sII, large cages) 7.8 17.1 28.3 51.5 61.8 5.85 NH3 (pure sII, small cages) 1.4 4.3 6.1 24.4 33.6 6.95 NH3 (binary sII, small cages) ∼0 0.6 1.3 1.8 2.9 5.09

Shin et al. PNAS Early Edition ∣ 3of6 Downloaded by guest on September 29, 2021 Fig. 4. Sample configurations of the NH3 guests hydrogen bonding with the water molecules of the large (L) and small (S) cages of the sI and sII clathrate hydrate (Top: sI, Bottom: sII cages). The snapshots of the cages were extracted from the periodic simulation cell. In cases where NH3 is incorporated into the water lattice, the displaced water molecule is also shown.

decompose under the pressure-temperature conditions of the have been attributed to episodic cryovolcanic effusion events simulation. As temperature and vibrational amplitudes of the which bring NH3 from the interior of Titan to its surface in the water molecules in the hydrate lattice increase, these lattice de- form of a fog or (36). Most work on ammonia present in fects lead to the breakdown of the water framework structure and Titan focuses on ammonia in aqueous solution in the “magma” instability of the hydrate phase. and its effect on methane clathrate hydrate inhibition and decom- From Table 1, the ammonia molecules in the large sI and sII position in that region (5). Our work shows that under tempera- cages form hydrogen bonds more readily than in the corre- ture and pressure conditions similar to those found on Titan’s ≈ 90 ≈ 1 6 sponding small cages. In addition, the larger hydrogen bonding surface (5) (T K and Patm . bar), considering the pre- formation enthalpy in the sI hydrate compared to the sII hydrate, sence of methane in the atmosphere of Titan and availability of reveals that the water lattice in the sI phase is less susceptible ice on its surface, it is possible that the extruded ammonia vapor to hydrogen bonding with ammonia and is preferred when the forms binary clathrate hydrate phases with methane. Clathrate ammonia forms a clathrate phase with amorphous ice upon hydrate formation after ammonia vapor deposition in the pre- annealing. sence of methane gas and annealing to about 100 K can provide In contrast to the pure NH3 hydrates, binary CH4 þ NH3 sII a mechanism for the removal of ammonia and methane from hydrate shows a H3N⋯H-OH hydrogen bond probability of only Titan’s atmosphere. Ethane clathrate hydrate formation may also approximately 3% even at 170 K. Incorporating methane in the be catalyzed by the presence of ammonia. cages of the binary clathrate hydrate apparently stabilizes the Similar cryovolcanic activity is also seen in Saturn’s moon cages which encapsulate ammonia. The molecular dynamics Enceladus where plumes of ammonia, methane, and water vapor simulation results are consistent within the framework of experi- are extruded from the South Pole (37). The sources of these mental knowledge of the ammonia hydrate system described methane extrusions in both moons have been related to clathrate above. Strong hydrogen bonding of ammonia with water in the hydrate dissociation (5, 38, 39). solid phase is expected. The stability of the ammonia hydrate is The broader significance of the catalyzing effect of ammonia dependent on the low temperature and/or stabilizing effect of on methane hydrate formation under vapor deposition conditions methane help gas. may be to the conditions of primordial ices in planets, comets, Discussion and in formation models. The ammo- nia can catalyze the formation of nonstoichiometric gas hydrates The presence of both ammonia and methane give a clathrate which are then trapped in icy grains and accreted into planetary hydrate that is much more stable than that of the pure ammonia objects. hydrate (stability up to 180 K for the mixed clathrate as compared In addition to subsurface processes, ammonia-bearing liquids to 150 K for the pure NH3 clathrate). On the other hand, the and vapors may interact directly with surface clathrate hydrate presence of ammonia is critical in forming a clathrate in a tem- phases on Titan. In situ clathrate hydrate formations (not invol- perature region where methane by itself does not form a clathrate ving ammonia) have been considered important in determining hydrate. The activation of ice surfaces by ammonia at low tem- the surface composition and structures of this moon (40–42) and peratures is a well known phenomenon (35), so it may well be that the presence of ammonia may play a role in these processes. synergistic behavior of ammonia and methane on the amorphous Polar, water miscible molecules such as ammonia are tradition- ice surface produce a reasonably stable clathrate: ammonia to ally considered as clathrate hydrate formation inhibitors. Our initiate the reaction by introducing defects and methane to sta- experiments and computations show that the inhibition effect is bilize the clathrate lattice by limiting guest-host hydrogen bond- not due to inherent instability of the solid clathrate hydrate phase ing. Experiments with ethane and ammonia gave similar results of these guest molecules, but is rather the stabilizing effect of (Fig. S8). From the work presented it is clear that ammonia plays these guests on the aqueous phase from which the clathrate an important role, so far unrealized, in forming solid clathrate hydrate is formed. phases at low temperatures in planetary environments. It may be difficult to quantify the effects of ammonia on a clathrate Materials and Methods hydrate-forming environment as it is clear that some ammonia Sample Preparation. Vapor codepositions of water and guest materials phases have time and temperature-limited regions of existence. (ammonia, methane, and 50 mole % ammonia/methane mixture) were Recent spectrophotometric studies by Nelson and coworkers performed in an evacuated chamber at approximately 0.01 mbar. The water have shown variations in the surface reflectance on Titan which was vaporized from a pipette into the evacuation chamber by low pressure

4of6 ∣ www.pnas.org/cgi/doi/10.1073/pnas.1205820109 Shin et al. Downloaded by guest on September 29, 2021 and deposited on a copper plate which was cooled down to approximately covered by quartz glass and dry nitrogen gas was blown over the surface dur- 16 K by DISPLEX (Air Products). In each experiment a total of 600 mmHg of ing measurements in order to keep ice from condensing. the guest gas (ammonia, methane or 1∶1 ammonia∶methane mixture) was injected into a 1 L bulb and slowly injected into the deposition chamber. The Computational Methods. Molecular Dynamics simulations were performed water and guest gas vapor flows were controlled by leak valve and after 24 h with DL_POLY version 2.20 (46) using the leapfrog algorithm with a time step approximately 2 g of water and 0.5 g of guest vapors were deposited of 1 fs. The positions of the water atoms of the structure I and struc- on the copper plate. The copper plate covered with the product deposit ture II clathrate hydrate phases were taken from X-ray and was removed from the evacuation chamber and quickly immersed in liquid the water hydrogen atoms assigned to oxygen atoms in the unit cell in such a nitrogen with minimal exposure to air. Significant moisture condensation on way as to simultaneously satisfy the ice rules and minimize the net unit cell the sample during the short transfer period is not expected. For the various dipole moment. The centers of mass of the guests are initially put in the cen- characterization experiments the materials were transferred to the powder ter of the hydrate cages. For simulations of the sI clathrate hydrate, 3 × 3 × 3 X-ray diffraction and Raman instruments. replicas of the unit cell are used with 162 large cages and 54 small cages in the In the single crystal experiments, a THF þ NH3 binary sII hydrate was pre- simulation cell. For simulations of the sII clathrate hydrate, a 2 × 2 × 2 replica pared from a 1∶17 solution of THF in 5% aqueous ammonia. The synthesis of the unit cell is used with 64 large cages and 128 small cages. conditions give an approximate mole ratio of 1∶0.946∶17 for THF∶NH3∶H2O In the simulations, the van der Waals and electrostatic intermolecular in- in this solution. Upon cooling the solution to 263 K masses of crystals teractions of water are modeled with the TIP4P potential (47), THF with the appeared. Crystals suitable for diffraction were identified by examination under a microscope mounted in a cold box. The structure obtained from AMBER force field (48) NH3 with the OPLS force field of Rizzo and Jorgensen the single crystal diffraction experiment was used to determine that 39% (49), and the TRAPP potential for CH4 (50). The potential parameters in the of the small cages were occupied by ammonia which gives an approximate force fields are given in Table S1. The partial electrostatic charges on the clathrate hydrate composition of 1∶0.78∶17 for THF∶NH3∶H2O. Different am- atoms of THF are calculated using the CHELPG method (51) and the other monia small cage occupancies are likely to be found starting from different guest molecules include partial atomic charges as part of the force field. initial compositions. Whether small cages could be filled with a more ammo- The water and guest molecules are given freedom of motion in the simula- nia-rich liquid is uncertain and should be the subject of a separate study. tions but their internal structure is considered rigid. A cutoff of 13 Å is used for the long-range forces in the simulation. X-Ray Data Collection and Structure Solution. Single crystal X-ray diffraction For the THF (in large cages) + NH3 (in small cages) binary sII clathrate data were measured on a Bruker Apex 2 Kappa diffractometer at 100 K, using hydrate three sets of simulations at 100 K, (temperature of experimental graphite monochromatized Mo Kα radiation (λ ¼ 0.71073 Å). The unit cell single determination), 183 K, and 200 K were performed. was determined from randomly selected reflections obtained using the For each simulation, one set of simulations with the all small cages occupied Bruker Apex2 automatic search, center, index, and least squares routines. by NH3 guests and a second set with 39% of the small cages occupied by NH3

Integration was carried out using the program SAINT, and an absorption cor- guests (in accordance to the experimental values) were performed. In addi- CHEMISTRY rection was performed using SADABS (43). The crystal structures were solved tion, seven simulation sets were performed at 100, 120, 140, 160, 170, 200, by direct methods and the structure was refined by full-matrix least-squares and 240 K for the pure NH3 sI and sII clathrate hydrates and the CH4 (large routines using the SHELXTL program suite (44). All atoms were refined ani- cages) + NH3 (small cages) binary sII clathrate hydrate to study the stability of sotropically. Hydrogen atoms on guest molecules were placed in calculated these phases. Simulations for each clathrate hydrate are performed for 6 ns positions and allowed to ride on the parent atoms. with 100 ps of temperature scaled equilibration to bring the clathrate hy- drate with each guest combination to the desired volume and temperature Powder X-Ray Diffraction (PXRD). The PXRD pattern was recorded on a in the constant pressure—constant temperature (NPT) ensemble. θ∕θ BRUKER AXS model D8 Advance diffractometer in the scan mode using The hydrogen bonding probabilities between NH3 guest and host water, α λ ¼ 1 5406 λ ¼ 1 5444 ∕ ¼ 0 5 Cu K radiation ( 1 . Å, 2 . Å, and I2 I1 . ). The samples p, were calculated from the radial distribution functions (RDF), gðrÞ between stored in liquid nitrogen were quickly transferred to the X-ray stage cooled the corresponding atoms on the guest ammonia and cage water molecules, down to approximately 100 K in air and diffraction patterns were measured with increasing temperature. The experiment was carried out in the step Z rmin mode with a fixed time of 2 s and a step size of 0.03014° for 2θ ¼ 8 to p ¼ ρgðrÞ4πr 2dr: [1] 42° at each temperature. The powder pattern was refined by the Le Bail 0 method using the profile matching method within FULLPROF (45). In Eq. 1, rmin is the first minimum in the RDF which appears after the hydro- Raman Spectroscopy. The Raman spectra were measured using a dispersive gen bond peak of ∼2 Å which represent hydrogen bonded NH3 with the cage Raman microscope instrument with the focused 514.5 nm line of an Ar-ion water molecules. laser for excitation. The scattered light was dispersed using a single-grating −90 spectrometer (1,200 grating) and detected with a CCD detector ( °C, ACKNOWLEDGMENTS. We thank G. L. McLaurin and S. Lang for technical sup- cooled by liquid nitrogen). The sample kept in liquid nitrogen was loaded port. We thank an anonymous reviewer for providing constructive comments onto a brass sample holder, which was cooled down to approximately 100 K on this manuscript. We also thank the National Research Council of Canada in air and measured with increasing temperature. The sample holder was for financial support.

1. Lunine JI, Stevenson DJ (1987) Clathrate and ammonia hydrates at high pressure: 11. Uras N, Devlin JP (2000) Rate study of ice particle conversion to ammonia hemihydrate: Application to the presence of methane on Titan. Icarus 70:61–77. Hydrate crust nucleation and NH3 diffusion. J Phys Chem A 104:5770–5777. 2. Fortes AD, Choukroun M (2010) Phase behavior of ice and hydrates. Space Sci Rev 12. Uras N, Buch V, Devlin JP (2000) Hydrogen bond surface chemistry: Interaction of NH3 153:185–218. with an ice particle. J Phys Chem B 104:9203–9209. 3. Loveday JS, et al. (2001) Stable methane hydrate above 2 GPa and the source of Titan’s 13. Kurnosov A, Dubrovinsky L, Kuznetsov A, Dmitriev V (2006) High Pressure/high . Nature 410:661–663. temperature behavior of the methane—ammonia water system up to 3 GPA. 4. Tobie G, Lunine JI, Sotin C (2006) Episodic outgassing as the origin of atmospheric Z Naturforschg 61b:1773–1576. methane on Titan. Nature 440:61–64. 14. Nelmes RJ, Loveday JS, Guthrie M, Francis DJ (2000) Molecular systems and mixtures 5. Choukroun M, Grasset O, Tobie G, Sotin C (2010) Stability of methane clathrate under pressure. ISIS Experimental Report RB 10795 (Rutherford Appleton Laboratory, hydrates under pressure: Influence on outgassing processes of methane on Titan. Oxfordshire, UK). Icarus 205:581–593. 15. Dong T, et al. (July 6–10, 2008) Experimental determination of methane hydrate 6. Cable ML, et al. (2012) Titan tholins: Simulating titan organic chemistry in the Cassini- formation in presence of ammonia. Proceedings of the 6th International Conference Huygens era. Chem Rev 112:1882–1909. on Gas Hydrates (ICGH 2008). 7. Fortes AD (2012) Titan’s internal structure and the evolutionary consequences. 16. Dong T, et al. (2009) Experimental study of separation of ammonia synthesis vent gas Space Sci 60:10–17. by hydrate formation. Petrol Sci 6:188–193. 8. Castillo-Rogez J, Lunine JI (2010) Evolution of Titan’s rocky core constrained by Cassini 17. Wang L, Liu A, Guo X, Chen G, Li G (2008) Experimental determination and calculation observations. Geophys Res Lett 37:L20205. of methane hydrate formation in the presence of ammonia. J Chem Ind Eng (China) 9. Choukroun M, Tobie G, Grasset O (2006) Ammonia, a methane hydrate inhibitor— 59:276–280. Implications for Titan’s atmospheric methane. Lunar and Planetary Science, XXXVII; 18. Fortes AD, Wood IG, Brodholt JP, Vočadlo L (2003) The structure, ordering and equa- Papers Presented to the Thirty-Seventh Lunar and Planetary Conference p 1640. tion of state of ammonia dihydrate ðNH3 · 2H2OÞ. Icarus 162:59–73. 10. Sloan ED, Koh CA (2008) Clathrate Hydrates of Natural (CRC Press, Boca Raton, 19. Fortes AD, Suard E, Lemée-Cailleau MH, Pickard CJ, Needs RJ (2009) Crystal structure FL), 3rd Ed,, pp 230–232. of ammonia monohydrate phase II. J Am Chem Soc 131:13508–13515.

Shin et al. PNAS Early Edition ∣ 5of6 Downloaded by guest on September 29, 2021 20. Mak TCW (1965) Hexamethylenetetramine hexahydrate: A new type of clathrate 34. Hernandez J, Uras N, Devlin JP (1998) Coated ice nanocrystals from water-adsorbate hydrate. J Chem Phys 43:2799–2805. vapor mixtures: Formation of ether—CO2 clathrate hydrate nanocrystals at 120 K. 21. Koga K, Tanaka H (1996) Rearrangement dynamics of the hydrogen-bonded network J Phys Chem B 102:4526–4535. of clathrate hydrates encaging polar guest. J Chem Phys 104:263–272. 35. Delzeit L, Powell K, Uras N, Devlin JP (1997) Ice surface reactions with acids and bases. 22. Alavi S, Susilo R, Ripmeester JA (2009) Linking microscopic guest properties to macro- J Phys Chem B 101:2327–2332. scopic observables in clathrate hydrates: Guest-host hydrogen bonding. J Chem Phys 36. Nelson RM, et al. (2009) Saturn’s Titan: Surface change, ammonia and implications for 130:174501. atmospheric and tectonic activity. Icarus 199:429–441. 23. Buch V, et al. (2009) Clathrate hydrates with hydrogen bonds. Phys Chem Chem Phys 37. Porco CC, et al. (2006) Cassini observes the active south pole of Enceladus. Science – 11:10245–10265. 311:1393 1401. č 24. Shinohara H, Nagashima U, Tanaka H, Nishi N (1985) Magic numbers for water-ammo- 38. Fortes AD, Grindrod PM, Trickett SK, Vo adlo L (2007) Ammonium sulfate on Titan: – nia binary clusters: Enhanced stability of ion clathrate structures. J Chem Phys 83:4183. Possible origin and role in cryovolcanism. Icarus 188:139 153. 25. Diken EG, Hammer NI, Johnson MA, Christie RA, Jordan KD (2005) Mid-infrared char- 39. Fortes AD (2007) Metasomatic clathrate xenoliths as a possible source for the south þ polar plumes of Enceladus. Icarus 191:743–748. acterization of the NH · ðH2OÞ clusters in the neighborhood of the n ¼ 20 “magic” 4 n – number. J Chem Phys 123:164309. 40. Fortes AD, Stofan ER (March 14 18th, 2005) Clathrate formation in the near-surface þ þ environment of Titan. 36th Lunar and Planetary Science Conference (abstr 1123). 26. Khan A (2001) Theoretical studies of NH4 · ðH2OÞ20 and NH3ðH2OÞ20H clusters. 41. Osegovic JP, Max MD (2005) Compound clathrate hydrate on Titan’s surface. J Geophys Chem Phys Lett 338:201–207. þ Res 110:E08004. 27. Willow SY, Singh NJ, Kim KS (2011) NH4 Resides inside the water 20-mer cage as þ 42. Choukroun M, Sotin C (2012) Is Titan’s shape caused by its meteorology and carbon opposed to H3O , which resides on the surface: A first principles molecular dynamics cycle? Geophys Res Lett 39:L04201. simulation study. J Chem Theory Comput 7:3461–3465. 43. Sheldrick GM (2002) SADABS Version 2.03 (University of Gottingen, Germany). 28. Jeffrey GA (1984) Hydrate Inclusion Compounds in Inclusion Compounds, eds JL 44. Sheldrick GM (2000) SHELXTL, Version 6.10 (Bruker AXS Inc., Madison, WI). Atwood, JED Davies, and DD MacNicol (Academic Press, London), Vol 1. 45. Rodriguez-Carvajal J (1990) FULLPROF: A program for rietveld refinement and pattern 29. Hallbrucker A, Mayer E (1990) Unexpectedly stable nitrogen, oxygen, carbon monox- matching analysis. Abstracts of the Satellite Meeting on Powder Diffraction of the XV ide and clathrate hydrates from vapor-deposited amorphous solid water: An Congress of the IUCr (International Union of Crystallography, Toulouse, France) p 127. X-ray and two-step differential scanning calorimetry study. J Chem Soc Faraday Trans 46. Smith W, Forester TR, Todorov IT DL_POLY 2.20 (CCLRC, Daresbury Laboratory, – 86:3785 3792. Daresbury). 30. Ripmeester JA, Ding L, Klug DD (1996) A clathrate hydrate of formaldehyde. J Phys 47. Abascal JLF, Sanz E, Garcia Fernandez R, Vega C (2005) A potential model for the study – Chem 100:13330 13332. of ices and amorphous water: TIP4P/Ice. J Chem Phys 122:234511. ş 31. Monreal IA, Devlin JP, Ma lakci Z, Çiçek MB, Uras-Aytemiz N (2011) Controlling non- 48. Cornell WD, et al. (1995) A second generation force field for simulation of proteins, classical content of clathrate hydrates through the choice of molecular guests and nucleic acids, and organic molecules. J Am Chem Soc 117:5179–5197. temperature. J Phys Chem A 115:5822–5832. 49. Rizzo RC, Jorgensen WL (1999) OLPS all-atom model for amines: Resolution of the 32. Schicks JM, Ripmeester JA (2004) The coexistence of two different methane hydrate amine hydration problem. J Am Chem Soc 121:4827–4836. phases under moderate pressure and temperature conditions: Kinetic versus thermo- 50. Martin MG, Siepmann JI (1998) Transferable potentials for phase equilibria. 1. United dynamic products. Angew Chem Inter Ed 43:3310–3313. atom description of n-alkanes. J Phys Chem B 102:2569–2577. 33. Pironon J, Grimmer J, Teinturier S, Guillaume D, Dubessy J (2003) Dissolved methane 51. Breneman CM, Wiberg KB (1990) Determining atom-centered monopoles from mole- in water: Temperature effect on Raman quantification in fluid inclusions. J Geochem cular electrostatic potentials. The need for high sampling density in formamide con- Explor 78–79:111–115. formational analysis. J Comput Chem 11:361–373.

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