microbial habitability of icy worlds

Microbial Habitability of Icy WorldsAs our exploration of space begins its sixth decade, we have new toolsand techniques to probe questions of planetary habitability

John C. Priscu and Kevin P. Hand

For most of Earth’s history, life wasmicroscopic and, even today, micro-organisms dominate the planet.Hence, we believe that, if life existsbeyond Earth, it likely started as mi-

croorganisms and may remain at this stage.Much of contemporary astrobiological researchfocuses on the metabolic potential of microor-ganisms and their ability to inhabit extremeenvironments.

The search for life beyond Earth prioritizesthe search for liquid water because water onEarth is closely associated with life. However,our understanding of where liquid water can befound is changing. Moons in the outer solarsystem, including Europa, Ganymede, andEnceladus that orbit either Jupiter or Saturn,although covered with ice, carry subsurface

oceans containing many times the volume ofliquid water on Earth and may provide thegreatest volume of habitable space in our solarsystem. On many of these worlds, water is main-tained as a liquid through radiogenic decay,tidal energy dissipation, and the mere fact thatice floats and serves as a good insulator. Theseoceans are there today and have likely persistedfor much of the history of the solar system,providing key environments in which to searchfor extant life beyond Earth—life from a second,independent origin. The recent discoveries ofmetabolically active microorganisms in subgla-cial environments on Earth provide useful ana-logues in that search.

Of these worlds, Europa holds perhaps thegreatest potential as a modern habitat for micro-bial life, and its relatively thin ice shell of about

5–15 km eases the technical challenges oftrying to detect such life. Along with a liquidocean, Europa also likely harbors a rockyseafloor that can supply energy and ele-ments needed to drive metabolism (Fig. 1).With the goal of investigating the habitabil-ity of Europa, the National Aeronauticaland Space Agency (NASA) has recentlyidentified a mission to Europa as secondonly to a Mars sample-return mission. Here,we focus on the potential for microbial hab-itability on Europa, drawing on what weknow about microbial life in Earth’s sub-iceenvironments.

Assessing the Habitability

of Ocean Worlds

We know of three key requirements forhabitability—liquid water, a suite of biolog-ically essential elements, and a source ofenergy (Fig. 2). The subsurface liquid water

Summary

• Although covered with ice, several moons of theouter solar system carry subsurface oceans con-taining many times the volume of liquid wateron Earth and may provide the greatest volumeof habitable space in our solar system.

• Europa holds perhaps the greatest potential as amodern habitat for microbial life.

• We know of three key requirements for habit-ability—liquid water, a suite of biologically es-sential elements, and a source of energy.

• Functional subglacial ecosystems in Antarctica,in concert with what we know about the geo-chemistry of Europa, provide a compelling casethat its sub-ice ocean could support microbiallife.

• Discovering life on Europa or elsewhere in theouter solar system would have an enormousimpact on science and society.

John C. Priscu isProfessor of Ecol-ogy in the Depart-ment of Land Re-sources &Environmental Sci-ences, MontanaState University inBozeman, Montana.Kevin P. Hand is ascientist at the JetPropulsion Labora-tory, California Insti-tute of Technology,Pasadena, Califor-nia.

Volume 7, Number 4, 2012 / Microbe Y 167

reservoir of Europa has likely persisted for muchof the moon’s nearly 4.5 billion years. By virtueof its contact with a rocky floor, the 100-kmdeep ocean could be geochemically suitable forlife. Though the ocean lies beneath several tomany kilometers of ice, the global nature of theocean implies that much of this world could be

inhabited if the chemical conditions areappropriate.

In addition to those three key re-quirements, several other conditionsshould be considered, including wateractivity, temperature, radiation, pH, sa-linity, and temporal stability. In termsof energy, the environment should be ina state of energetic disequilibrium topower life either through chemical orphoton-catalyzed reactions. The avail-ability of free energy is a critical deter-minant of whether metabolism, repair,growth, and reproduction can occur.The mantra “follow the energy” hasbecome a theme that constrainsNASA’s “follow the water” approach,which has driven the search for life be-yond the Earth.

Europa as a Microbial Habitat

The ocean of Europa is not particularlyextreme in terms of temperature andpressure. The temperature of the watermay be suppressed to about �20°C bythe dissolution of salts, but ultimatelythe temperature hovers near the freez-ing point. The pressures, despite theocean being about 100 km deep, are notthat great because the gravitational ac-celeration is less than one-seventh thatof our more massive Earth. The 110MPa pressure in the 11-km-deep Mari-nas Trench on Earth, which is known tosupport an active microbial assem-blage, is comparable to the seafloor of a100-km ice shell plus ocean on Europa.

Europa is composed of chondriticmaterial, that is, space rocks rich inbiologically essential elements. The sur-face chemistry is dominated by sulfurand water, making the cycling of sulfuron Europa important for its potentialhabitability. Spectra from the GalileoNear Infrared Mapping Spectrometer

(NIMS) indicate regions where hydrated sulfateconstitutes up to 90% of the numerical molecu-lar surface abundance. Moreover, radiolysis(chemistry driven by radiation processing) likelydrives a sulfur cycle, forming surface reservoirsof hydrated sulfate, sulfur dioxide, elementaland polymerized sulfur, and possibly traces of

F I G U R E 1

Views of Europa. (A) Enhanced composite image revealing the water-ice shell of Europa.The chemistry of the brown-red regions is largely unknown but oxidized sulfur speciesare known to be a key constituent. These areas may represent rocky material derivedfrom the interior, implanted by impact, or from a combination of interior and exteriorsources. The bright feature containing a central dark spot in the lower third of the imageis a young impact crater �50 km in diameter. (B) Cutaway view showing the internalstructure of Europa. The interior characteristics are inferred from gravity field andmagnetic field measurements by NASA’s Galileo spacecraft. Europa’s radius is 1,565 km,slightly smaller than our Moon. Europa has a metallic (iron, nickel) core (shown in gray).The core is surrounded by a silicate shell (shown in brown). The silicate layer of Europais in turn surrounded by a shell of water in ice or liquid form (shown in blue and white).The surface layer of Europa is shown as brown to indicate that it may differ from theunderlying layers. (C) Detail of surface units on Europa that may indicate transfer ofmaterial between the ocean and ice shell. Such areas would be prime targets for futurelander missions designed to detect life. (a) the “Puddle” resulted from surface water thatwas once liquid and refroze. The crater in the middle of the frozen puddle is caused bya meteorite impact. The puddle might have formed as water melted from the heat of theimpact or when water bubbled up from the subsurface ocean; (b) Castalia Maculaconsists of unusually dark and reddish material, most of which is confined to a broadtopographic depression 350 m deep located between two large uplifted domes 900 and750 m high, to the north and south, respectively. The preservation of topography at thebottom of Castalia Macula indicates that dark material initially filled the depression to acertain depth but was subsequently removed via drainage, resulting in a dark stain up tothe original equipotential surface; (c) Conamara Chaos is a region of chaotic ice whererafts of ice have moved around and rotated; (d) high resolution of boxed inset in (c).Image credit: NASA/JPL.

168 Y Microbe / Volume 7, Number 4, 2012

hydrogen sulfide. Some sulfur on Eu-ropa comes from volcanoes on thenearby satellite of Jupiter, Io. As such,volcanism on Io is influencing the hab-itability of Europa.

From a bioenergetics standpoint, thecoupling of surface oxidants with hy-drothermal seafloor reductants couldbe key for Europa’s habitability (Fig. 3).Whether Europa is geologically activetoday and cycles surface oxidants likesulfate into the ocean remains an openquestion. Based on the paucity of im-pact craters, Europa’s ice shell is con-sidered geologically young, making itreasonable to expect exchanges be-tween the ice shell and ocean.

When Europa formed, quenched hy-drothermal fluids rich in hydrogen,methane, and organic compoundslikely coupled with dissolved sulfate,yielding energy like that found in sul-fate-reducing microbial ecosystems inanoxic environments on Earth:

SO42��2H��4H2(aq)3H2S(aq)

�4H2O(l)

From estimates based on known mi-crobes, these reactions would be capa-ble of producing about 1016 kg of totalbiomass throughout the Europan oceanover its history. This total is small com-pared to what happens on Earth, wherephotosynthesis dominates and pro-duces about 1014 kg of biomass peryear. A sulfate and carbon flux from theice shell would serve to maintain a cycle ofsulfate reduction on a hydrothermally activeEuropa.

Polar Sub-Ice Habitats

The 200 or more Antarctic subglacial lakes, esti-mated to collectively contain about 7% of all lakewater on Earth, provide examples of how lifeadapted to cold, dark environments comparableto Europa. Many of these lakes lie beneath morethan 3 km of ice and have had no direct contactwith the atmosphere for more than 15 millionyears. The largest is Lake Vostok, which is about1,000 m deep and holds about 5,400 km3 ofwater, making it the third deepest lake on our

planet and the sixth largest in terms of volume(Fig. 3). Water remains liquid in the lake owing tobackground geothermal heating, the insulatingproperties of the overlying ice sheet, and pressure-induced lowering of the freezing point. Data fromVostok accretion ice, lake water frozen to theunderside of the Antarctic ice sheet above the lake,reveal an active microbial consortium within thesurface waters of the lakes with cell abundanceranging from 150 to 460 cell ml-1. Sequence datafrom DNA encoding for small-subunit ribosomalRNA (16S rRNA) reveal phylotypes related to the�-, �-, and �-Proteobacteria, Firmicutes, Bacte-roidetes, and Actinobacteria. If those microbes aretypical of the lake microbiota, the microorganismswithin Lake Vostok are not evolutionarily distinct.The phylotypes from Vostok are related to aerobic

F I G U R E 2

The habitability of Europa. At present, our understanding of the conditions necessary forlife can be distilled down to three broad requirements: (1) a sustained liquid waterenvironment, (2) a suite of elements critical for building life (e.g., C, H, N, O, P, S), and(3) a source of energy that can be utilized by life. Here we show how these “pillars ofhabitability” intersect with our current understanding of the conditions on, and within,Europa.


and anaerobic bacteria with metabolisms dedi-cated to iron and sulfur respiration or oxidation.This similarity implies that these elements play akey role in the bioenergetics of microorganisms inLake Vostok, whose likely key chemoautotrophicmetabolic pathways include:

4FeS2�15O2�14H2O716H��8SO42�

�4Fe(OH)3

Oxic------------------------------------------------------------

Anoxic

FeS2�14Fe3��8H2O715Fe2��2SO42�

�16H�

These substrates can derive from physical glacialprocesses and do not require geothermal input.The pathways could supply organic carbon andsupport heterotrophic metabolisms that use O2,NO3

�, SO42�, S0, or Fe2� as electron acceptors.

The chemoautotrophic reactions fix carbon diox-ide using iron and sulfur as both electron donorsand electron acceptors. The pathways also indi-cate that these transformations may occur acrossan aerobic/anaerobic boundary. Organic carbonproduced by chemoautotrophic metabolism could

then fuel heterotrophic metabolism within thelake.

If similar microbial ecosystems exist through-out Antarctica’s sub-ice environment, this unex-plored habitat may contain a huge unexploredpool of bacterial carbon. Further, these subgla-cial bacteria might play an important role inmineral weathering beneath the Antarctic icesheet. Direct sampling of these subglacial lakeswill enable us to develop unequivocal conclu-sions about the phylogenetic and metabolic di-versity in these ecosystems.

Blood Falls, Subglacial Outflow

Another example of a subglacial ecosystem in-volving sulfur and iron intermediates that drivemicrobial metabolism is Blood Falls, Antarctica,whose subglacial outflow originates beneath theTaylor Glacier in the McMurdo Dry Valleys(Fig. 4). A warming event during the PlioceneEpoch 3–5 million years ago enabled marinewaters to enter the Taylor Valley. As the TaylorGlacier advanced during the late Pliocene orPleistocene, those marine waters were sealedbeneath the glacier, where cryoconcentrationand chemical and biological weathering pro-cesses produced a suboxic subglacial brine three

F I G U R E 3

Schematic showing the relationships among ice, water, and rock for Europa and Subglacial Lake Vostok. Microbial metabolism in bothsub-ice systems can be driven by coupling surface oxidants with reductants associated with the rocky seafloor.


times saltier than seawater and rich iniron and sulfur. This environment hasnot been in direct contact with the at-mosphere since it was sealed severalmillion years ago.

A majority (74%) of clones and iso-lates from Blood Falls share high 16SrRNA gene sequence homology withphylotypes from marine systems. Bacte-rial 16S rRNA gene clone libraries aredominated by a phylotype with 99% se-quence identity with Thiomicrospira arc-tica, a psychrophilic marine autotrophicsulfur oxidizer. The remainder of the li-brary contains phylotypes related to theclasses �-proteobacteria, �-proteobacte-ria, and �-proteobacteria and the divisionBacteroidetes. The library includes cloneswhose closest cultured relatives metabo-lize iron and sulfur compounds.

These findings are consistent withthe high iron and sulfate concentra-tions detected in Blood Falls, whichare likely due to the interactions of thesubglacial brine with the underlyingiron-rich bedrock. That the majorityof clones in the Blood Falls library arerelated to the obligate chemlithoau-totroph Thiomicrospira arctica re-veals the capacity for subglacial che-mosynthetic primary production.Thiomicrospira may provide new organic car-bon in the absence of sunlight and at perma-nently low temperatures.

Thus, the bacterial consortia below the Tay-lor Glacier grow chemoautotrophically or che-moorganotrophically by harvesting energy frombedrock minerals, or the assemblage may growheterotrophically on ancient marine organics byrespiring Fe(III) or SO4

2�. Isotopic measure-ments of sulfate, water, carbonate, and ferrousiron in concert with functional gene analyses ofadenosine 5�-phosphosulfate reductase implythat a microbial consortium facilitates a cata-lytic sulfur cycle resulting from a limited photo-synthetic carbon supply, producing a systemrich in electron acceptors relative to electrondonors despite being anaerobic. This situationproduces an environment that is reduced, butnot sulfidic.

The discovery of functional microbial ecosys-tems in Lake Vostok and Blood Falls, oncethought to be inhospitable, together with what

we know about the geochemistry of Europa,provide a compelling case that Europa’s sub-iceocean might support microbial life. Thus, thephylogenetic and metabolic diversity here onEarth can guide our search for organisms onEuropa and other ice-covered moons of theouter solar system.

Perhaps a Second Origin of Life

According to the rock record, Earth was inhab-ited within a billion years of being formed, andthose early microorganisms were as complexand competent in their cellular and molecularfunctions as those of today. Although we knowlittle of how fast life evolves, the temporal win-dow of the Europan ocean offers ample time forcomplex cellular structure and biogeochemistryto develop. Without understanding how ourown tree of life developed, we should not readtoo much into the chemistry of Europa and life’sorigins there. Nevertheless, such questions are pre-cisely why Europa is such a prime astrobiological

F I G U R E 4

Blood Falls, an iron-rich subglacial discharge from the Taylor Glacier, McMurdo DryValleys, Antarctica. Microorganisms in this subglacial system couple iron respiration to acatalytic sulfur cycle that creates no net sulfide. The result yields a subglacial ferrous-richbrine that becomes oxidized as it reacts with oxygen in the atmosphere as it isdischarged.


target—it poses a testing ground for a second,independent origin of life in our solar system.Informally, scientific wisdom suggests that:

Liquid water � Biologically essential ele-ments � Energy � Catalytic surfaces � Time3Life

Even if microorganisms are absent from aEuropa that fully satisfies the left-hand side ofthat expression, we could gain insight into the

conditions that led to life on Earth. Similarly, ifwe discover life on Europa, we could then begina rigorous cross-comparison to investigate theconditions leading to the emergence of life onboth worlds. Such a discovery would have anenormous impact on science and society andwould provide us with another world throughwhich to advance our understanding of howmicroorganisms interact with their environmentand how life evolves.

ACKNOWLEDGMENTS

We are grateful for funding from the NASA Astrobiology Institute (NAI5–0021) and the Astrobiology of Icy Worlds node atthe Jet Propulsion Laboratory. This NASA grant together with NSF grants OPP-0839075, OPP-0838933, and OPP-1027284allowed us to generate many of the ideas included in this paper. We also thank Jill Mikucki and Brent Christner for producingmuch of the Antarctic data.

SUGGESTED READING

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microbial habitability of icy worlds

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