DOI: 10.1126/science.1217291, 452 (2012);336 Science

Fred J. Ciesla and Scott A. SandfordSolar NebulaOrganic Synthesis via Irradiation and Warming of Ice Grains in the

This copy is for your personal, non-commercial use only.

clicking here.colleagues, clients, or customers by , you can order high-quality copies for yourIf you wish to distribute this article to others

  here.following the guidelines

can be obtained byPermission to republish or repurpose articles or portions of articles

  ): August 14, 2014 www.sciencemag.org (this information is current as of

The following resources related to this article are available online at

http://www.sciencemag.org/content/336/6080/452.full.htmlversion of this article at:

including high-resolution figures, can be found in the onlineUpdated information and services,

http://www.sciencemag.org/content/suppl/2012/03/29/science.1217291.DC1.html can be found at: Supporting Online Material

http://www.sciencemag.org/content/336/6080/452.full.html#relatedfound at:

can berelated to this article A list of selected additional articles on the Science Web sites

http://www.sciencemag.org/content/336/6080/452.full.html#ref-list-1, 5 of which can be accessed free:cites 46 articlesThis article

http://www.sciencemag.org/content/336/6080/452.full.html#related-urls7 articles hosted by HighWire Press; see:cited by This article has been

http://www.sciencemag.org/cgi/collection/planet_sciPlanetary Science

subject collections:This article appears in the following

registered trademark of AAAS. is aScience2012 by the American Association for the Advancement of Science; all rights reserved. The title

CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience

on

Aug

ust 1

4, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

on

Aug

ust 1

4, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

on

Aug

ust 1

4, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

on

Aug

ust 1

4, 2

014

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fr

om

plates are evidence of multiple distinct surgesof lava or one continuous flow with some tem-poral variation in flux or flow path. Nonethe-less, the features here are very well preserved,indicating that Cerberus Palus is either veryyoung or was buried shortly after formation andrecently exhumed.

References and Notes1. J. B. Murray et al.; HRSC Co-Investigator Team, Nature

434, 352 (2005).2. D. M. Burr, R. J. Soare, J.-M. Wan Bun Tseung, J. P. Emery,

Icarus 178, 56 (2005).3. D. P. Page, Icarus 189, 83 (2007).4. M. R. Balme, C. Gallagher, Earth Planet. Sci. Lett. 285,

1 (2009).5. J. B. Plescia, Icarus 88, 465 (1990).6. L. Keszthelyi, S. Self, T. Thordarson, J. Geol. Soc. London

163, 253 (2006).7. W. L. Jaeger, L. P. Keszthelyi, A. S. McEwen, C. M. Dundas,

P. S. Russell, Science 317, 1709 (2007).8. L. P. Keszthelyi et al., Icarus 205, 211 (2010).

9. W. L. Jaeger et al., Icarus 205, 230 (2010).10. W. K. Hartmann, D. C. Berman, J. Geophys. Res. 105,

(E6), 15011 (2000).11. D. M. Burr, J. A. Grier, A. S. McEwen, L. P. Keszthelyi,

Icarus 159, 53 (2002).12. A. McEwen et al., Icarus 176, 351 (2005).13. J. L. Bandfield, V. E. Hamilton, P. R. Christensen, Science

287, 1626 (2000).14. P. R. Christensen et al., J. Geophys. Res. 106 (E10),

23823 (2001).15. D. L. Peck, T. Minakami, Geol. Soc. Am. Bull. 79, 1151

(1968).16. M. H. Carr, R. Greeley, Volcanic Features of Hawaii: A

Basis for Comparison with Mars (U.S. Government PrintingOffice, Washington, DC, 1980).

17. M. T. Mellon, J. Geophys. Res. 102 (E11), 25617 (1997).18. P. H. Smith et al., Science 325, 58 (2009).19. J. S. Levy, D. R. Marchant, J. W. Head, Icarus 206, 229

(2010).20. W. V. Boynton et al., Science 297, 81 (2002).21. T. R. Watters et al., Science 318, 1125 (2007).22. J. Zimbelman, W. Garry, J. E. Bleacher, L. S. Crumpler,

Lunar Planet. Sci. Conf. 42, 2443 (2011).23. G. P. Walker, Bull. Volcanol. 53, 546 (1991).

24. K. Hon, J. Kauahikaua, R. Denlinger, K. Mackay,Geol. Soc. Am. Bull. 106, 351 (1994).

25. D. L. Peck, U.S. Geol. Surv. Prof. Pap. 550B, 148(1966).

26. J. P. Lockwood et al., U.S. Geol. Surv. Prof. Pap. 1613,1 (2000).

27. S. Thorpe, J. Fluid Mech. 46, 299 (1971).28. L. Keszthelyi et al., Geochem. Geophys. Geosyst. 5,

Q11014 (2004).29. R. F. Katz, R. Ragnarsson, E. Bodenschatz, N. J. Phys. 7,

37 (2005).30. Video of spiraling microplate formation in wax spreading

center model by (29) may be viewed here: http://iopscience.iop.org/1367-2630/7/1/037/media/movie.mpg.

Acknowledgments: We thank A. C. Enns, K. X. Whipple,and A. B. Clarke for insightful conversation during thepreparation of this manuscript and R. Greeley, whoseguidance prompted this work. All original data reported inthis paper are archived by NASA’s Planetary Data System.

20 January 2012; accepted 27 March 201210.1126/science.1219437

Organic Synthesis via Irradiationand Warming of Ice Grains in theSolar NebulaFred J. Ciesla1* and Scott A. Sandford2

Complex organic compounds, including many important to life on Earth, are commonly foundin meteoritic and cometary samples, though their origins remain a mystery. We examined whethersuch molecules could be produced within the solar nebula by tracking the dynamical evolutionof ice grains in the nebula and recording the environments to which they were exposed. We foundthat icy grains originating in the outer disk, where temperatures were less than 30 kelvin,experienced ultraviolet irradiation exposures and thermal warming similar to that which has beenshown to produce complex organics in laboratory experiments. These results imply that organiccompounds are natural by-products of protoplanetary disk evolution and should be importantingredients in the formation of all planetary systems, including our own.

Complex organic compounds have beenfound in meteorites and interplanetarydust particles, leading many to suggest

that Earth’s prebiotic material was deliveredby comets and chondritic planetesimals. Theorigin of these organic compounds, however, isunknown. Whereas organic molecules can beproduced during aqueous alteration of a parentbody (1) or through Fischer-Tropsch reactionsin protoplanetary disks (2), the high D/H ratiosfound in meteoritic organics point to a low-temperature origin (3). Irradiation of astrophys-ical ice analogs (containing simple moleculeslike H2O, CO, CO2, NH3, and CH3OH) by ul-traviolet (UV) photons in the laboratory hasproduced of a suite of organic molecules simi-lar to those found in primitive bodies in our so-lar system, including amino acids, amphiphiles,

quinones, and nucleobases (4–10). These experi-ments simulated conditions (temperatures, pres-sures, radiation fluxes) similar to those foundin dark molecular clouds—the collection of gasand dust that collapses to form stars and planets.Within these clouds, ice-mantled grains are ex-posed to relatively low fluxes of UV from theambient interstellar radiation field, allowing or-ganics to be produced. It remains unclear, how-ever, if the full suite of complex organics foundin primitive bodies could be produced within amolecular cloud and to what extent the com-pounds were preserved during the formation ofthe solar system.

These experimental conditions are also rel-evant to the outer solar nebula, where tem-peratures were low enough for C-, H-, O-, andN-bearing ices to form (11). If ices in this regionwere irradiated to substantial levels, organicswould have been produced, increasing the in-ventory of such compounds beyond what mayhave been inherited from the molecular cloud.Indeed, observations of molecular emission fea-tures suggest that protoplanetary disks support

active organic chemistry, processing the raw ma-terials from the molecular cloud to yield higherabundances of organic species, though the path-ways for production are unclear (12).

To investigate the production of organicsafter molecular-cloud collapse, we modeledthe paths of ice-mantled grains through the so-lar nebula (Fig. 1) (13–16). Particles migratedaround the nebula due to disk evolution, gasdrag, gravitational settling, and both radial andvertical turbulent diffusion. We assumed that thelevel of turbulence in the disk is characterized bythe turbulence parameter, a, which describesboth the viscosity in the disk, n = acsH where csis the local speed of sound in the disk and H isthe local gas scale height, and the diffusivity oftrace materials, D (~n) (16, 17). We set a = 0.001everywhere, as the magnetorotational instabilityis expected to have operated in the outer disk (18).

The disk was assumed to be in a steadystate and had a surface density distribution

∑ðrÞ ¼ 2000r

1 AU

� �−1g/cm2 [amounting to

110= of the solar mass out to 70 astronom-

ical units (AU)] and a thermal structureTðrÞ ¼ 200 r

1 AU

� �−12 K (where r is the distancefrom the Sun), appropriate for flared disksaround young T Tauri stars (11, 19). We trackedthe dynamics of 5000 ice-mantled grains withradius a = 1 mm and unit density. Althoughparticles of a broad range of sizes would havebeen present, we chose to follow 1-mm particlesas individual organic hot spots, and globules inmeteorites and comets are often found to be ofthis spatial scale (20, 21). Particles began at themidplane of the disk (with the height above thedisk midplane given by z, and the midplane de-fined as z = 0 AU) where T = 30 K (r = 49 AU).At this temperature, C- and N-bearing ices ofthe type needed to form organics condensed(22), and D/H ratios in water are elevated dueto ion-molecule reactions (23).

1Department of the Geophysical Sciences, University ofChicago, 5734 South Ellis Avenue, Chicago, IL 60430, USA.2NASA Ames Research Center, MS 245-6, Moffett Field, CA94035, USA.

*To whom correspondence should be addressed. E-mail:fciesla@uchicago.edu

27 APRIL 2012 VOL 336 SCIENCE www.sciencemag.org452

REPORTS

As a particle moved through the disk, wecalculated the number of UV photons incidenton its surface. The radiation was assumed to beincident on the disk with a flux, F0, directednormal to the disk midplane. The flux wasattenuated with depth as photons were absorbedby solid particles. Thus, the flux everywhere wasF(r,z) = F0e

−t(r,z), where t is the optical depth ofmaterial suspended in the disk above the point ofinterest [tðr,zÞ ¼ ∫∞jzjrgðr,zÞkdz, where rg(r,z) isthe density of material in the disk and k is theaverage opacity of the suspension]. We assumean opacity of k = 7.5 cm2/g, a conservative valuethat is on the high end of the range expected inthe cool outer regions of a protoplanetary disk(24). Lower opacities would increase the numberof photons seen by each particle. We take as abaseline an incident flux equivalent to the currentinterstellar UV flux of 108 photons cm−2 s−1 (1G0)(25), but higher fluxes can be considered by mul-tiplying by the desired enhancement factor.

The starting location of the particles wasshielded such that the flux was attenuated by

more than 25 orders of magnitude. As most ofthe mass of the nebula was located around themidplane, these conditions are often used incalculating the chemical evolution of primitivematerials. At this location, an ice grain wouldhave seen <10−25F0pa

2∆t ~ 10−11 photons if itremained at its starting location throughout thesimulation, a period of ∆t = 106 years. How-ever, in the presence of vertical diffusion, smallparticles spend ~68% of their time within 1Hof the midplane but 32% of their lifetimes athigher altitudes, with ~5% being spent above2H (14). Because the UV flux was a strong func-tion of height, it was the infrequent but non-negligible excursions to high altitudes that wereprimarily responsible for small grains seeinglarge numbers of photons. Irradiation exposuresalso increased as grains diffused outward inthe disk, where the lower surface densities of gasand dust allowed the UV to penetrate closer tothe disk midplane. Thus, the radial and verti-cal motions of the grains controlled their UVexposures.

Figure 2 shows that the cumulative numberof UV photons grains encountered did not climbuniformly. Rather, the increases in incident pho-tons were episodic and occurred when a grainwas lofted to high altitudes or far out in the disk.Plotting the irradiation histories against the tem-peratures seen by the particles, where we tookthe particle temperature as being equal to thegas temperature everywhere, demonstrates howthe UV exposure generally rose early while thegrains were cold and when all key ices remainedon the grain. Less than 0.5% of photons woulddesorb these molecules (26), which would thenrecondense on the same or another grain. Thus,loss of mass in this manner would be minimal.

Figure 3 shows that a typical dosage for theparticles was ~5 × 1012 photons in our nominalcase. Assuming a pure H2O grain, this corre-sponds to ~50 UV photons per molecule. Exper-imental results suggest an efficiency of productionof approximately one organic molecule producedper 400 incident photons (6, 16). Thus >12% ofthe mass of ices in the outer solar nebula would

Fig. 1. (Left) Trajectoryof one of the survivingparticles (which are definedas those that did not mi-grate inside of 0.1 AU ofthe young Sun) throughthe solar nebula superim-posed on a map of the UVradiation flux in the disk.The flux is normalized toits value at z = T∞ andassumed to propagate nor-mal to the disk midplane.The blue and green sym-bols denote the startingand final locations, respec-tively. (Right) The r and zcoordinates of the particle through time.

Fig. 2. (A) Cumulative number of photons incident on five grains throughoutthe 106-year lifetime in the disk, assuming an incident flux of 1G0. The blackcurve corresponds to the grain whose trajectory is shown in Fig. 1; the other

curves represent other random particles from the simulation. (B) Totalincident photons seen by the same particles plotted against their temper-atures. The inset shows a zoomed-in view.

www.sciencemag.org SCIENCE VOL 336 27 APRIL 2012 453

REPORTS

be converted to organic compounds. However,protoplanetary disks like our solar nebula areexposed to enhanced UV fluxes, either fromtheir own central stars (27) or from other starsin a low-mass cluster, resulting in average in-cident fluxes of up to ~103G0 (28). This in-creases the average dosage of ice grains to50,000 photons per molecule, greatly increasingorganic production.

Grain growth would have resulted in lowerphoton dosages due to decreased particle crosssections per unit volume (16, 29). However, thedecrease in opacity of the nebula would have al-lowed UV photons to penetrate deeper into thedisk (29) to irradiate the grain aggregates. Further,models of dust growth show that fragmentationwould constantly free particles from the larger ag-gregates through energetic collisions (30). Thus,even if icy grains remain as 1-mm entities for justa part of the 106 years modeled here, they canreceive substantial UV dosages (Fig. 2).

By itself, irradiation does not produce theorganic compounds. When UV photons are in-cident on astrophysical ices in the laboratory,they breakmolecular bonds in the ices, producingreactive ions and radicals. If these reactivephotoproducts are adjacent to each other, theymay react to form new compounds, even at verylow temperatures. When the irradiated ice iswarmed, the photoproducts become mobile andreact more readily. Such reactions occur duringwarm-ups through any temperature range but areparticularly enhanced during the amorphous-amorphous transition near 80 K, the amorphous-to-cubic transformation around 135 K, and thesublimation of the H2O in the ice at T > 135 K(4–10, 16). Thus, warming of irradiated icesyields a burst of organic synthesis, even if the iceis not currently being irradiated. Reactions broughton by warming are still largely constrained byproximity rather than considerations of normalchemical equilibrium. However, these experi-mental results are robust in that the amounts andtypes of molecules produced are largely insen-sitive to the temperature of the ices during ir-

radiation and the exact composition of thestarting ices (16).

Particle warming would have occurred asgrains diffused to high altitudes where the in-creased photon flux would have heated grainsbeyond the midplane temperature. Though weassumed our disk was isothermal with height,temperatures may reach ~10 to 50 K abovemidplane temperatures at heights of |z| > 0.2routside ~10 AU (31). As such, not only wouldparticles accumulate substantial UV dosages,but they would also be warmed as they movedthrough the disk. Thus, the conditions shownto produce organics in laboratory experiments,irradiation and warming, would be natural con-sequences of the dynamical evolution of ices inthe solar nebula. Photo-processing in the solarnebula thus represents an ideal environment forthis form of organic synthesis.

The grains in our study are irradiated duringtheir large-scale movement in the disk, whichsuggests that similar products would be madeavailable to meteoritic and cometary bodies,consistent with observations (20, 21). Further,organics on particles brought to the innermostregions of a protoplanetary disk would vapor-ize, allowing the products of this organic chem-istry to be observed in the gas phase, offering anexplanation for the emission features observedby the Spitzer Space Telescope (12). As wepredict that complex species such as amino acidswill be formed, identification of more complexorganic species in other disks may serve to testthis method of production. Because the totalUV fluences received by ices in the solar nebulaare considerably greater than those experiencedby typical ices in dense molecular clouds, diskprocessing would yield greater overall conver-sions of ices into organics and would produceorganics of greater complexity. The exact massof organic production remains uncertain, as itwill depend on the incident UV flux and themass of ice contained in the outer disk. Ourresults, however, demonstrate that cold, icy 1-mmgrains would see UV dosages of ~1012 to 1015

photons for modest incident fluxes of 1 to 102G0.This allows for substantial organic production,with at least ~5% of the mass of ices being con-verted to organics and production being limitedmore by the availability of starting materialsthan by energetic photons (16). These fluxes aremuch less than those thought to be necessary fororganic production to occur in protoplanetarydisks (~106G0) (29). Thus, rather than being lim-ited to disks around stars located near massiveOB stars, complex organics should be producedin disks around all stars and made available fordelivery to the surface of planets where theycould play a role in the origin of life.

References and Notes1. E. T. Peltzer, J. L. Bada, G. Schlesinger, S. L. Miller,

Adv. Space Res. 4, 69 (1984).2. J. A. Nuth III, N. M. Johnson, S. Manning, Astrophys. J.

673, L225 (2008).3. S. A. Sandford, M. P. Bernstein, J. P. Dworkin, Meteorit.

Planet. Sci. 36, 1117 (2001).4. W. Hagen, L. J. Allamandola, J. M. Greenberg, Astrophys.

Space Sci. 65, 215 (1979).5. W. A. Schutte, L. J. Allamandola, S. A. Sandford,

Adv. Space Res. 12, 47 (1992).6. M. P. Bernstein, S. A. Sandford, L. J. Allamandola,

S. Chang, M. A. Scharberg, Astrophys. J. 454, 327 (1995).7. M. P. Bernstein et al., Science 283, 1135 (1999).8. M. P. Bernstein, J. P. Dworkin, S. A. Sandford,

G. W. Cooper, L. J. Allamandola, Nature 416, 401 (2002).9. G. M. Muñoz Caro et al., Nature 416, 403 (2002).

10. M. Nuevo et al., Adv. Space Res. 48, 1126 (2011).11. E. I. Chiang, P. Goldreich, Astrophys. J. 490, 368 (1997).12. J. S. Carr, J. R. Najita, Science 319, 1504 (2008).13. F. J. Ciesla, Astrophys. J. 723, 514 (2010).14. F. J. Ciesla, Astrophys. J. 740, 9 (2011).15. S. Charnoz, L. Fouchet, J. Aleon, M. Moreira, Astrophys. J.

737, 33 (2011).16. Materials and methods are available as supplementary

materials on Science Online.17. F. J. Ciesla, J. N. Cuzzi, Icarus 181, 178 (2006).18. T. Sano, S. M. Miyama, T. Umebayashi, T. Nakano,

Astrophys. J. 543, 486 (2000).19. L. Hartmann, N. Calvet, E. Gullbring, P. D’Alessio,

Astrophys. J. 495, 385 (1998).20. S. A. Sandford et al., Science 314, 1720 (2006).21. K. Nakamura-Messenger, S. Messenger, L. P. Keller,

S. J. Clemett, M. E. Zolensky, Science 314, 1439 (2006).22. K. Lodders, Astrophys. J. 591, 1220 (2003).23. K. Willacy, Astrophys. J. 660, 441 (2007).24. Z. Zhu, L. Hartmann, C. Gammie, Astrophys. J. 694, 1045

(2009).25. H. J. Habing, Bull. Astron. Inst. Neth. 19, 421 (1968).26. K. Öberg, H. Linnartz, R. Visser, E. F. van Dishoeck,

Astrophys. J. 693, 1209 (2009).27. T. J. Bethell, E. A. Bergin, Astrophys. J. 739, 78 (2011).28. F. C. Adams, E. M. Proszkow, M. Fatuzzo, P. C. Myers,

Astrophys. J. 641, 504 (2006).29. H. B. Throop, Icarus 212, 885 (2011).30. S. J. Weidenschilling, Icarus 60, 553 (1984).31. P. Woitke, I. Kamp, W.-F. Thi, Astron. Astrophys. 501,

383 (2009).

Acknowledgments: F.J.C. and S.A.S. acknowledge fundingfrom NASA’s Origins of Solar Systems program. S.A.S. alsothanks the Astrobiology Institute for funds.

Supplementary Materialswww.sciencemag.org/cgi/content/full/science.1217291/DC1Supplementary TextFigs. S1 to S11References (32–47)

30 November 2011; accepted 13 March 2012Published online 29 March 2012;10.1126/science.1217291

Fig. 3. Total number of in-cident photons for each ofthe 4979 surviving grainsplotted against their loca-tions after 106 years. A typ-ical exposure for our nominalflux (black diamonds) is ~5 ×1012 photons. The red andblue symbols represent thesame calculations using thelower and higher opacities,respectively, as described inthe text. The variations inaverage flux due to opacitydifferences are less than oneorder of magnitude.

27 APRIL 2012 VOL 336 SCIENCE www.sciencemag.org454

REPORTS