Sulfur Biogeochemistry—Past and Present

Microbially mediated sulfur-redox 192Several moderately thermophilic, nonmarine sulfate reducers are known, whichinclude the bacteria Thermodesulfobacterium commune (Zeikus et al., 1983),T. hveragerdense (Sonne-Hansen and Ahring, 1999), and Thermodesulfovibrioyellowstonii (Henry et al., 1994); T. hydrogenophilum is a moderately thermo philic,marine sulfate reducer isolated from Guaymas Basin (Jeanthon et al., 2002).In addition to S 0 -reduction, microbial sulfate-reductionhas been documented in marine hydrothermal systems, thoughrelatively little is known about the microbial populations thatcarry out this process in these habitats, especially at temperatures>80 °C. In heated deep-sea sediments of Guaymas Basin, Gulf ofCalifornia, very high microbial sulfate-reduction rates (up to 61µM SO 42−per day) were measured at temperatures ≥80 °C and infact as high as 110 °C (Fossing and Jørgensen, 1990; Gundersenet al., 1992; Elsgaard et al., 1994; Weber and Jørgensen, 2002).In shallow-marine hydrothermal sediments at Vulcano, similarlyhigh microbial sulfate reduction rates (72 µM SO 42−per day)were observed at 90 °C (Tor et al., 2003). Nonetheless, only afew sulfate reducers have been cultured from marine hydrothermalenvironments (Elsgaard et al., 1995; Sievert and Kuever,2000). Among the >130 species of sulfate-reducing archaea andbacteria that have been described to date, comprising membersof four bacterial phyla and one archaeal genus (Loy et al., 2002),only three marine hyperthermophiles are known. These speciesare exclusively members of the genus Archaeoglobus within theeuryarchaeota 2 and include organisms from both Guaymas Basin(A. profundus; Burggraf et al., 1990b) and Vulcano (A. fulgidus;Stetter, 1988). In addition to these isolates, Archaeoglobus spp.have also been identified by 16S rRNA sequence analyses ofGuaymas sediments (Teske et al., 2002) and in an in situ growthchamber deployed at a deep-sea hydrothermal vent on the Mid-Atlantic Ridge (Reysenbach et al., 2000). Finally, A. fulgidusand A. profundus were isolated from high-temperature oil fieldformation waters in the North Sea and Alaska (Stetter et al.,1993; Beeder et al., 1994; Nilsen et al., 1996).The vast majority of crenarchaeota, a considerable numberof hyperthermophilic euryarchaeota, and several high-temperaturebacteria carry the biochemical machinery required to oxidizeor reduce S-bearing compounds. A principal parameter thatgoverns the presence of active S-oxidizers and S-reducers in athermal environment is the availability of energy sources. In thisregard, it is not only vital to determine whether S-redox is exergonic,but also to quantify the amount of energy that is releasedin situ from specific reactions. If a reaction is endergonic, themicrobial catalysis of that reaction is a moot point. However,if the reaction of interest yields energy, it can be incorporatedinto a framework of microbial metabolism. The next level ofcomplexity then includes a comparison of energy-yields, firstfrom an array of S-redox reactions and ultimately from an evenlarger set of reactions that includes non-sulfur-bearing terminalelectron acceptors (TEAs) and electron donors. Quantifying theenergetics of this larger set is beyond the scope of this chapter;here, we concentrate on evaluating overall Gibbs free energies ofreaction (∆G r) for S-redox processes in a model system of shallow-marinehydrothermal activity. To put these calculations intocontext, however, we first briefly review the energetics of chemolithoautotrophyin experimentally investigated or computationallymodeled hydrothermal systems. Where possible, we focuson S-redox, but we also include some discussion of redox amongC-, N-, and Fe-bearing compounds.ENERGETICS OF CHEMOLITHOAUTOTROPHY INMARINE HYDROTHERMAL SYSTEMSIn this section, we consider the energetics of chemolithoautotrophyin a variety of hydrothermal environments, includingthose in the present abyssal and shallow sea, those on earlyEarth, and in putative systems on Mars and Europa. We do notpretend to give an exhaustive review of chemolithoautotrophyin terrestrial or extraterrestrial hydrothermal systems—past orpresent. Rather, we highlight examples that consider microbialprocesses within a geochemical framework. In many cases, apaucity of compositional data has precluded energy calculationsof S-dependent metabolisms or other simple chemolithoautotrophicreactions. Nevertheless, insight can be gleanedfrom models of abiotic organic synthesis and energetics ofchemoorganoheterotrophy, and we review these processes inseveral hydrothermal environments.Deep-Sea Hydrothermal SystemsMixing of hot, chemically reduced, slightly acid hydrothermalfluid with cold, oxidized, slightly alkaline seawater providesgeochemical energy in deep-sea vent systems (Jannasch,1985; Karl, 1995). This chemical disequilibrium, coupled withsluggish reaction kinetics for redox reactions, allows certainmicroorganisms to harness this energy (McCollom and Shock,1997). Thermodynamic calculations show that in such mixingenvironments at 21°N on the East Pacific Rise, for example, theaerobic oxidation of H 2S, CH 4, Fe 2+ , and Mn 2+ is exergonic atlow temperatures (40 °C) temperatures(McCollom and Shock, 1997). It also was shown thatthe reduction of SO 42−, S 0 , and CO 2with H 2as the electron donoris energy-consuming at low temperatures, but energy-yielding athigh temperatures. In vent plumes, however, the aerobic oxidationof S 0 , metal sulfides, and H 2, as well as chemolithotrophicsulfate-reduction, methanogenesis, and aerobic methanotrophyare all exergonic (McCollom, 2000).By comparison, the energetics of chemoorganoheterotrophyat deep-sea vents have not received much attention, largelybecause few studies have been published that give concentrationsof aqueous organic compounds. However, several studies evaluatedthe energetics of abiotic organic and biomolecule synthesis.In these investigations, dissolved H 2, present in the hydrothermalfluid due to high-temperature water-rock interactions, serves asthe electron donor in the reduction of CO 2(or HCO 3−). As anexample, thermodynamic computations revealed that the synthesisof 11 of the 20 common amino acids from CO 2, NH 4+, H 2S,