The same is true for hydrothermal vents (Tunnicliffe, 1992) and some deep underground environments (Chapelle et ah, 2002), where thermal energy is the ultimate source of reducing power. Anaerobic metabolism is responsible for the abundance of N2 in the atmosphere; otherwise N2-fixing bacteria would have consumed most of the N2 pool long ago. The contribution of different anaerobic metabolic pathways to carbon metabolism varies temporally and spatially due to changes in the abundance of electron donors and acceptors (Figure 1).
Regeneration at the aerobic-anaerobic interface can supply a large portion of terminal electron acceptors consumed in anaerobic metabolism. The free energy yield of the reaction is provided for pathways that do not require light. Given some relatively recent discoveries of new C02 assimilation pathways (eg, the hydroxypropionate cycle and anaerobic ammonium oxidation) and the growing interest in deep subsurface microbiology, new C02 incorporation pathways may be revealed in the near future. .
METHANE
In both cases, the waste product, CH4, still contains potential energy in the form of reducing equivalents that can support additional anaerobic metabolism. Increasing concentrations of CH4 during periods of increased solar insolation and interglacial warming have greatly increased global warming in the past (Petit et al., 1999), and there is concern that this will occur in the future. Changes in atmospheric CH4 content have historically been accompanied by changes in the area of northern and tropical wetlands (Blunier et al., 1995; Chappellaz et al., 1993).
Methanes have been shown to play this role in the breakdown of alkanes, a group of particularly stable hydrocarbons abundant in fossil fuels (Anderson and Lovley, 2000; Zengler et al, 1999). They are the largest and most diverse group in Archea, which is phylogenetically separate from the other two domains of life, Bacteria and Eukaryota. It has been suggested that a quinone-like role in electron transfer may be fulfilled by phenazine compounds in the Methanosarcinales (Abken et al., 1998; Deppenmeier et ai, 1999).
As the proportion of soil organic carbon >2 mm decreased rapidly with depth, 70% of total CH4 production occurred in the upper 5 cm of the soil profile. In other cases, depth-dependent decreases in potential CH4 production are not associated with changes in the quality of the soil organic carbon pool. However, the relative contributions of the two pathways can vary considerably across ecosystems, seasons, and depths.
The size of the labile carbon pool is an important predictor of methanogenic pathways in marine sediments (Blair, 1998). In the absence of oxidation, and provided that the relative contributions of the methanogenic pathways differ in time or space, the relationship between 3D and 513C is negative. Although changes in the relative contributions of the two pathways coincide with shifts in the structure of methanogenic communities (Chin et al., 1999b; . Fey and Conrad, 2000), this is probably not a direct response of methanogens to temperature.
NITROGEN
For example, nitrogen export from the Mississippi River Basin has been linked to the expansion of anaerobic sediments in the Gulf of Mexico (Rabalais et al., 2002). This contrasts with a similar survey by Rosch et al. 2002) in which denitrification was not a genetic trait of most of the uncultivated bacteria in a hardwood forest soil. Their denitrifying enzyme system is linked to the mitochondrial electron transport chain where it produces ATP (Kobayashi et al., 1996).
They do not grow under strict anaerobic conditions, but require a minimal amount of 02 (Zhou et al., 2001). Because fungi represent a large proportion of the microbial biomass in soil (Ruzicka et al., 2000), they may be an important source of N20 in some terrestrial ecosystems. For example, denitrification enzyme activity in a temperate hardwood forest was higher in wet years than dry years (Bohlen et al., 2001).
Glucose additions stimulated denitrification in 11 of 13 agricultural soils that were treated with manure (Drury et al., 1991). Nitrification is generally considered to be the dominant source of NO in upland soils, but there are studies suggesting the opposite (reviewed by Ludwig et al., 2001). Green rusts are Fe(II)-Fe(III) precipitates that form in non-acidic, Fe(II)-rich soils and sediments (Hansen et al., 1994).
It is clear that NO^-N is readily consumed in the anammox process (Mulder et al., 1995; Dalsgaard and Thamdrup, 2002), although it is first reduced to NO^. In a review of the topic, Wrage et al. 2001) proposed that the highest contributions from nitrifying denitrifiers are likely to occur under conditions of low carbon and nitrogen content. Unlike the abiotic reaction, chemolithoautotrophic denitrification coupled to NO^~ proceeds rapidly under the low-temperature, near-neutral pH conditions that are typical of the Earth's surface (Weber et al., 2001) (Sect.
The reaction may only be favorable with certain forms of MnO2 (Hulth et al., 1999) or high levels of NH|.
IRON AND MANGANESE
Some Fe(III)-reducing organisms, particularly members of the Geobacteraceae family, can reduce heavy metal contaminants such as U(VI) (Holmes et al., 2002). Trace metals form surface complexes or co-precipitates with Fe(III) and Mn(IV) oxides and are released during the reduction of Fe(III) and Mn(IV) (Zachara et al., 2001). These minerals are also produced by Fe(III)-reducing bacteria during ferrihydrite reduction (Zachara et al., 2002).
Fe(III)-reducing bacteria growing on ferrihydrite can produce extracellular fine-grained magnetite (Fe304) (Lovley et al., 1987; Fredrickson et al., 1998). Shewanella oneidensis (formerly S. putrefaciens) produced and deposited an unidentified iron mineral intracellularly (Glasauer et al., 2002). The capacity for dissimilatory Fe(III) and Mn(IV) reduction is widely distributed among the subdivisions of the Bacteria, including all subclasses of the Proteobacteria ( Coates et al., 2001 ) and some hyperthermophiles.
More than 40 isolates have been characterized linking anaerobic growth to disparate Fe(III) respiration ( Coates et al., 2001 ). Complete oxidation of organic carbon to C02 is found in three of the four genera in the Geobacteraceae family (Lovley, 2000c), and phylogenetically distinct genera such as Geovibrio and Deferribacter (Greene et al., 1997). Bacterial cells adsorbed to mineral surfaces also inhibit Fe(III) reduction rates (Urrutia et al., 1999).
Other complexing agents such as hydroxamate have no effect on Fe(III) dissolution rates (Holmen et al., 1999). Nevertheless, no extraction technique is completely discriminatory for a particular metallic phase or mineral (Zachara et al., 2002). Stucki et al., 1996) and may therefore support a substantial part of the anaerobic microbial carbon metabolism on the planet.
Microbial oxidation is considered the primary mechanism of Mn(II) oxidation in circumneutral freshwaters (Ghiorse, 1984; Nealson et al., 1988).
SULFUR
Sulfate-reducing bacteria are anaerobes located at the end of the anaerobic food web, where they act as an important cog in the sulfur and carbon cycles. The first isolated user of acetate was a Gram-positive sporulating bacterium of the genus Desulfotomaculum (Widdel and Pfennig, 1977). The family Desulfobacteriaceae is much less distinct and includes several genera (perhaps > 20), including many complete oxidizing species (Castro et al., 2000; Widdel and Bak, 1992).
Because of the complex nature of the anaerobic bacterial food web, it is generally thought that SO2.-. Sulfate reducers in salt marsh sediments may comprise >30% of total bacteria (Hines et al, 1999). Depth increases in reduced sulfur compounds and the abundance of SO4-reducing bacteria are useful as comparative indicators of the SO|~ reduction process, but they are poor indicators of the actual rate of activity.
Anaerobic CH4 oxidation supports a large fraction of the SO4" reduction in some marine sediments (Table 6). The ability to use organic disulfide molecules, such as cysteine or glutathione, as terminal electron acceptors appears to be limited to certain members of the S° - reducing bacteria (Pfennig and Biebl, 1976) In fact, most of the sulfur-reducing bacteria known belong to the Archaeal domain (Hedderich et al., 1999).
However, sulfur-reducing eubacteria are quite diverse and are found within other subclasses of the Proteobacteria, many of which are not phylogenetically related to SO4-reducers (Lau et al., 1987; Schleifer and Ludwig, 1989). Thiosulfate appears to be a key component of the sulfur cycle in sediments because it can be oxidized, reduced and disproportionated. Members of the Proteobacteria, especially the a group, appear to be important DMS producers in the ocean (Gonzalez et al., 1999).
In some Beggiatoa spp. sulfide can be oxidized with O2 or NO^ as an electron acceptor, and N2 is a nitrate reduction product (Sweerts et al., 1990).
COUPLED ANAEROBIC ELEMENT CYCLES
Methane oxidation in the surface soil layer of a flooded rice field and the effect of ammonium. 1994) Effects of headwater sulfate concentration on sulfate reduction and sulfur storage in lake sediments. 1999) Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha subclass of the class Proteobacteria.
The role of certain infaunal and vascular plants in mediating redox reactions in marine sediments. Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. The role of microbial mats in reduced gas production on early Earth.
The cyctochrome system of sulfate-reducing bacteria. 1981) Seasonal rates of methane oxidation in anoxic marine sediments. 1985). A thiosulfate shunt in the sulfur cycle of marine sediments. 1991) Pathways and microbiology of thiosulfate transformations and sulfate reduction in a marine sediment (Kattegat, Denmark). 1988) Seasonal cycling of sulfur and iron in pore water in a Delaware salt marsh. 1991) Sulfur speciation and sulfide oxidation in the water column of the Black Sea. 1992).
1999) Sulfur speciation and sulfide oxidation in the Black Sea water column. 2001) Chemical speciation drives hydrothermal vent ecology. 1995) Diagenesis of organic matter components in vascular plants during burial in lake sediments. 2002) Black Sea microbial reefs fueled by anaerobic oxidation of methane. 1992b) Importance of methane-oxidizing bacteria in the methane budget as revealed by the use of a specific inhibitor.
Alkyl sulfonic acids in the atmosphere. 2001) Degradation of model lignin and lignin composition under sulfate-reducing conditions. 1997) Seasonal changes in the relative abundance of uncultivated sulfate-reducing bacteria in a salt marsh sediment and rhizosphere of Spartina alterniflora. Potential methane production and rates of methane oxidation in peatland ecosystems of the Appalachian Mountains, United States.
