888

water-in-oil-in-water (11) by encapsulationof the initial simple emulsion. In principle,the size, the number, and even the composi-tion of the drops can be controlled at eachstep of the process, leading to a unique wayof producing monodisperse, perfectly con-trolled, multiple emulsions. However, mas-tering the surface properties of the channelis a prerequisite for this process to runsmoothly and controllably. A way aroundthis is to produce the multiple emulsion inone step, using three concentric flows so asto avoid contact of the inner streams with thechannel wall. Such a geometry is difficult tofabricate within the usual two-dimensionalmicrofluidic structures obtained by lithogra-phy, but it was recently achieved with aclever multiple-micropipette device.Monodisperse core-shell particles and cap-sules (12) were obtained, as well as poly-merosomes of controlled sizes synthesizedfrom block copolymers (13).

Microfluidics can thus be a powerful andversatile tool for materials or colloidal engi-neering. It is the only technique that canproduce 100% encapsulation of an activesubstance by means of a one-step process.Engineering new controlled materials thenbecomes a game limited only by the numberof combinations of the basic products, andby ones imagination.

A controversial question naturally fol-lows: Besides being a smart research tool,can microfluidic droplet devices be used asproduction tools (chemical plants on achip)? With a flow rate of 1000 l/hour perchannel, one needs 1000 channels in parallelto produce a liter of material per hour. Highlevels of integration can be reached on achip, but likely a linking up of many deviceswill be necessary, potentially leading tocomplications for connections and control.Developing the corresponding technologymay be economically sensible only for mate-rials with very high added value (such asthose in biology, pharmaceuticals, or cos-metics), but not for conventional chemistryor basic material production.

A large number of research reports andpatents attest to the ongoing attempts todevelop new research tools for biological orpharmaceutical applications by means ofdroplet microfluidics. The goal is to handlethe many droplets that can be generatedwith only a minute amount of material, andto divide and recombine them in a multi-plicity of nanoreactors so as to performhigh-throughput screening and combinator-ial studies (14). Some would like to see thisapproach as the next-generation technologythat will replace the widely used combina-torial robotic platforms.

What is required is on-chip control andreproducibility of many droplet processes:fabrication, sorting, storage, fusion,

breakup, and trafficking (3, 8, 15), amongothers. For example, droplet generation iscurrently controlled by tuning the inputflow rates. Unfortunately, this affects simul-taneously the frequency, size, composition,and speed of the droplets, whereas onewould want to control each of these param-eters independently. A natural microfabri-cation strategy is to integrate actuators toachieve local control of droplet motion.Pneumatic actuators have proven highlyintegrable in a different microfluidic con-text (16), and electrostatic actuation withintegrated electrodes is also being investi-gated. The gain in control may unfortu-nately result in somewhat sophisticated andspecialized chips with limited flexibilityand versatility. It may be necessary to stan-dardize a few basic on-chip functions, witha drift toward passive strategies that oftencombine simplicity and robustness.

Improvements in design should beguided by attention to basic physics andchemistry. Interfaces are essential at suchsmall scales, and surfactants should beavoided as much as possible. Hence, a syn-ergy between microfabrication require-ments and surface chemistry is needed toyield robust channel wetting properties.This will create the needed reproducibilityof droplet generation for a range of flow-ing liquids and flow rates. The complexdynamics of thousands of droplets flowingin channels with long-range hydrodynamic

correlations will require modeling, possi-bly with the help of concepts borrowedfrom dynamical system theories. Theresult will be the design of smart networktopologies and (ideally passive) function-alities (15), opening the way to control,reproducibility, and versatility in on-chipdroplet management, ultimately at thedroplet level.

References

1. T.Thorsen, R.W. Roberts, F. H.Arnold, S. R. Quake, Phys.Rev. Lett. 86, 4163 (2001).

2. H. Stone, A. D. Stroock, A. Ajdari, Annu. Rev. Fluid Mech.36, 381 (2004).

3. D. R. Link, S. L. Anna, D. A. Weitz, H. A. Stone, Phys. Rev.Lett. 92, 054503 (2004).

4. J. D. Tice, A. D. Lyon, R. Ismagilov, Anal. Chim. Acta 507,73 (2004).

5. P. Guillot,A. Colin, in preparation.6. R. Dreyfus, P. Tabeling, H. Willaime, Phys. Rev. Lett. 90,

144505 (2003).7. K. Jensen,A. Lee, Lab. Chip 4, 432N (2004).8. H. Song, J. D. Tice, R. F. Ismagilov, Angew. Chem. Int. Ed.

42, 768 (2003).9. D. Tsoi, K. Hatton, T. A. Doyle, Langmuir 21, 2113

(2005).10. A. F. Nieves et al., Adv. Mater. 17, 680 (2005).11. S. Okushima, T. Nisiksako, T. Torii, T. Higuchi, Langmuir

20, 9905 (2004).12. A. S. Utada et al., Science 308, 537 (2005).13. E. Lorenceau et al., Langmuir, in press.14. B. Zheng, L. S. Roach, R. F. Ismagilov, J. Am. Chem. Soc.

125, 11170 (2003).15. Y.Tan, J. S. Fisher,A. I. Lee,V. Cristini,A. Phillip, Lab. Chip

4, 292 (2004).16. T. Thorsen, S. J. Maerkl, S. R. Quake, Science 298, 580

(2002); published online 26 September 2002(10.1126/science.1076996).

10.1126/science.1112615

Since the two Viking landers toucheddown on Mars in 1976, the ubiqui-tous surface soil and dust have

defied attempts to model their propertiesand understand how they formed. The fine

soil that givesMars its red colorholds clues to thepresence of liquidwater, the rock

weathering processes, and the potentialbiological history of the planet. Throughdust storms, it plays a key role in the cli-matic cycles of Mars. It may hamperexploration by interfering with roboticand human performance, but may alsooffer a valuable resource by supplyingwater and fuel and suppor ting plant

growth and food production. What isknown and what is still puzzling about themartian soil? And do we have similar soilson Earth? Recent results from the Marsexploration rovers Spirit and Opportunityand from terrestrial studies add to ourunderstanding and open new questions.

Data from the Viking landers andorbiters and the Pathf inder rover (16)show that the surface of Mars is coveredby a blanket of fine-textured soil compo-sitionally similar to the atmospheric dust(see the figure). The soil contains silicon,iron, aluminum, magnesium, calcium,titanium, sulfur, and chlorine at uniqueelemental proportions (that is, relativelyrich in sulfur and chlorine compared tomost terrestrial soils). It lacks organicmatter and shows strong oxidizing activ-itya combination that suggests the pos-sibility of rapid chemical decompositionof organic matter leading to the decima-tion of living organisms. It is rich in

P L A N E TA RY S C I E N C E

The Enigma of the Martian SoilAmos Banin

The author is in the Department of Soil and WaterSciences, Hebrew University, Rehovot 76100, Israel,and at the SETI Institute, Mountain View, CA 94043,USA. E-mail: amos.banin@huji.ac.il

Enhanced online atwww.sciencemag.org/cgi/content/full/309/5736/888

5 AUGUST 2005 VOL 309 SCIENCE www.sciencemag.org

P E R S P E C T I V E S

Published by AAAS

on A

ugus

t 1, 2

015

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fro

m

on A

ugus

t 1, 2

015

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fro

m

on A

ugus

t 1, 2

015

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fro

m

889

amorphous weathered silicate and ironoxide grains but lacks grains of well-developed secondary silicates such asclays. It also lacks carbonates but con-tains high concentrations of chlorine andsulfur salt-minerals (evaporites) andmagnetically active minerals.

More recent results obtained by theMars exploration rovers Spirit andOpportunity provide evidence for local-ized formations of water-modified weath-ered rocks that contain the mineral jarosite(710). This mineral typically forms inaqueous environments of highly acidic sul-fate solutions. On Earth, it is found nearmine spills and in acid sulfate soils. In gen-eral, however, the elemental compositionof the soils analyzed by the two rovers issimilar to that summarized above.

Using onboard spectroscopic tools, therovers established the pervasive presenceof nanometer-scale iron oxide particles inthe soils. The use of the rover wheels fortrenching and of a brush and a rock abra-sion tool for rock cleaning enabled theacquisition of depth profiles of elementalconcentrations and mineral types in thesoils and on the surface of rocks at the roversites. The results show that the nanometer-scale iron oxide particles and the evaporitesare usually more concentrated at the soil-atmosphere and rock-atmosphere inter-faces (7, 1012).

This evidence poses a number of ques-tions (13). Where is all the organic matterimported by meteorites or produced other-wise? Is the soil really highly oxidizing? Ifso, to what extent and as a result of whatformation mechanism? How are the solu-ble evaporites emplaced in the soil? Arethey really water-transported evaporites?Do they provide evidence for extensivewater on the martian surface? If yes, thenwhere are the other minerals, such as claysand carbonates, that should form duringlow-temperature hydrothermal weather-ing? Why are the abundant secondary ironoxides and silicates in the soil primarily inthe form of nanometer-scale crystalsrather than larger, more mineralogicallystable grains? Is the soil coupled chemi-cally and mineralogically to the local sur-face rocks? And is there any connection toextinct or extant life in the soil?

Several hypotheses have been proposedto explain the formation of the soil andanswer these questions. The acid fog sce-nario (13, 14) suggests that a major portionof the soil formed by weathering at themicroscopic rockatmosphere interfaceover hundreds of millions of years. Thisunique weathering process is driven by mistsand fogs of acidic volcanic aerosols, whichare neutralized through chemical reactionswith mineral components of the surface

rocks. No liquid wateris involved in thisweathering process,thus preventing thegrowth of larger crys-tals and the formationof secondary mineralssuch as clays. In otherhypotheses, liquidwaterin the form ofeither shallow seas (15) or seep-ing-up acidic groundwater (16)creates precipitation environ-ments that are conducive to theformation of jarosite, for example.

There is some debate overwhether Mars is reallycovered with soil.Squyres et al. definemartian soil as anyloose, unconsolidatedmaterials that can bedistinguished fromrocks, bedrock, orstrongly cohesive sed-iments. No implica-tion of the presence orabsence of organic materialsor living matter is intended[(8), p. 799; (9), p. 1702]. Ialso favor the use of the termsoil rather than the termregolith (defined as a layerof loose heterogeneous mate-rial covering solid planetaryrock) or the often-used termdirt to describe martian soil.However, the above definitionis perhaps too narrow and can be broad-ened to agree more precisely with the gen-eral definition of soil on Earth.

Terrestrial soils may be defined as thetop weathered or partly weathered layer ofthe terrestrial lithosphere that is exposedto and modif ied by atmospheric,hydrolytic, and biotic effects. Soil con-sists of a porous mineral matrix that con-tains a mixture of weathered and non-weathered rock grains, organic matter,and debris of dead organisms. The weath-ering agents are physical (such as thermalexpansion/contraction and freeze/thawcycles) and chemical (mostly hydrolyticprocesses but also reduction/oxidationand other reactions).

With current evidence, martian soils can bedefined, analogously to terrestrial soils, as thetop nonconsolidated layer of weathered and/orpartly weathered rocks of the martian litho-sphere that is exposed to and modified byatmospheric and hydrolytic effects. Note thatthis definition omits the biotic effect. It cannotbe ruled out that part of the soil formed early inMars history, when conditions on its surfacemay have been much like those on the primi-

tive Earth, so that abiotic andprimitive biotic evolutioncould have taken place androck weathering that formedsoils was enhanced. How-ever, current evidence sug-gests that rock weatheringand soil formation on Mars is

a very slow process thatcontinues to the present.These weathering pro-cesses are driven by thechemical interactions ofgaseous and aqueousspecies, transported bythe martian atmosphereand hydrosphere, withthe martian rocks. Forexample, the typical red

color of Mars is due to the oxida-tion of iron (rusting) in exposedrock minerals by oxidizing gasesthat form photochemically in theatmosphere. The sulfate and chlo-

ride salt evaporites mayhave been added to thesoil as it formed by acidfog weathering causedby acidic volcanicvolatiles transported inthe atmosphere. Themartian hydrosphereinfluenced soil forma-tion through outflows ofwater (either fresh wateror highly saline brines),catastrophic floods,and/or the melting of

permafrost by shallow volcanism. Thereleased water interacted with martian rocksand modified their mineralogy through disso-lution and reprecipitation.

The chemical interactions with theatmosphere and hydrosphere profoundlyaltered the mineralogy and the reactivityof the top layer of the martian lithosphere,rendering it much more chemically reac-tive than the original lava and forming theglobal martian soil layer (pedosphere).Martian soil thus has several attributesthat render it a soil rather than a regolith.In contrast, the Moon is covered with aregolith composed of primary rock parti-cles broken down physically or mechani-cally, mostly by micrometeorite impacts,but never exposed to atmospheric effectsor hydrolytic weathering.

Are there terrestrial sites, soils, ormineral mixtures that are true analogs formartian soil? Navarro-Gonzlez et al.(17) have argued that soils in one of thedriest regions on Ear th, the AtacamaDesert in Chile, are a model for martiansoils. They found that the number of cul-turable bacteria decreased steeply along aCR

EDIT

:NA

SA

Viking 2 Lander sampling-arm

trench and frost patches

Pathfinder-Sojourner

wheel marks

Mars exploration rover

Spirit surface scraping

Mars exploration rover

Opportunity touchdown prints

Back to the soil. Close-ups of Marssoil taken by landers and rovers.

www.sciencemag.org SCIENCE VOL 309 5 AUGUST 2005

P E R S P E C T I V E S

Published by AAAS

890

north-south transect, reaching extremelylow values at the driest site. Using simula-tions of the Viking biology experiments(3 , 4) , they showed that pyrolyzableorganic matter decreased to extremelylow values along the transect from thewetter to the drier sites; abiotic formatedecomposition was measured in all thesites. In this respect, Atacama soils mayindeed be the closest model for Mars soilson Earth.

However, the f indings are controver-sial, and many questions remain open.Maier et al. (18) have reported orders-of-magnitude higher counts of culturablebacterial cells in samples from the samesites but taken from deeper horizons in thesoil profile, not just from the top surfacelayer as reported in (17). Furthermore,detailed calculations and additional analy-ses suggest that the Atacama soils containfar higher concentrations of total organiccarbon than the Mars soils analyzed in theViking pyrolysis experiment may havehad, considering the systems detectionlimits for organic carbon [in the range of afew parts per billion (ppb) for most com-pounds and up to several hundred ppb fora few compounds]. Recalculation of thedata reported in figure 2C of (17) showsthat the total organic carbon released as

benzene and formic acid from theAtacama soils varied from ~13,000 ppb inthe driest sites to ~85,000 ppb in thewettest sitesmuch higher than the detec-tion limits of the Viking pyrolysis instru-ments (3).

Is the martian soil completely devoidof organic matter, as concluded by theViking team? Or was the protocol usedby the Viking pyrolysis instrument lim-ited in its detection ability (19)? Theanswer to this question will profoundlyaffect our view of the presence orabsence of life on Mars. Future missionsto Mars should reanalyze, as a high prior-ity, the total concentrations of organiccarbon and the biologically importantelement nitrogen in the soils. This willcontribute to our understanding of thesoils mode of formation, its reactivityand toxicity, utility as a resource, andastrobiological connections.

The above questions notwithstanding,the Atacama Desert is a unique spot onEarth. It behooves the scientific commu-nity to carefully control and preserve sec-tions of this environment for future study.Selected sites in this deser t could bedeclared a nature preserve to preventthe contamination of this ecosystem byexcessive human act ivi ty. Thus pre-

served, these sites could continue to beused as a testing ground for sterilizationand quarantine protocols developed forvehicles and missions sent to Mars andfor careful f ield experimentation withsamples returned from Mars by futuremissions.

References and Notes

1. P.Toulmin III et al., J. Geophys. Res. 82, 4625 (1977).2. B. C. Clark et al., J. Geophys. Res. 87, 10059 (1982).3. K. Biemann et al., J. Geophys. Res. 30, 4641 (1977).4. G. V. Levin, P. A. Straat, J. Geophys. Res. 82, 4663

(1977).5. A. Banin, B. C. Clark, H.Wnke, in Mars, H. H. Kieffer, B.

M. Jakosky, C.W. Snyder, M. S. Matthews, Eds. (Univ. ofArizona Press,Tucson,AZ, 1992), pp. 594625.

6. R. Rieder et al., Science 278, 1771 (1997).7. G. Klingelhfer et al., Science 306, 1740 (2004).8. S.W. Squyres et al., Science 305, 794 (2004).9. S.W. Squyres et al., Science 306, 1698 (2004).

10. R.V. Morris et al., Science 305, 833 (2004).11. R. Gellert et al., Science 305, 829 (2004).12. R. Rieder et al., Science 306, 1746 (2004).13. A. Banin et al., J. Geophys. Res. 102, 13341 (1997).14. N. J.Tosca et al., J. Geophys. Res. 109, E05003 (2004).15. S.W. Squyres et al., Science 306, 1709 (2004).16. R. G. Burns, D. S. Fisher, J. Geophys. Res. 95, 14415

(1990).17. R. Navarro-Gonzlez et al., Science 302, 1018 (2003).18. R. M. Maier et al., Science 306, 1289 (2004).19. S.A. Benner et al., Proc. Natl. Acad. Sci. U.S.A. 97, 2425

(2000).20. Supported in part by NASA Astrobiology Institute/SETI

Institute Astrobiology Project NNA04CC05A.

10.1126/science.1112794

Awell-known dermatologist oncenoted, No one ever dies from skinfailure. Indeed, the skin faithfully

renews itself throughout our lifetime andwe usually take for granted its remarkableability to expand during wound healing.This capacity for proliferation dependson stem cells located in hair follicles andin the epidermis, the outermost layer ofthe skin (see the figure) (1, 2). Stem cellsin these areas are distinguished from sur-rounding epidermal cells by their essen-tially quiescent nature. Stem cells occa-sionally divide to maintain their presencein the skin (a process called renewal)but they also generate rapidly proliferat-

ing cells called transient or transientamplifying cells. These cells are commit-ted to differentiate and are necessary fortissue homeostasis and repair. Controll-ing the transition of a stem cell to a tran-sient amplifying cell is of utmost impor-tance to the skin. Too many transientamplifying cells may cause hyperplasiaor thickening of the epidermis. On theother hand, skin thinning and atrophy canresult from too few transient amplifyingcells . These cel ls must themselvesundergo terminal differentiation as theymove to superficial positions in the skinbefore ultimately being sloughed fromthe surface. The well-orchestrated transi-tions between these cellular states requirefine control, because alterations in theseevents could lead to cancer, nonmalig-nant growths, or poor tissue healing.

On page 933 of this issue, AznarBenitah et al. (3) convincingly show thatdeletion of Rac1, a small GTP-bindingprotein of the Rho family, has a profoundeffect on skin homeostasis. After condi-t ional delet ion of Rac1 in mice, the

authors noted transient hyperprolifera-tion and then premature terminal differ-entiation of epidermal cells. The epider-mis f irst thickened, then thinned, andultimately the skin failed to functionproperly. Mice developed cysts and hairloss. This series of events suggests thatloss of Rac1 prevents stem cell renewal.This consequently would result in con-version of s tem cel ls into t ransientamplifying cells, causing hyperplasia.The f inding implies that in vivo, Rac1normally maintains the epidermal stemcell niche by suppressing the switch thatpromotes the f irst transition event tocommitted cell populations.

A second complementary explanationfor the skin-thinning phenotype is anincrease in the later transition of tran-sient amplifying cells to terminal differ-entiation. This could also result in deple-tion of the stem cell reservoir and is con-sis tent with a dynamic equi l ibr iummodel of the stem cell, transient amplify-ing, and terminally differentiated cellpopulations (4).

The striking effect of Rac1 deletion onskin homeostasis is likely not mediated byeffects on stem cells alone. Rac1 isexpressed in all skin cells of the basal layerof the epidermis, not just the stem cells.One possibility is that expression of Rac1 is

D E V E L O P M E N TA L B I O L O G Y

Rac1 Up for Epidermal Stem CellsG. Paolo Dotto and George Cotsarelis

G. P. Dotto is at the Institute of Biochemistry,University of Lausanne, Chemin de Bovaresses 155,CH-1066 Epalinges, Switzerland, and the CutaneousBiology Research Center, Massachusetts GeneralHospital, Charlestown, MA 02129, USA. G. Cotsarelisis in the Department of Dermatology, KligmanLaboratories, University of Pennsylvania School ofMedicine, M8 Stellar-Chance Building, 422 CurieBoulevard, Philadelphia, PA 19104, USA. E-mail:cotsarel@mail.med.upenn.edu

5 AUGUST 2005 VOL 309 SCIENCE www.sciencemag.org

P E R S P E C T I V E S

Published by AAAS

DOI: 10.1126/science.1112794, 888 (2005);309 Science

Amos BaninThe Enigma of the Martian Soil

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 1, 2015 www.sciencemag.org (this information is current as ofThe following resources related to this article are available online at

http://www.sciencemag.org/content/309/5736/888.full.htmlversion of this article at:

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

http://www.sciencemag.org/content/309/5736/888.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/309/5736/888.full.html#ref-list-1, 10 of which can be accessed free:cites 18 articlesThis article

7 article(s) on the ISI Web of Sciencecited by This article has been

http://www.sciencemag.org/content/309/5736/888.full.html#related-urls1 articles hosted by HighWire Press; see:cited by This article has been

http://www.sciencemag.org/cgi/collection/enhancedEnhanced Content

subject collections:This article appears in the following

registered trademark of AAAS. is aScience2005 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 A

ugus

t 1, 2

015

ww

w.s

cien

cem

ag.o

rgD

ownl

oade

d fro

m