Sulfur Biogeochemistry—Past and Present

Microbially mediated sulfur-redox 21Mars and EuropaThe Earth provides the only irrefutable evidence of life inour solar system. To date, the search for signs of extraterrestriallife has focused on Mars and the Jovian satellite Europa. Onthese extraterrestrial bodies, hydrothermal systems may haveonce existed (or may still exist) (Farmer, 1996; Newsom et al.,1999; Chyba, 2000; Greenberg and Geissler, 2002; Rathbun andSquyres, 2002), and, like on early Earth, the microbial catalysisof redox reactions among S-bearing compounds seems plausible.It is generally hypothesized that the putative extraterrestrial lifeis unicellular and carbon-based, requiring liquid water and geochemicalenergy sources. Evidence that liquid water existed onthe surface of Mars some time in its history is mounting, as is theevidence for present or past subsurface ice. For example, NASA’sMars Orbital Laser Altimeter (MOLA) on the Mars Global SurveyorMission (MGS) revealed high-resolution topographic datasuggesting that the Martian highlands have undergone extensivefluvial resurfacing, particularly in the Margaritifer Sinus region(Hynek and Phillips, 2001). This area, located near the easternend of Valles Marineris, features well-preserved valleys andchannels, which provide strong evidence of past surface water,perhaps due to precipitation-recharged groundwater sapping(Carr and Chuang, 1997; Grant, 2000; Grant and Parker, 2002).Furthermore, the Thermal Emission Spectrometer (TES) on MGSdetected gray crystalline hematite (Fe 2O 3) in Meridiani Planumas well as in several minor deposits in other regions (Christensenet al., 2000). The formation of hematite on Earth usually requiresthe presence of liquid water, and the Meridiani Planum formationis hypothesized to have accumulated in an ancient, subaqueousenvironment (Edgett and Parker, 1997).Results from recent missions to Mars support the view thatMars was once wet. In particular, data obtained by NASA’sMars Exploration Rover Opportunity at Meridiani Planum havecorroborated this hypothesis with analyses of Martian rockswith high sulfate salt contents and hematite nodules, whichwere almost certainly deposited in a shallow lake environment(Arvidson, 2004; Morris et al., 2004; Squyres, 2004). Thesenew data indicate that the pertinent question is no longer ifliquid water existed on the surface of Mars, but rather howmuch and when. Indeed, various precipitation events, groundwater,and surface water (both liquid and frozen) may haveplayed a large role in shaping the surface of early Mars and inproviding putative habitable environments.In addition to apparent sources of surface and subsurfacewater, Mars exhibits morphological evidence of heat sources,many of which occur in association with evidence for liquidwater (Brakenridge et al., 1985; Gulick and Baker, 1990; Farmer,1996). A likely consequence of these concurrent events is theformation of hydrothermal systems, which on Mars could haveresulted from the interaction of groundwater or subsurface icewith magmatic intrusions (Gulick, 1998), or due to hydrothermalconvection in crater-lakes driven by the thermal anomaly producedby impact (Rathbun and Squyres, 2002).Europa, the second Galilean satellite of Jupiter, has potentialhydrothermal systems as well. Magnetometer data fromNASA’s Galileo probe have indicated the presence of a liquidwater ocean beneath Europa’s icy crust, and tidal dissipation inEuropa’s rocky core due to shared orbital resonance with its sistersatellites Io and Ganymede may lead to hydrothermal heating atthe water-rock interface (Chyba, 2000; Greenberg and Geissler,2002). Fluid mixing in postulated hydrothermal systems mayprovide (or have provided) the geochemical energy sources forprimary biomass synthesis and perhaps chemolithoautotrophy onEuropa as well as Mars.Both Mars and Europa have been the focus of geochemicalenergy modeling in recent years. McCollom (1999) identifiedpotential energy sources for autotrophs in a postulatedEuropan hydrothermal system, showing that methanogenesisfrom CO 2and H 2would be exergonic regardless whether theEuropan ocean is reduced and methane-rich or oxidized andsulfate- and bicarbonate-rich. In certain geochemical scenarios,sulfate-reduction would also supply sufficient energy to supportmicrobial metabolism. This view, however, is counter tothat of Gaidos et al. (1999), who argue that a lack of oxidantsin the Europan ocean would severely minimize the chances ofdiverse life surrounding hydrothermal systems. They furthernote that Fe(III)-reduction might support a simple communityof microorganisms, but methanogens, sulfate reducers, andaerobic chemolithoautotrophs are unlikely to thrive on Europa.It is worth reiterating that McCollom (1999) does not envisiona dense biota surrounding the hydrothermal vents on Europa,nor a complex community structure, but merely concludes thatgeochemical energy sources could support the emergence andpersistence of life in localized ecosystems. Similarly low, butnevertheless noteworthy energy yields were also computed byJakosky and Shock (1998), who inventoried the amount of geochemicalenergy from volcanic activity and mineral weatheringreactions in model Martian and Europan hydrothermal systems.They found that energy was sufficient on Mars for life to haveemerged, but also concluded that life is not now, and probablynever was, ubiquitous on Mars or Europa. More optimisticabout the biological potential of Mars is a recent study byVarnes et al. (2003), which asserts that substantial geochemicalenergy may be available in Martian hydrothermal systems,depending on the mineral composition of the host rock.ENERGETICS OF SULFUR-REDOX AT VULCANO: ACASE STUDY OF SHALLOW MARINE VENTSPyrodictium occultum emerged from a shallow-sea hydrothermalvent field at Vulcano as the first organism in pure cultureto grow optimally at temperatures >100 °C (Stetter, 1982; Stetteret al., 1983). Since then, a number of other archaea that cangrow at these temperatures have been cultured and characterized.They include Aeropyrum pernix; Caldococcus litoralis; Hyperthermusbutylicus; Methanopyrus kandleri; several membersof Pyrobaculum, Pyrococcus, Pyrodictium, and Thermococcus;