Microbial production and oxidation of methane in deep subsurface

Earth-Science Reviews 58 (2002) 367 – 395 www.elsevier.com/locate/earscirev

Microbial production and oxidation of methane in deep subsurface Svetlana Kotelnikova Department of Microbiology, St. George’s University, School of Medicine, P.O. Box 7, St. George, Grenada Accepted 11 July 2001

Abstract The goal of this review is to summarize present studies on microbial production and oxidation of methane in the deep subterranean environments. Methane is a long-living gas causing the ‘‘greenhouse’’ effect in the planet’s atmosphere. Earlier, the deep ‘‘organic carbon poor’’ subsurface was not considered as a source of ‘‘biogenic’’ methane. Evidence of active methanogenesis and presence of viable methanogens including autotrophic organisms were obtained for some subsurface environments including water-flooded oil-fields, deep sandy aquifers, deep sea hydrothermal vents, the deep sediments and granitic groundwater at depths of 10 to 2000 m below sea level. As a rule, the deep subterranean microbial populations dwell at more or less oligotrophic conditions. Molecular hydrogen has been found in a variety of subsurface environments, where its concentrations were significantly higher than in the tested surface aquatic environments. Chemolithoautotrophic microorganisms from deep aquifers that could grow on hydrogen and carbon dioxide can act as primary producers of organic carbon, initiating heterotrophic food chains in the deep subterranean environments independent of photosynthesis. ‘‘Biogenic’’ methane has been found all over the world. On the basis of documented occurrences, gases in reservoirs and older sediments are similar and have the isotopic character of methane derived from CO2 reduction. Groundwater representing the methanogenic end member are characterized by a relative depletion of dissolved organic carbon (DOC) in combination with an enrichment in 13C in inorganic carbon, which is consistent with the preferential reduction of 12CO2 by autotrophic methanogens or acetogens. The isotopic composition of methane formed via CO2 reduction is controlled by the d13C of the original CO2 substrate. Literature data shows that CH4 as heavy as 40x or 50x can be produced by the microbial reduction of isotopically heavy CO2. Produced methane may be oxidized microbially to carbon dioxide. Microbial methane oxidation is a biogeochemical process that limits the release of methane, a greenhouse gas from anaerobic environments. Anaerobic methane oxidation plays an important role in marine sediments. Similar processes may take place in deep subsurface and thus fuel the deep microbial community. Organisms or consortia responsible for anaerobic methane oxidation have not yet been cultured, although diverse aerobic methanotrophs have been isolated from a variety of underground niches. The presence of aerobic methanotrophs in the anoxic subsurface remains to be explained. The presence of methane in the deep subsurface have been shown all over the world. The flux of gases between the deep subsurface and the atmosphere is driven by the concentration gradient from depth to the atmosphere. However, methane is consumed by methanotrophs on the way of its evolution in oxidized environments and is transformed to organic form, available for further microbial processing. When the impact of subsurface environments to global warming is estimated, it is

E-mail address: [email protected] (S. Kotelnikova). 0012-8252/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 0 1 2 - 8 2 5 2 ( 0 1 ) 0 0 0 8 2 - 4

368

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

necessary to take into account the activity of methane-producing Archaea and methane-oxidizing biofilters in groundwater. Microbial production and oxidation of methane is involved in the carbon cycle in the deep subsurface environments. D 2002 Elsevier Science B.V. All rights reserved. Keywords: methane oxidation; methanotroph; methanogenesis; ‘‘biogenic’’ methane; stable isotopes; sediments; deep subsurface; igneous rock aquifer; oil-field; borehole; nuclear waste disposal

1. Introduction Methane, a highly reduced form of carbon, plays an important role in many geochemical processes in the Earth’s crust. Although methane is only a minor constituent of the atmosphere, it has received considerable attention because its role as a ‘‘greenhouse gas’’. Its concentration in the atmosphere is increasing at the alarming rate of about 1% year 1 (Cicerone and Oremland, 1988). Methane contributes approximately 15% to the present greenhouse warming (Christiansen and Cox, 1995). Estimate of the total release of methane to the atmosphere is 5.05  107 Mtonnes year 1 (Crutzen, 1991). This total is comprised of approximately equal contributions from: (1) natural wetlands; (2) rice paddies; (3) ruminants and termites; (4) coal and gas mining; (5) oceans, freshwaters and biomass burning (Crutzen, 1991). Microbial CH4 emissions from deep subsurface igneous and sedimentary rocks were not included in the estimates. CH4 is a common constituent in the deep subsurface. As much as 20% of the world’s natural gas resources is estimated to have been generated by microbes (Rice, 1993). Subsurface coal deposits, oil wells, natural gas storage in carbonate shelves, coal swamps, coastal plains, deep sea upwellings and hydrocarbon deposits are major sources of ‘‘biogenic’’ methane (Rice, 1993). Microbial methane oxidation is a biogeochemical process that limits the release of methane from anaerobic environments (Hanson and Hanson, 1996). The information about subsurface microbial methane oxidation is still very limited. In recent years, deep subsurface microbiology has received considerable attention because of industrial and domestic contamination of groundwater, and the consideration of the subterranean environment as a site for disposal of nuclear waste. The last decade of subterranean microbiological research greatly extended our knowledge about how the huge diversity of

the microbial world relates to microbial processes in the deep subsurface and the biogeochemical role of subterranean biota. Specific physiological groups of anaerobic microorganisms that can survive autotrophically have previously been detected in different subterranean sites (Zobell, 1958; Rozanova and Ivanov, 1996; Olson et al., 1981; Daumas et al., 1986; Stevens and McKinley, 1995; Fredrickson and Onstott, 1996). The Earth’s crust appears to be inhabited from the surface down to 3290 m or more below ground by microorganisms. The subsurface microbes that have been described until now are phylogenetically diverse and different from those found on the surface (Rozanova and Khydykova, 1974; Chapelle et al., 1987; Balkwill et al., 1989; Brockman et al., 1989, 1992; Fredrickson et al., 1989, 1991a,b; Pedersen et al., 1996a,b). The goals of this paper are: (1) to provide an overview of subsurface geological environments containing ‘‘biogenic’’ methane; (2) to summarize data on methanogenic Archaea in the deep subsurface; (3) to describe known processes of microbial methane oxidation in deep subsurface; (4) to contribute to our understanding of mechanisms of subsurface production and oxidation of this important greenhouse gas; and (5) to demonstrate the role of methane-related subterranean microorganisms in the global carbon cycle.

2. Definitions Two modes of origin for methane are commonly recognized: microbial production ‘‘biogenic’’ and ‘‘abiogenic’’ chemically produced (thermocatalytic) methane. ‘‘Abiogenic’’ or ‘‘thermogenic’’ methane may be derived from heating of kerogen, pyrolysis or inorganic reaction of water with hot ultramafic rocks and metals (Horita and Berndt, 1999). Essentially, at elevated temperatures, reduced minerals can

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

carry out reactions similar to that methanogenic enzymes (which utilize the same metals) catalyze at low temperatures. In geological literature, the gas generated by the decomposition of organic matter by anaerobic microbes at low temperatures is commonly referred to as ‘‘biogenic’’ gas. ‘‘Biogenic’’ gas is distinguished by its isotopic composition. Classical theory claims that naturally occurring ‘‘biogenic’’ methane has a very depleted stable carbon isotope (13C) content (Whiticar et al., 1986). However, the distinction between ‘‘biogenic’’ and ‘‘abiogenic’’ gases in geochemical literature that presents d13C is incorrect if autotrophic methanogensis is significant in the subsurface. Microbial production and oxidation of methane are performed by natural microbial populations involved in the biogeochemical cycle of carbon. Chemical reactions catalysed by microbes responsible for methane production and oxidation are described in Boone et al. (1993), Hanson and Hanson (1996), and Kotelnikova and Pedersen (1999). Methanogens are group of strict anaerobic microorganisms, that produce methane and phylogenetically affiliated to the kingdom Euarchaeota of the domain Archaea (Woese et al., 1990). Methanotrophs are unique in their ability to utilize methane as a sole sources of carbon and energy and phylogenetically are affiliated to the a, h and g subdivisions of kindom Proteobacteria in the domain Eubacteria (Hanson and Hanson, 1996).

3. Microbial life in the deep subsurface 3.1. Deep subterranean aquifers as environments for microbial life Deep subterranean groundwater occurs in thin granitic fractures or in pores between attached mineral grains of many igneous rocks. Groundwater ranges from fresh to brackish to highly saline. Groundwater has mineral compositions often unique to certain sites and depths. The deep subterranean environments may have characteristics that are not predictable based upon knowledge of surface habitats. Minerals and microelements are often more abundant and available in groundwater than in typical marine or lake water.

369

Deep groundwater is often highly pressurized and saturated with gases. One liter of granitic groundwater from 400 m depth contained 52– 75 ml of dissolved gas (Kotelnikova and Pedersen, 1998c, 1999). For continental crust, pressure and temperature increases by about 100 atm and 25 jC per kilometer, respectively. For oceanic crust, the temperature rises about 15 jC per kilometer. Dr. Thomas Gold calculated, assuming a maximum life-tolerant temperature of about 110 jC, that microbes could exist at depth of more than 3 km (Gold, 1993). He assumed that pores in rock account for about 3% of Earth’s upper crust and microbes occupy 1% of those pores. Later, it was calculated that the global carbon content in sunsurface Procariota (5.18  1014 kg) is comparable to carbon content in terrestrial plants (5.60  1014 kg)(Whitman et al., 1998). Many subterranean environments are anoxic (Sherwood Lollar et al., 1993b; Banwart, 1995; Romero et al., 1995) and thereby appropriate for anaerobic organisms. Some studies, when thorough methods of oxygen and redox measurements have been used, showed presence of oxygen in recharging and shallow groundwater (Madsen and Bollag, 1989; Bowman et al., 1993; Gascoyne et al., 1997). Aerobic activity and microorganisms have been found in the subsurface (Borzenkov et al., 1991; Bowman et al., 1993; Madsen and Bollag, 1989; Pedersen, 1996). Reduction of ¨ spo¨ Hard Rock Laboratory oxygen was detected in A groundwater (Kotelnikova and Pedersen, 1998c, 1999, 2000), that was the result of both aerobic and anaerobic processes. The increased free-energy yield associated with the use of oxygen as electron acceptor may explain the stimulatory effect upon exposure of anoxic groundwater to air (Fig. 1). Identification of factors that limit or determine microbial activity requires an immense amount of geological, hydrological and chemical information—all of which is extremely difficult to obtain due to the inaccessibility of this habitat. Enormous pressures and unique mineral compositions in groundwater makes the cultivation of the deep-dwelling inhabitants problematic. 3.2. How microorganisms survive in the deep subsurface The sun’s energy, a widely used energy source for autotrophic processes on the surface, is not available in

370

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

Fig. 1. Microorganisms occur in pores, fractures and aquifers in the deep subsurface (from Kotelnikova and Pedersen, 1999).

the subsurface. As a rule, the deep subterranean microbial populations dwell at more or less oligotrophic conditions (Table 1). However, concentrations of dissolved organic carbon (DOC) in subterranean environ-

ments are comparable to the concentrations in sea and freshwater aquifer systems inhabited by microorganisms. Thus, one of the energy sources for subsurface organisms may be DOC. Subterranean DOC is mainly

Table 1 Dissolved organic carbon concentrations in different aquatic environments Location Surface environments Baltic Sea water Skagerak Sea water River stream water, USA Sediments below the river stream kanal Wetland pond Subsurface environments Antrim shale groundwater, USA Permian carbonate rocks in China ¨ spo¨, Sweden Fracture zone groundwater, A ¨ spo¨, Sweden Select zone groundwater, A Big Soda Lake, Nevada Deep Costal Plain Sediments groundwater, Maryland Subwetland subsurface water

Dissolved organic carbon (mg l 1)

Approximate age (year)

Reference

3.5 0.9 – 3 3.1 – 32.1 1.6 – 6.8

n.d. n.d. n.d. n.d.

(Zweifel et (Mann and (Mann and (Mann and

4.8 – 32.6

n.d.

(Mann and Wetzel, 1995)

36 – 840 1800 11 – 18 0.3 – 2.8 60 0.4 – 1.0

22 000 n.d. 140 500 – 10 000 n.d. n.d.

(Martini et al., 1996) (Liu-Xiaozeng et al., 1988) (Banwart et al., 1996) (Winberg et al., 1996) (Geodekyan et al., 1983) (Chapelle et al., 1987)

7.1 – 48.2

n.d.

(Mann and Wetzel, 1995)

al., 1995) Wetzel, 1995) Wetzel, 1995) Wetzel, 1995)

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

composed of humic and fulvic acids (Pettersson et al., 1990). Deep subsurface DOC is a less suitable substrate for microbial utilization than surface DOC because it has been exposed to microbial degradation at shallow depths. Humic acids may be used as a shuttle compounds for the oxidation of organic compounds by iron-reducing bacteria (Lovely et al., 1996). The appearance of isotopically light carbon at shallow ¨ spo¨ (Sweden) indicates ongoing microbial depth in A oxidation and fermentation of organic matter that has been intruded with the shallow water from the surface (Banwart et al., 1996). Subsurface DOC may undergo slow microbial degradation and may serve as a source of energy and carbon for microorganisms, although the biochemical mechanisms responsible for this process are not presently known. An alternative energy source for microbes, namely H2(aq), has been found in a variety of subsurface environments. Concentrations of H2(aq) observed in the deep aquifers are significantly higher than in other tested aquatic environments (Table 2). Anaerobic microbes have the highest affinity for H2(aq) known in nature (Conrad et al., 1983b; Zinder, 1993). Thus, H2(aq) may be a bioavailable energy source for the development of microbial autotrophic populations in deep groundwater. Before the hydrogen-dependent subterranean biosphere hypothesis was proposed (Ivanov, 1990; Boston et al., 1992; Gold, 1992; Pedersen and Albinsson, 1992), it has been a general concept that all life on

371

Earth depends on the sun via photosynthesis. The hypothesis assumes that the subterranean biosphere can be based on the energy of hydrogen and independent of photosynthetically produced organic carbon and oxygen. If molecular hydrogen and carbon dioxide are present, development of autotrophic microorganisms would be possible. Stevens and McKinley (1995) reported evidence that this occurs in nature without dependence on organic matter or oxygen from photosynthesis. We showed that anaerobic autotrophic organisms may produce organic matter from hydrogen by means of respiring carbon dioxide (methanogens and acetogens), sulfate (sulfate-reducing bacteria), or iron (iron-reducing bacteria) in the dark in oligotrophic igneous rock in Sweden (Kotelnikova and Pedersen, 1997; Fig. 2). It has later been claimed that hydrogen production from basalt– groundwater interaction may not exclusively support microbial metabolism in the subsurface (Anderson et al., 1998). The experiment in the Anderson et al. paper (1998) has since been refuted by Stevens and McKinley (2000). As potential hydrogen consumers, chemoautotrophic organisms may be able to act as a primary producers of organic carbon initiating heterotrophic food chains in deep subterranean environments independent of photosynthesis (Pedersen, 1999). The ultimate limitation for an active microbial life might be the availability of H2(aq) as an energy source over time (Pedersen, 1999).

Table 2 Concentrations of hydrogen detected in different environments Environment

Hydrogen, at 20 jC

Reference

Surface environments Freshwater Eutrophic Lake water Soil Paddy soils Atmosphere Sewage sludge

10 – 300 nM 0.1 – 160 nM 0 – 0.4 nM 533 nM 0.41 nM 28 – 203 nM

(Dahm et al., 1983) (Conrad et al., 1983a) (Conrad and Seiler, 1980) (Conrad, 1988) (Conrad, 1988) (Zinder, 1993)

Subsurface environments Geothermal springs Freshwater sediments Marine sediments Fennoscandian Shield Canadian Shield Columbia Deep Basalt groundwaters ¨ spo¨ granitic groundwaters A

46 – 48 mM 0.047 – 0.75 nM 25 – 60 nM 60 AM – 28 mM 10 AM – 300 mM 0.01 – 100 AM 0.05 – 100 AM

(Conrad et al., 1985) (Diekert and Wohlfarth, 1994) (Novelli et al., 1987) (Sherwood Lollar et al., 1993a) (Devol et al., 1984) (Stevens and McKinley, 1995) (Kotelnikova and Pedersen, 1996, 1997)

372

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

Fig. 2. Scheme of subterranean microbial anaerobic community based on energy of hydrogen (from Pedersen, 1997).

The origin of H2 in different subsurface systems is diverse. Hydrogen may result from mixed geochemical (Apps and Van de Kamp, 1993) and ‘‘biogenic’’ reactions, such as biofilm – rock interactions decreasing the pH on mineral surfaces containing reduced metals and releasing protons from the water. At least six possible ‘‘abiogenic’’ processes exist by which crustal hydrogen is generated (Apps and Van de Kamp, 1993): (1) reaction between dissolved gases in the system C – H –O –S in magmas, especially in those with basaltic affinities; (2) decomposition of methane to carbon (graphite) and hydrogen at T z 600 jC; (3) reaction between CO2, H2O, and CH4 at elevated temperatures in vapors; (4) radiolysis of water by radioactive isotopes of uranium, thorium, and their daughters, and potassium; (5) cataclasis of silicates under stress in the presence of water; and (6) hydrolysis by ferrous minerals in mafic and ultramafic rocks. Hydrogen gas associated with Ca2 + OH-rich alkaline groundwater (pH = 10 –12), emanating from

ultramafic rocks of the Oman ophiolite was formed by low-temperature redox reactions in a closed groundwater environment (Neal and Stanger, 1983). Neal and Stanger (1983) proposed that H2 may be formed through water decomposition in the presence of some metal hydroxides under strongly reducing conditions. The hydrolysis of water by ferrous iron under strongly reduced conditions is the most important abiogenic process of the six listed (Apps and Van de Kamp, 1993). Another source of H2 has been proposed by Freund and demonstrated in the lab (using synthetic minerals), if not in nature. He believes that solid-state redox reactions occur between silicates and water or CO2 trapped in the mineral lattice during cooling of igneous melts. Products of the reactions may include H2, H2O2, and organic acids, and may slowly diffuse out of igneous rock (Freund, 1998; Freund et al., 1999). In addition, biogenic microbial processes or corrosion may contribute to H2 production in the subsur-

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

face. For example, hydrogen emission rate from landfills where microbial organic matter degradation dominated was around 5 mM day 1 (Nozhevnikova et al., 1993). The other important reduced gas observed in the subsurface is methane. Is it possible that CH4 fuels the deep subsurface microbial community? Methane may be the other energy source in the subsurface provided that there are available microbial electron acceptors. For example, chemosynthetic systems based on methane as source of carbon and energy have been observed around deep sea methane seeps (Martens et al., 1991; Pond et al., 1998; Sassen et al., 1993; Bidle et al., 1999). Carbonate nodules and slabs in late Holocene shell terrigenous deposits of the modern Fraser River delta are formed close to the seafloor by precipitation from saline water of crystals of high-Mg calcite cement (Nelson and Lawrence, 1984) (Table 3).

4. Methane in subsurface environments 4.1. Stable isotope composition as tool to study the origin of the gas The origin and distribution of CH4 sources over the planet have been discussed previously (Rice, 1993; Schoell, 1988). A high concentration of CH4 relative to other hydrocarbons (more than 99%) indicates a bacterial or ‘‘biogenic’’ source rather than a thermogenic source (Claypool and Kaplan, 1974; Vogel et al., 1982).

373

The origin of CH4 in selected groundwater flow systems is investigated through carbon stable isotope geochemical studies. The carbon isotope ratios of dissolved CH4 and dissolved inorganic carbon (DIC) in sampled groundwater are not controlled by equilibrium fractionation processes but by kinetic isotope effects (Murphy et al., 1992). The d13C value for carbon is defined as (Craig, 1953): d13C=[(Rsample/Rpdb) 1]  1000, where R = 13C/12C and R (PDB) Pee Dee Belemite standard = 0.0112372. It was previously believed that only CH4 having d13C values ranging from 60 to 90 parts per thousand (per mil) (PDB) is of ‘‘biogenic’’ origin, having been produced by highly specialized anaerobic Archaea (Claypool and Kaplan, 1974; Nakai, 1960; Rosenfeld and Silverman, 1959; Schoell, 1980), while CH4 generated thermogenically during natural gas formation typically has d13C values ranging from 30 to 50 per mil (PDB) (Sackett, 1978). However, CH4 produced through CO2 reduction and acetate fermentation has a different isotopic composition of carbon (Whiticar et al., 1986). Temperature, organic substrate and age may be the factors controlling the relative importance of the two pathways (Schoell, 1988). Enrichment of d13C values can also be result of microbial oxidation of methane, because light 12CH4 is preferentially consumed (Alperin et al., 1988; Barker and Fritz, 1999; Coleman et al., 1981; Ovsyannikov and Lebedev, 1967; Aravena and Wassenaar, 1993). The isotopic carbon composition of both CH4

Table 3 Total microbial counts in subsurface environments Location, depth (m)

Microbial count, (cells ml 1)

Reference

Gabon, Africa, 105 Maryland sediment cores, 92 – 104 Paris Basin groundwater, 1000 – 2000 Montana Deep aquifer, 1200 – 1800 Columbia River Deep Basalt aquifers, 1200 (viable counts) ¨ spo¨ deep granitic groundwaters, 129 – 860 A 25 – 600 70 – 446 Stripa bed-rock groundwater, 812 – 1240 South Carolina groundwater, 0 – 50

105 – 106 108 – 104 103 – 105 103 103 – 104

(Pedersen et al., 1996b) (Chapelle et al., 1987) (Daumas et al., 1986) (Olson et al., 1981) (Stevens and McKinley, 1995)

105 106 – 105 105 106 – 107 108 – 106

(Pedersen and Ekendahl, 1992b) (Pedersen et al., 1996a) our study (Ekendahl et al., 1994) (Fredrickson et al., 1991a)

374

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

and CO2 may be changed by microbial CH4 oxidation and the d13C of residual CH4 becomes heavier, while that of CO2 becomes lighter (Whiticar and Faber, 1985; Preuss et al., 1989). The isotopic effects of microbial metabolism and other processes should be reported in terms of a, the fractionation factor, rather then a particular d13C of a product that results from the fractionation. This is important because the d13C of a product depends on the d13C of the source. Photosynthetic organic matter, and methane derived from it (since there is little fractionation associated with heterotrophic decomposition) have relatively constant d13C because it is derived from essentially a infinite pool of inorganic carbon of the atmosphere. In the subsurface, autotrophic methane is derived from a limited pool of inorganic carbon as for example CO2 originating from carbonates or much older minerals. Such CO2 may be very heavy since it is not a product of photosynthesis. 4.2. Distribution of ‘‘biogenic’’ methane in the deep subsurface ‘‘Biogenic’’ gas has been discovered all over the world. Estimates of the resource potential of ‘‘biogenic’’ gas have been reviewed by Rice (1993). Significant accumulations of ancient ‘‘biogenic’’ gas have been discovered in Africa, Asia (Baylis et al., 1997; Liu-Xiaozeng et al., 1988; Traynor and Sladen, 1997), East Pacific (Welhan and Craig, 1979), Europe (Okyar and Ediger, 1999), and North America (Blair, 1998; Scott, 1997). ‘‘Biogenic’’ CH4 was detected in a variety of environments such as glacial drift (Coleman et al., 1981), marine sediments (Albert et al., 1998; Bernard, 1980), the marine subsurface 7250 m depth (Geodekyan et al., 1983), lake sediments (Iversen et al., 1987; Kuivila et al., 1988; Oremland and Des Marais, 1983; Winfrey et al., 1977), and carbonate rocks from a depth of 6000 m (Liu-Xiaozeng et al., 1988). Subsurface ‘‘biogenic’’ gas was demonstrated in onshore gas seeps in Papua New Guinea (Baylis et al., 1997). Gas accumulations in a sandstone of late Oligocene age, which were located in the central part of the southeast structure of the North Sea had ‘‘biogenic’’ origin (Ekern, 1986). ‘‘Biogenic’’ CH4 has recently been found in the sandstone associated with oil-fields at a depth of 2 km in Permian rocks of

Kolguyev Island in Barents Sea in Russia (Grigoriev and Utting, 1998). ‘‘Biogenic’’ CH4 accumulations are associated with a variety of rock types (carbonate, clastic, and coal), and occur in a variety of marine and non-marine depositional settings generally characterized by rapid deposition (Rice, 1993). They occur in Mississipian and younger rocks, and burial depths as great as 4600 m (Schoell, 1988). Dissolved ‘‘biogenic’’ CH4 was present at concentrations exceeding 10 mM in the pore water of sulfidic, salt-brine-enriched sediments underlying chemosynthetic communities at the base of the Florida escarpment (Martens et al., 1991). For example, Mattavelli and Novelli (1988) estimated that 77% of the original gas reserves in Italy occur in deep-water clastic rocks (4000 m depth) in the Apennine foredeep, and 82% of the gas in the foredeep is of ‘‘biogenic’’ origin. Geochemical studies of core samples from the Black Sea have shown the gases in sediments to be mainly CH4 of ‘‘biogenic’’ origin (Reeburgh et al., 1991). The areas of acoustic turbidity filled with CH4 of ‘‘biogenic’’ origin have been found in Black Sea sediments at a depth of 35 m below water surface (Okyar and Ediger, 1999). Concentrations of CH4 around oil wells near the coast of the Netherlands in the North Sea were as high as 5 AM (Scranton and McSchane, 1991). Production of ‘‘biogenic’’ CH4 was dependent on the fresh groundwater flow in marine sediments at depth of 1.5 m (Albert et al., 1998). Organic-rich rocks and oil – gas accumulations have been correlated in numerous sedimentary basins. Evidence for microbially generated CH 4 has been obtained for the deep shale in the Michigan basin (Martini et al., 1996). 4.3. Methane in the deep igneous subsurface The deep igneous subsurface was previously not considered as a source of natural gas (Stenhouse and Grogan, 1991). It was believed that Earth’s upper mantle is too oxidized to support the presence of other than minor concentrations of gases dissolved in magmas (Burruss, 1993). The concentration of methane in the gases transported with magmas is insignificant, and this could not be the source of commercial gas fields. Later, the view

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

that methane should be chemically stable in the upper mantle and that is migrating into the crust has been advanced (Burruss, 1993; Gold, 1993). Evidence for ongoing ‘‘abiogenic’’ methane generating processes in deep granite has been published (Flo¨den and So¨derberg, 1994; Sherwood Lollar et al., 1993a,b). The drilling of the ultradeep borehole Stenberg 1 to a depth of 6.5 km and Graveberg 1 to a depth of 6.7 km inside the Siljan Ring in Sweden resulted in the discovery of gas which contained 80% CH4 (Gold, 1993). Some biological molecules, such as steranes, were found in the Siljan Ring oil. Steranes are thought to be derived from sterol, a component of methaneoxidizing bacteria. The carbon isotop ratio of the CH4 became heavier with increasing depth, and it was as heavy as 12xto 15xin the Gravberg 1 well, and 7.2x to 7.8x in the Stenberg 1 well (Gold, 1993). ¨ spo¨ deep It was shown that CH4 is present in the A groundwater, in the Southern Sweden at concentrations as high as 1 mM (Pedersen and Albinsson, 1992a). Evidence for microbially generated CH4 has been obtained for the deep granites in Olkiluoto, Finland and in Canada (Aravena and Wassenaar, 1993; Sherwood Lollar et al., 1993a). ‘‘Biogenic’’ CH4 accounts for 75 –95 vol.% of the occurrence at Enonkoski Mine in Finland (Burruss, 1993). The granitic onshore seepage in Vietnam contained ‘‘biogenic’’ methane mixed with the thermogenic gas (Traynor and Sladen, 1997). These studies indicated that microbial methanogenesis is involved in the carbon cycle in the deep granites, dolomites, oil-fields and sandstones. 4.4. Factors determining ‘‘biogenic’’ methane in deep geological environments The factors that favor significant generation of ‘‘biogenic’’ gas are rapid sediment deposition and sufficient pore space for the methanogens, which have an average size of 1 Am to thrive (Boone et al., 1993). The generation of ‘‘biogenic’’ gas requires an environment that is anoxic, containing available CO2 and low sulfate concentrations (Oremland, 1988), in the temperature range between 9 jC (Kotelnikova et al., 1998) and 110 jC (Stetter, 1992; Huber et al., 1994). The upper temperature

375

may determine the maximum depth at which subsurface methanogens can be active. Rice (1993) believes that abundant organic matter is absolutely necessary for formation of ‘‘biogenic’’ methane. Both CO2 reduction and fermentation are operating in recent environments such as near-surface sediments. Data, however, indicate that CO2 reduction is the main pathway for deeply buried ancient ‘‘biogenic’’ gas formations (Rice, 1993). Hydrogen-rich and bioavailable organic substrates are associated with young, shallow sediments. The organic matter associated with old ‘‘biogenic’’ methane consists mainly of products of lignin decomposition, humic acids. Most ancient ‘‘biogenic’’ gas accumulations are associated with this type of organic matter at concentrations of 0.5– 1% (Rice, 1993). If the environment is poor in metabolizable organic matter, then the ‘‘biogenic’’ methane becomes isotopically heavier with time. The change from fermentation to CO2 reduction with increasing depth has been documented previously (Jenden and Kaplan, 1986; Risatti, 1987). Acetate fermentation and CO2 reduction may operate simultaneously but are quantitatively important at different stages of organic matter deposition. The ‘‘biogenic’’ gases in reservoirs and older sediments are similar and have the isotopic character of methane derived from CO2 reduction (Claypool and Kaplan, 1974; Mattavelli et al., 1992; Schoell, 1980). The isotopic composition of methane formed by CO2 reduction is controlled by the d13C of the original CO2 substrate. In granitic groundwater of ¨ spo¨ Hard Rock Laboratory in Sweden, the d13CO2 A ranged from 7xto 12xand the resulting d13CH4 values ranged between 33xand 51x (Karlsson and Wikberg, 1987; Wallin et al., 1995). In Canada, the values for the resulting d13CH4 were around 45x(Barker and Fritz, 1982). The isotopic composition of CH4 formed later is a reflection of the net effect of the addition and removal of CO2, and so-called aging effect (decrease of fermentation with age of organic carbon source). ‘‘Biogenic’’ CH4 as heavy as 40xcan be produced by the microbial reduction of isotopically heavy CO2. It means that the heavy CH4 in the granitic formations of the ¨ spo¨ Hard Rock Laboratory in Canadian shield and A Sweden may have ‘‘biogenic’’ origin. The heavy DIC values of Fritz et al. (1979), Stevens and

376

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

McKinley (1995) and Martini et al. (1998) cannot be explained by processing of organic matter but they may be explained by the use of abiogenic electron donor (H2). These studies have anticipated the role of chemolithotrophic methanogens reducing CO2 with H2 in deeply buried ancient ‘‘biogenic’’ gas formations in subsurface.

5. Methanogenic Archaea in the deep subsurface environments The actual ‘‘biogenic’’ production of CH4 is accomplished by methanogenic Archaea. Methanogens have been found in a wide variety of anoxic environments including biogas reactors, marine and freshwater and sediments, marshes and swamps, wetlands, bogs, rice paddies, tundra and desert soils, landfills, as marine plankton symbionts (Balch et al., 1979; Oremland, 1988; Peters and Conrad, 1995; Whitman et al., 1991) and in animal and insect gastrointestinal tracts (Zinder, 1993). Methanogenesis is the terminal step in the carbon flow in anaerobic habitats and it plays an important role in the degradation of organic compounds (Zinder, 1993). In anoxic freshwater environments where bicarbonate is the dominant electron acceptor, hydrogen is mostly oxidized by methanogens and acetogenic bacteria (Drake, 1994). Methanogens produce methane from a limited set of substrates such as H2 and CO2, formate, acetate, methanol, and methylamines (Oremland, 1988). In marine sediments methanogenic Archaea use methanol and methylamines because these substrates cannot be consumed by sulfate-reducing bacteria (Oremland and Policin, 1982). ‘‘Biogenic’’ CH4 in the granitic subsurface is produced from H2 and CO2 or from acetate, methanol and methylamines (Kotelnikova and Pedersen, 1998b). The literature data clearly indicate that subsurface methanogens are ubiquitous. Methanogenic Archaea were cultured from different subsurface environments including deep sediments (Phelps et al., 1989, Fig. 3f). Methanobacterium thermoautotrophicum, the first known thermophilic methanogen, was isolated from a hydrothermal vent in Yellowstone National Park (Zeikus and Wolfe, 1972). M. briantii was isolated

from the deep aquifers from 657 –673 m depths in Florida, USA (Godsy, 1980). Methanothermus fervidus is a methanogen isolated from deep hydrothermal vents in Iceland (Stetter, 1981). Three out of 19 cores obtained from depths of 14 to 182 m below land surface near Maryland, USA contained viable methanogenic Archaea (Chapelle et al., 1987). Madsen and Bollag (1989) failed to enrich methanogens during short-term incubation in the presence of formate, acetate, and bicarbonate from sediments beneath the Savannah River Plant. Methanogens were enriched and identified with 16S rRNA gene probes (Fredrickson and Onstott, 1996) in basaltic groundwater. Methanogenic communities were active in the deep alkaline non-saline anaerobic groundwaters in Southeast Washington (Stevens et al., 1993). Most probable viable numbers (MPN) of methanogens ranged between 10 and 104 cells ml 1 in rock aquifers of Hanford Reservation (Stevens and McKinley, 1995). Olson et al. (1981) enriched thermophilic rod-like methanogens at 50 jC from 1485 m depth from dolomitic limestone formation at depth of 2000 m groundwater in Madison Great Plant, USA. Daumas et al. (1986) found two methanogenic cells per milliliter growing at 20 jC and 65 jC in subsurface geothermal spring water from depths of 1000 –2000 m in the Paris Basin, France. Antrim Shale (Michigan basin, USA) is organicrich, extensively structured, and is both a source and reservoir for microbial methane co-produced with variably saline waters. Carbon isotope composition of CH4 from Antrim Shale is typical of the established range for mixed gas (d13C = 47xto 56x ) (Martini et al., 1998). However, the unusually heavy residual CO2 (d13C= + 22x ) require microbial mediation. The light isotopically fraction of CO2 could be reduced directly to methane or throught acetate microbially. The difference of dD values of methane and CO2 in the formation water provides the strongest evidence of microbial methanogenesis. Methane hydrates represent an enormous carbon and energy source in many low temperature deep marine sediments. Analysis of microbial communities associated with methane hydrates in the Cascadia margin detected methanogenic genes in one out of three of the DNA samples. The gene was distantly related to the family Methanosarcinaceae (Bidle et

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

377

¨ spo¨ Hard Rock Laboratory. Methylohalophilus-like Fig. 3. Morphology of subterranean methanogens isolated from granitic groundwater in A methanogen, depth of 414 m: phase contrast microscopy (a), UV epifluorescent cells (b). Methanobacterium subterraneum strain C2BIS depth of 440 m, akridine orange stained cells (c). Trimethylamine consuming methanogens from the depth of 70 m, akridine orange stained cells (d), phase contrasted cells (e). M. subterraneum strain 3067, depth 409 m, UV epifluorescent cells (f).

al., 1999). DNA genes close to Methylocaldum sp. have also been found in the sediments and fluids of the Cascadia gas hydrate zone (Bidle et al., 1999).

Thus, methanogens could be detected and enriched from different depths from different geological sediment formations.

378

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

5.1. Methanogens in oil-fields and natural gas effluents Microbial methanogenesis is an ubiquitous process in oil-fields. Methane formed by CO2 reduction is most common in older sediments and commercial gas fields (Schoell, 1980). This was studied in detail in Russia (Belyaev and Ivanov, 1983; Belyaev, 1996; Belyaev et al., 1983, 1986; Ivanov et al., 1985; Rozanova and Ivanov, 1996). Belyaev et al. (1983) reported the following measurements for this environment: d13CH4 values of methane 52xto 69x; 2.5 – 6.0  103 metha1 nogens l ; methanogenesis rates of 195 to 227 Al of methane l 1 day 1; and as high as 69% of methane in situ originating from (14C)-acetate. Methanogenic activity observed in West Sibirian and Tatarian oilfields in Russia confirmed the existence of indigenous microflora in the oil strata waters (Belyaev, 1996). Author believes that low d13CH4 values of 52xto 69xmay be a result from mixing of methane generated by methanogens with ‘‘abiogenic’’ gases derived from thermal cracking of petroleum. Incidentally, it is the fact that also proves our hypothesis for deep subsurface autotrophic methanogenesis. Such an isotopically heavy CH4 could be produced from heavy CO2 via acetate. Methanogenic Archaea affiliated with the genus Methanobacterium were isolated from deep subsurface (1650 m depth) oil-bearing sedimentary rock and formation water in an old flooded oil-field in Russia (Belyaev et al., 1983, 1986). The isolated strains grew optimally at 45 jC on H2 + CO2 and proliferated as autotrophs without vitamin additions. The isolates did not use formate. The organisms grew in a wide range of temperatures (20 –50 jC) and salinities (0.045 –33 g l 1). Acetate addition significantly enhanced the final cell yield. It was assumed that methane generation from ‘‘biogenic’’ acetate accounted for the low d13CH4 values of methane in the field. One of the isolates from oil-bearing sandstone was described as a new species, Methanobacterium ivanovii (Belyaev et al., 1986). A strain of Methanosarcina masei capable of using acetate, methanol, methylamines and H2 + CO2 was isolated from deep formation water (Ivanov et al., 1985). The ability to grow autotrophically is not typical for Methanosarcina, but it was associated with the subsurface isolate. A halophilic mesophilic methano-

gen obligately dependent on Ca2 + ions was isolated from the same environment and was named Methanococcoides euhalobium (Obraztsova et al., 1984). The methanogens isolated from oil-bearing formations could inhabit this environment, since they were new taxonomically and physiologically well adapted to the habitat. 5.2. Methanogens and homoacetogens in granitic aquifers There is evidence of methanogenesis based on geochemical, isotope and microbiological data in the ¨ spo¨ Hard Rock Laboratory (Sweden) (Pedersen and A Albinsson, 1992a). Different physiological and morphological groups of methanogens were found in groundwater down to 460 m, and autotrophic and halotolerant methanogens were isolated in pure cultures (Fig. 3). Direct counts of autofluorescent cells (420 nm) varied from 2.5  103 to 7.4  105 cells ml 1 groundwater while viable cell counts of methanogens able to utilize hydrogen/carbon dioxide, formate, methanol, methylamines and acetate varied from 12 to 4.5  105 cells ml 1 groundwater (Kotelnikova and Pedersen, 1998b). In most aquifers, total counts of methanogens constituted between 1% and 18% of the total number of cells inhabiting the rock. Enrichment studies demonstrated uneven distribution of methanogens in different boreholes. Methylotrophic and acetoclastic methanogens dominated in shallow boreholes at depth of 68 m below surface with relatively high content of dissolved organic carbon (DOC), while H2/CO2 and formate consuming organisms prevailed in the deep (345 –460 m) boreholes with low DOC values. Three autotrophic methane-producing Archaea were isolated from deep granitic groundwater at depths of 68, 409 and 420 m (Kotelnikova et al., 1998). One of the isolates, described as Methanobacterium subterraneum (Kotelnikova et al., 1998), is eurythermic as it can grow at a wide range of temperatures from 3.6 up to 45 jC. The results of the MPN counts and the ¨ spo¨ showed that viable radiotracer experiments in A methanogens and homoacetogens coexisted in the deep groundwater between 45 and 450 m below surface (Kotelnikova and Pedersen, 1998b). The presence of both ‘‘biogenic’’ methane and culturable autotrophic methanogens were found in

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

granitic groundwater at the Olkiluoto site in Finland at the depth of 328, 450 and 863 m (Haveman et al., 1999; Pedersen, 1999; Haveman and Pedersen, submitted for publication). Autotrophic and heterotrophic acetogens were cultured from four sites from depths of 119 to 950 m in the Fennoscandian Shield in Finland (Haveman et al., 1998, 1999; Haveman and Pedersen, submitted for publication). In the deep granitic subsurface, both autotrophic groups—methanogens and acetogens, use the energy of hydrogen (Pedersen, 1997). They may thereby initiate a food chain (Fig. 2). This is opposite to the anaerobic decomposition process, in which they terminate the food chain. The data suggests that acetatedependent methane production is mediated by homoacetogenesis. The occurrence of an active, deep, hydrogen-based autotrophic organic carbon production system adds a significant but earlier overlooked reducing force to deep granitic rock. Cultivation of methanogens requires the application of special anaerobic techniques. The organisms described in the literature have been isolated without application of pressure. Deep subsurface requires that an organism combines a set of specific physiological characteristics. Namely: (1) the ability to develop and multiply at expense of inorganic energy and carbon sources; (2) under anoxic conditions; (3) the ability to survive at broad range of salinities, temperatures, and pH; and (4) to fix gaseous nitrogen. It is logical to expect that subsurface organisms are (5) barophilic and (6) prefer biofilm settings. The difficulties of culturing methanogenic Archaea from the deep subsurface indicates that they may be present in many more habitats not just the one from which they have been cultured.

6. Methane oxidation in the deep subsurface CH4-bearing seeps have been observed in many parts of continental margins at depths from 100 to 3800 m (Ivanov et al., 1993). Cold gas seeps from subsurface methane and hydrocarbon deposits occur in a variety of the cold deep marine environments including the Kattegat strait between Denmark and Sweden, the Northern Continental shelf off Norway, off Baffin Island, Canada, California, and along the coast of Alaska and Japan (Hogan et al., 1991; Juniper

379

and Sibuet, 1987; Kennicutt et al., 1985). Authigenic calcite, aragonite, magnesian calcite and protodolomite occur at the surface of the sediment above methane seeps (Ivanov et al., 1993). The carbonate carbon of gas seep calcites has extremely light d13C, which shows that the mineral was formed by microbial oxidation of methane. This was confirmed by microbiological studies. High numbers of methanotrophic bacteria were found in bottom sediments containing cement nodules both in the Okhotsk sea and at the surface of the aragonite minerals in the Black sea (Ivanov et al., 1993). Limestones originating from CH4 were observed in the carbonate rocks in Western India (Sarkar et al., 1996). Presumably, there are at least two different mechanisms of methane oxidation in deep subsurface environments. The first mechanism, anaerobic methane oxidation, probably involves a consortium of methanogens and sulfate-reducing bacteria, which occur universally in organic rich and anaerobic marine sediments and does not occur in low sulfate freshwater sediments (Reeburgh and Heggie, 1977). The second mechanism involves aerobic methane oxidation by aerobic methanotrophs, which assimilate methane via the ribulosomonophosphate (group I) or serine pathway (group II). 6.1. Anaerobic methane oxidation in marine sediments Anaerobic methane oxidation has been suggested as a process occurring in marine sediments (Bernes and Goldberg, 1976; Reeburgh, 1976), and it supposed to be an important link in the carbon and methane biochemical cycles, being a source of inorganic carbon for the formation of certain carbonate concretions and cements in marine settings (Raiswell, 1988). This process may provide a nearly quantitative sink for upwardly diffusing methane in many marine sediments. In some cases, it consumes between 5% and 20% of the global flux of methane to the atmosphere (Reeburgh and Alperin, 1988). Even though the process of anaerobic methane oxidation is well documented geochemically (Devol, 1983, 1984; Reeburgh, 1980; Blair and Aller, 1995; Hoehler et al., 1994; Iversen and Jorgensen, 1985), its mechanisms and controls are poorly characterized (Reeburgh and Alperin, 1988; Harder, 1997; Hoehler et al., 1994). The microorgan-

380

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

isms that could be responsible for the observed anaerobic methane oxidation have never been isolated or characterized. Active anaerobic methane oxidation was observed at the interface between the methaneproducing and sulfate-reducing zones in deep marine sediments in Scan Bay, USA (Reeburgh, 1980), the Amazon Shelf (Blair and Aller, 1995), and an upwelling area off Namibia (Niewo¨hner et al., 1998). Nearly total methane oxidation occurred in the anoxic deep zone of Big Soda Lake, Nevada (Iversen et al., 1987). The maximum rate of CH4 oxidation typically occurs at the base of the sulfate reducing zone, resulting in a subsurface peak in the rate of sulfate reduction (Reeburgh and Alperin, 1988; Blair and Aller, 1995; Devol, 1983; Iversen et al., 1987). Deep sulfate reduction rate is fueled by methane oxidation and appears to be inversely related to the availability of more easily oxidized substrates. Numerous studies have demonstrated the importance of anaerobic methane oxidation in the consumption of sulfate in marine sediments. Integrated methane oxidation rates within the transition zone accounted for 23% to 100% of sulfate-reduction rates (Reeburgh and Alperin, 1988; Devol et al., 1984; Iversen and Jorgensen, 1985; Niewo¨hner et al., 1998). Borowski et al. (1997) concluded that anaerobic methane oxidation is the dominant sulfate-consuming process in marine sediments. They calculated the methane flux toward the sea floor from measured sulfate porewater profiles assuming that downward sulfate flux is stoichiometrically balanced by upward methane flux. Hoehler et al. (1994) has suggested that methane can be oxidized quantitatively by a consortium of methanogenic Archaea and sulfate-reducing bacteria. In the upper, sulfate-reducing part of the sulfate – methane transition zone, sulfate reducers would consume excess hydrogen and thus limit methanogenesis. In the deeper zone of methanogenesis, the methanogens would obtain sufficient hydrogen, presumably through the fermentation process, to produce methane. At the junction of the sulfate-reducing and methanogenic zones, methanogens are hypothesized to oxidize methane and produce carbon dioxide and hydrogen via a reversal of CO2 reduction, using water as an electron acceptor (Harder, 1997). The methane would be converted to CO2 and H2 by a methanogen under a condition of low H2 partial pressure. The H2 would subsequently be oxidized by sulfate-reducing bacteria

(Hoehler et al., 1994). Inhibiting effects of sulfate and molybdate additions on the anaerobic methane oxidation in sulfate depleted sediments supported this hypothesis (Hansen et al., 1998). Anaerobic methane oxidation has been detected in numerous methane-containing sediments (Alperin et al., 1988; Iversen et al., 1987; Sarkar et al., 1996). It has been shown that methane is being consumed by Archaea which possess 16S RNA genes distantly related to Methanomicrobiales and Methanosarcinales (Hindrichs et al., 1999). The authors observed lipid biomarkers that are commonly characteristic of Archaea and are strongly depleted in 13C indicating due to use of ‘‘biogenic’’ methane as carbon source. Hindrichs et al. hypothesize that cells containing the 13 C depleted lipids posses the newly discovered 16S RNA genes. The oxidative consumption of methane generally proceeds with a significant isotope fractionation (Barker and Fritz, 1999; Coleman et al., 1981), and isotopic variation in methane observed in sulfatecontaining anaerobic sediments has often been interpreted as an indication of anaerobic methane oxidation at the expense of sulfate (Oremland, 1988). However, large variation (29x ) in the d13C value of methane, as was recently found, depended on sulfate availability in tropic swamp sediments, where no anaerobic CH4 oxidation was detected (Miyajima and Wada, 1998). 6.2. Methane oxidation and methanotrophs in the deep subsurface Methane is probably one of the principal energy sources available for bacterial oxidation in groundwater in the presence of oxygen. Aerobic freshwater and marine sediments serve as biofilters of methane produced in the anoxic zone (see review by Hanson and Hanson, 1996). In freshwater lakes with anoxic hypolimnia, methane production and oxidation are frequently significant parts of the total carbon cycle. For example, 54– 55% of the total carbon input is regenerated as methane. In terms of methane flux balance, about 46– 62% of the upward methane flux is oxidized within the narrow aerobic zone in the lake sediment (Harrits and Hanson, 1980; Kuivila et al., 1988). Galchenko et al. (1988) detected 105 – 106 cells ml 1 of methanotrophic bacteria in sediments from

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

381

Fig. 4. Scheme of the aerobic metabiosis based on oxygen and hydrogen originated from radiolysis of water and on methane suggested to be important in the deep subsurface.

the Black Sea (Galchenko et al., 1988). In the sediments 65 – 70% of the methanotrophs detected by immunofluorescence were type I methanotrophs of genera Methylomonas and Methylobacter. Microbial methane oxidation has been studied in the deep subsurface because methanotrophs may add significant potential for reduction of oxidized groundwater environments. In addition, 14 C-carbon is expected to be final and the most stable form of radionuclide transformations in case of radionuclide leakage from future Radioactive Waste repositories. Radioactive carbon-containing carbon dioxide would be transformed to methane at the expense of geological hydrogen by methanogens. Methane would be consumed by methanotrophs during its evolution in oxidized environments and transformed to organic carbon available for further microbial processing (Fig. 4). It should be noted that methanotrophs also attract attention also because of their non-specific soluble methane monooxygenase able to co-metabolize such toxic compounds as trichloroethylene (Bowman et al., 1993; Moran and Hickey, 1997) and chlorobiphenyls (Adriaens and Grabic Galic, 1994) in contaminated groundwaters.

6.3. Methanotrophs in oil-fields and natural gas effluents About 14 different species of methanotrophs were observed in deep oil-bearing stratal water from depths of 8– 40 m Tatariya, Russia (Abramochkina et al., 1987; Ivanov et al., 1979). Half of the species were affiliated to group II Methylosinus and Methylocystis genera. They dominated in the deep and less oxidized groundwaters and could fix gaseous N2. The rate of 14 CH4 oxidation in situ was measured as 14CO2 production. It varied from 187 to 294 Al l 1 day 1 (Borzenkov et al., 1991). Biomass from samples with more oxygen contained more 14C originating from methane than biomass from samples containing less oxygen. The highest numbers of methanotrophs (up to 6  104 cells ml 1) were observed in the near bottom zone of an injection well (Borzenkov et al., 1991). Active methane oxidation was observed in groundwater from oil-fields in the Volgograd region, Russia (45 – 45000 nM l 1 day 1) (Borzenkov et al., 1991) and in Apsheron, Georgia, former Russia (450 Al l 1 day 1) (Galushko and Ivanova, 1988, 1989). Fourteen new isolates of copper- and heat-tolerant meth-

382

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

anotrophs were isolated from the hot water effluent of a natural gas field (Bodrossy et al., 1995). These new isolates exhibited a DNA homology of up to 97% with the conserved regions in the soluble methane monooxygenase-coding gene (sMMO) cluster of Methylococcus capsulatus Bath. These data show that methane oxidation presence ranges widely in oil-bearing groundwaters. In addition, the observed methanotrophs originating from the oil-field and natural gas effluent groundwaters were phylogenetically different from the surface isolates. 6.4. Methanothrophs in aquifers at the Savannah River Site Groundwater collected from 13 sandy aquifer monitoring wells on the U.S. Department of the Energy Savannah River Site near Aiken, SC, were enriched with methane and 25 methanotrophic strains were isolated (Bowman et al., 1993). Groundwater from depths of 41.3 –45.5 m was oligotrophic (DOC was below 1 mg l 1) and contained 19– 20 mg l 1 oxygen and 0.1 – 200 methanotrophic cells ml 1. PLFA profiles of the isolates indicated that all of them contained high levels of 18:1N8c fatty acids. Subsequent phenotypic testing showed that the most isolates were group II methanotrophs of Methylosinus genus and one was identified as a strain belonging to the genus Methylocystis. Most exhibited sMMO activity as evidenced by the naphthalene oxidation assay, and sMMO gene probe hybridized to DNA extracted from most of the isolates. All isolates tested were able to fix nitrogen. Methanotrophs affiliated with group II could dominate in the groundwater because of their ability to grow at low organic carbon content and to fix nitrogen. Injection of methane and air into the subsurface groundwater resulted in enrichment of methanotrophic populations and methanotrophs that contained DNA sequences complementary to the methane monooxygenase gene (Jimenez et al., 1992; Pfiffner et al., 1993). Methane monooxygenase genes were present in more than 10% of screened subsurface sites. Methanotrophs play significant role in TCE degradation in the vadose zone at the Savannah River site. The bioremediation process by methanotrophs in the sediment subsurface was recently modelled (Travis and Rosenberg, 1997).

Thus, the observed methanotrophs originating from the basalt aquifers were group II methanotrophs, they could fix nitrogen and were active at limited organic carbon and oxygen availability. 6.5. Methane oxidation in igneous rock in Finland Methane of mixed ‘‘biogenic’’ and thermogenic origin dominated the gas of groundwater from 200 to 950 m depths in four igneous rock sites in Finland (Burruss, 1993; Sherwood Lollar et al., 1993a,b). ‘‘Biogenic’’ gas accounts for 75 – 95 vol.% of the occurrences at Enonkoski Mine in Finland. At each of the other shield sites, bacterial gas can account for up to 30 – 50 vol.% of the total gas accumulation (Burruss, 1993). A complicating factor in interpreting the carbon isotope data is anaerobic methane oxidation. Methane oxidisers preferentially use 12CH4, making residual d13CH4 values less negative (Coleman et al., 1981). Anaerobic methane oxidation has not been studied in deep basalt aquifers, oil-fields and natural gas effluents or granitic aquifers. However, a methane – sulfate depletion zone occurs in the depth profile of deep granitic groundwater (688 m bsl) in Olkiluoto, Finland (Haveman et al., 1999). At this horizon the maximal viable number of sulfate-reducing bacteria was observed (Haveman et al., 1998, 1999). We recently observed active methanotrophs (13 – 17 cells ml 1) in deep anaerobic granitic groundwater from a depth of 720 m below the surface in Finland (unpublished data). 6.6. Methane oxidation in ultradeep Witwatersrand Gold structures The Witwatersrand mining levels at East Driefontein Mines in South Africa are some of the deepest in the world. The late Archaean – early Proterozoic Witwatersrand basin is situated in the center of the Kaapvaal craton, South Africa and contains thick successions of Precambrian strata. The strata have extensively been mined and drilled during the 100 years since they were found to contain gold. The basement evolved between 3800 and 2800 Ma ago. The Witwatersrand supergroup consists of shales, quartzites, and one prominent lava unit. The most productive ‘‘reef’’ is a thin organic-rich layer, called the Carbon Leader, which also contains high uranium concentrations.

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

The gold mines of South Africa provide a unique ‘‘window’’ into the deep, continental biosphere (Krajick, 1999). During the Witwatersrand Deep Microbiology Project I collected biofilms from a dolomite chamber at 1000 m, from beneath a weeping borehole and dripping fracture at 3100 m, crushed carbon leader rock samples, as well as groundwater. These samples were inoculated into a variety of microbiological media of different pH to culture aerobic and anaerobic, mesophilic and thermophilic bacteria capable of utilizing methane and hydrogen as energy sources. Acridine orange direct counting in the groundwater from 3.1 km depth showed presence of 5.36  105 cells ml 1 (Kotelnikova et al., 1999). It was shown that Witwatersrand Gold mine gas contains methane (Moser, 1999). Most probable number, radiotracer experiment and enrichment culture results showed the presence of methanotrophs. Analysis of sulphide in the specific media showed that we could not culture any sulfate reducing forms oxidizing methane or hydrogen (Kotelnikova et al., 1999). We assumed the presence of syntrophic consortia of hydrogen-producing methanotrophs and anaerobic

383

organisms reducing ferric iron and/or manganese at expense of hydrogen thereby able to oxidize methane under anoxic conditions (Fig. 5). Analyses of ratios of ferric and ferrous iron in MPN tubes showed the reduction of iron in tubes containing methane and inoculated with groundwater. Controls inoculated with growth inhibitors did not show any reduction of iron. Mesophilic microorganisms reducing iron at expense of hydrogen were successfully cultivated. Thus, the presence of hydrogen-oxidizing and methane-oxidizing organisms associated with iron-reducers is suggested in this ultradeep groundwater (Kotelnikova et al., 1999). If at anaerobic conditions methane was respired with ferric iron and manganese, then a tremendous source of energy and carbon may become available for fuelling of subterranean life. This environment selects for radiation resistant and chemolithotrophic microorganisms that can utilize a wide variety of electron acceptors. Nitrate is not abundant in the deep East Dreinfontein groundwaters (Moser, 1999), while sulfate, ferric iron and oxidized manganese Mn(IV) – Mn (VII) are available as components of fracture

Fig. 5. Scheme of the anaerobic metabiosis based on metal-mediated methane-oxidation suggested to be important in the deep subsurface.

384

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

minerals. Methane may eventuelly contribute to the organic carbon production of the ultradeep system, constituting the energy base of subterranean microbial ecosystems. 6.7. Methanotrophs in igneous granitic rock aquifers at A¨spo¨ Hard Rock Laboratory in Sweden Since one of the main energy and carbon sources in ¨ spo¨ groundwater is assumed to be methane, particA ipation of methane-oxidizing bacteria in oxygen consumption was suggested. In theory, oxidation of 1 mol of methane demands eight electrons or four atoms of oxygen or 2 mol of oxygen. Laboratory scale experiments with oxidized granitic groundwater have shown that bacterial methane oxidation is responsible for a ¨ spo¨ significant part of oxygen consumption in A granitic groundwater (Kotelnikova and Pedersen, 1998c). In practice, not more than 46 –50% of methane issued from anaerobic environments is oxidized microbially (Hanson and Hanson, 1996). Our results showed that from 12% to 25% of the methane ¨ spo¨ was available in different groundwaters in A

utilized by bacteria (Kotelnikova et al., submitted for publication). MPN counts attested to the presence of single cultivable methanotrophs in the anaerobic water and 102 – 10 3 cells ml 1 in the oxidized groundwater. All tested anaerobic groundwater from ¨ spo¨ resulted in active enrichment 400 m depth in A and pure cultures oxidizing methane. Comparison of the total oxygen consumption activity by gas chromatography and radiotracer tests showed that methane oxidation was responsible for at least 0.32– 6.7% of oxygen consumption in the groundwater, for 5.1– 9.1% of oxygen consumption on a solid phase and ¨ spo¨ 9.08 – 57% of total oxygen consumption in the A tunnel pond water. The most probable number method showed that methane oxidizing organisms constituted 0.08 – 0.15% and 26– 35% of the total cell population in the groundwater and pond water, respectively. A specific inhibitor of methane oxidation, acetylene, reduced oxygen consumption by 16 – 70% (Kotelnikova and Pedersen, 1998c). Our results demonstrated that methanotrophs survived in the deep anaerobic groundwater at low numbers and that they were active. Specific methane oxidation rates, estimated

Fig. 6. Cell morphology and ultrastructure of Methylomonas scandinavica strain SRS. Negatively stained cell with single flagellum (a), thin section of the cell showing type I intracytoplasmic membranes and electron dense inclusions (b). Bars = 0.5 um. (from Kalyuzhnaya et al., 1999).

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

by 14C-carbon originating from methane incorporated to CO2 and biomass as in the presence of oxygen, ranged between 33 and 250 nmol CH4 l 1 day 1. Methane oxidation could be induced by addition of mineral solid surfaces. Presumably, our data could ¨ spo¨, underestimate the activity of methanotrophs in A since we measured the activity only in groundwater, while methanotrophs were much more active in biofilms (Kotelnikova and Pedersen, 1998a,c). Methanotrophs responsible for methane-oxidation in soils are tightly associated with the soil particles and lose activity very fast after dissociation (Prieme et al., 1996). The attached methane-utilising populations appear to be more active than the free-living populations. Methane-oxidizing bacteria could be inducted by oxidation of the groundwater. Pure cultures which actively oxidize methane have been isolated from ¨ spo¨, which are affiliated to Methylomonas, MethylA osinus, Methylococcus, Methylobacter and Methylocystis (Kalyuzhnaya et al., 1999; Kotelnikova et al., submitted for publication). One of the isolates grows without copper. New species Methylomonas scandinavica was described (Kalyuzhnaya et al., 1999; Fig. 6). Methane-utilizing bacteria were first enriched from deep granitic rock environments (Kotelnikova et al., 1998a) and their affiliation was determined by amplification of functional and phylogenetic gene probes (Kotelnikova et al., submitted for publication). Type I methanotrophs belonging to the genera Methylomonas and Methylobacter dominated in enrichment cultures from depths below 400 m. The observed methanotrophs originating from the granitic groundwaters were phylogenetically different from surface isolates and were active at high salinities, low temperatures and limited oxygen availability. The present concept for construction of a Swedish high level nuclear fuel waste (HLW) hard rock repository is deposition of the waste encapsulated in copper/steel canisters, surrounded by a bentoite clay buffer, in tunnel systems 500– 600 m below the surface in crystalline bedrock. The performance assessment of a repository includes possible microbially induced effects (Pedersen, 1996) (Fig. 7). In radioactive waste disposal, gas production is generally an undesirable process, while gas consumption may be beneficial for a waste repository. For instance, corrosion of steel in a penetrated copper/steel canister will produce hydrogen gas that in the worst case may form

385

bubbles that have to be released through the surrounding bentonite buffer, thereby increasing the risk for radionuclide migration from the waste (Pedersen et al., 1996a). Hydrogen consuming methanogens may reduce the negative effects from such hydrogen bubble formation, but they can also induce corrosion by decreasing the hydrogen concentration at a metal surface (Daniels et al., 1987). Some results indicate that gas production in intermediate and low level waste repositories with high content of organic material may be possible (Roffey, 1990; Roffey and Norqvist, 1991). Methantrophs could contribute to the reducing capacities of a microbial community around a repository, producing organic material and consuming oxygen (Figs. 4 and 6). An important research need in relation to radioactive waste disposal is therefore to investigate if microbial production and oxidation of methane can influence the performance of HLW, LLW and ILW repositories. Environments favorable for methanotrophs will be common in future High Level Waste (HLW) repositories during the open phase and for some time after closure. Once established, this group of bacteria will be active as long as there is oxygen present for the oxidation of methane and they will most probably react available methane with remaining oxygen after closure. 6.8. How aerobic methanotrophs survive in the subsurface Methanotrophs are found wherever stable sources of methane are present (Hanson and Hanson, 1996). Pure cultures of methanotrophs are not able to use any other electron acceptors than oxygen (Hanson and Hanson, 1996). However, there is some evidence that although methane-oxidisers are obligate aerobes, they are sensitive to oxygen and prefer microaerophilic habitats for development (Amaral and Knowles, 1995; Borzenkov et al., 1991; Bowman et al., 1993; Kotelnikova et al., 1998, submitted for publication). They are therefore often found concentrated in a narrow band between anaerobic and aerobic zones were methane meets an oxidized system. Consequently, the system will rapidly go anoxic if methane is in excess. Diverse and active methanotrophs were found in the deep subsurface, where oxygen could not be detected (Jimenez et al., 1992; Kotelnikova and Pedersen, 1998c; Kalyuzhnaya et al., 1999; Kotelni-

386

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

kova et al., submitted for publication). It was shown ¨ spo¨ granitic groundwater contains below 1 ppb that A of dissolved oxygen or is completely reduced (Banwart et al., 1996; Grenthe et al., 1992; Wikberg, 1987). Methanotrophs are microaerophiles (Hanson and Hanson, 1996). Ward et al. (1987) detected a qualitatively similar pattern of methane oxidation at the oxic/anoxic interface, where the process was aerobic, and at 280 and 1300 m below surface. Significant methane oxidation rates occurred in the anoxic deep groundwater (Kotelnikova et al., submitted for publication). Their activity was inhibited by a high concentration of oxygen (Kotelnikova et al., submitted for publication). Many anaerobic environments harbour active methanotrophs (Blair and Aller, 1995; Joulian et al., 1997; Nozhevnikova et al., 1999; Ward et al., 1987). Low temperature sludge methanogenesis was most active at

a depth of 40 – 60 cm while methane oxidation was active at depths between 20 and 40 cm (Nozhevnikova et al., 1999). Unusually high cell numbers of both viable methanogens and methanotrophs were observed in this environment (1010 –1011 cells ml 1). Eleven methanotrophic species were identified by the method of inderect immunofluorescence. Most methanotrophic cells produce resting stages, and the exospores and cysts of some methanotrophic bacteria appear to be well adapted for survival in oxygen depleted media (Hanson and Hanson, 1996). However, these resting stages were found only in some organisms and expressed only under some conditions. On the basis of immunofluorescence techniques, other studies suggest that densities and species composition of methanotrophs in situ do not vary significantly between what appear to be oxic and anoxic environ-

Fig. 7. Microbe-mediated processes in groundwater. Renewal of some inorganic electron acceptors is a result of chemical autooxidation (from Kotelnikova and Pedersen, 1999).

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

ments (Abramochkina et al., 1987; Borzenkov et al., 1991; Galchenko et al., 1988). In our study, the activity of methanotrophs varied relatively little between oxic groundwater or surfaces of rock periodically exposed to oxic conditions and anaerobic groundwater (Kotelnikova and Pedersen, 1998a; Kalyuzhnaya et al., 1999). Changes from oxic to anoxic conditions in situ had very little effect on survival of methanotrophs (Hanson and Hanson, 1996). Carbon starvation of pure cultures under anoxic conditions was favorable in comparison to oxic conditions. Survival and recovery of methanotrophs were generally highest for cultures starved under anoxic conditions as indicated by poststarvation measurements of methane oxidation, tetrazolium salt reduction, plate counts, and protein synthesis (Roslev and King, 1994). Significant methane-oxidizing potentials were observed in soils that had been anoxic for 90 years (Bender and Conrad, 1995). It was suggested that methanotrophic bacteria survive carbon deprivation under anoxic conditions by using maintenance energy derived solely from an anaerobic endogenous metabolism. This capability could explain a significant potential for methane oxidation in environments not continuously supporting aerobic methanotrophic growth. The presence of microaerophilic methanotrophs in the subsurface, provided that the deep groundwater is reduced, remains to be explained. The hypothesis follows: in this oligotrophic and gas-rich environment, methane may be consumed by a consortium of methanogenic Archaea and sulfate-reducing bacteria in hydrogen-depleted zones in biofilms. Fracture associated hydrogen-consuming organisms (methanogenic, acetogenic, sulfate-reducing) may create zones of low hydrogen partial pressure, providing energetically favorable conditions for reverse CO2 reduction. It was shown that formate was accumulated by Methylosinus trichosporium under conditions of oxygen limitation and excess methane (Rozanova and Galushko, 1987) and formate could be consumed by Desulfovibrio desulfuricans for sulfate reduction. Methane oxidation activity in anoxic methane and oil-bearing strata was twice as much as in oxic recharge water (Galushko and Ivanova, 1989). The only hypothesis that may explain these facts suggests the presence of syntrophic consortia of hydrogen-producing methanotrophs and anaerobic organisms respiring sulfate or ferrous iron, which are thereby able to oxidize methane

387

using anaerobic electron acceptors (Fig. 7). Methanotrophs may produce hydrogen by formate dehydrogenase as a source of reductant for biosynthesis of NADH (Dalton and Leak, 1985). Thus, the process of anaerobic methane oxidation may be carried out by methanotrophs and hydrogen-consuming organisms. The appearance of organisms or consortia able to use energy and carbon from methane and respire ferric iron, sulfate or manganese in the subsurface has been suggested (Kotelnikova et al., 1999). Fracture-associated methanogenic, acetogenic, iron- or sulfate-reducing microorganisms could consume H2 and create energetically favorable conditions for methane oxidation in the absence of oxygen. Production of more reduced intermediates is the only energetically favorable possibility under anaerobic conditions. In deep groundwater, it may be associated with uranium rich zones, as radiolysis oxygen may be produced. Any recharging groundwater carrying oxygen down to depth may stimulate methanotrophs. As oxygen becomes depleted the methanotrophs may hypothetically shift their energetic metabolism from oxygen to a hydrogen-consuming anaerobic partner and use it as electron sink.

7. Role of methane-related subterranean microorganisms in the global carbon cycle The presence of methane in the deep subsurface have been shown all over the world (Hogan et al., 1991; Scranton and McSchane, 1991; Pedersen and Albinsson, 1992a; Sherwood Lollar et al., 1993a; Martini et al., 1996; Kennicutt et al., 1985; Juniper and Sibuet, 1987). Microbial production and oxidation of methane is involved in the carbon cycle in deep subsurface environments. The flux of gases between the deep subsurface and the atmosphere is driven by the concentration gradient from the depth to the atmosphere. Gas from the subsurface may be emitted by diffusion through flooding water and soil. A gradient is built up by microbial production of methane in the deep anoxic groundwater and emission of thermogenic gas. However, it is modulated to a large extent by methane oxidation associated with biofilms and in the water phase and taking place in the oxic recharge and shallow groundwater. In the presence of oxygen, more than 25% of diffusive methane flux appears to be

388

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

oxidized in the oxic shallow groundwater (Kotelnikova and Pedersen, 1998c). The gas transport processes of gases from deep groundwater have not been studied in detail. Granitic geological formations are widely distributed over the Northern hemisphere. Methane is one of the most active gases causing the ‘‘greenhouse’’ effect on the planet’s atmosphere. When the impact of granitic environments is estimated, it is necessary to take into account the activity of methaneoxidizing biofilters in shallow groundwater layers.

8. Conclusions Methanogenic Archaea of diverse taxonomic affiliations were cultured from deep subsurface environments including the hydrothermal vents, flooded oil-fields, deep sedimentary and granitic aquifers. Subsurface methanogens were able to utilize hydrogen/carbon dioxide, formate, methanol, methylamines and acetate. Their 16S RNA genes were distantly related to surface methanogens. In comparison with the surface relatives, they as a rule had smaller size, tolerated higher salt concentrations and could grow at wider range of temperatures. The isolated organisms probably represent indigenous methanogenic populations because the isolates are well adapted to the subsurface habitat. Carbon dioxide is one of the main carbon sources for subsurface microbial methanogenesis. Chemolithoautotrophic microorganisms from deep aquifers that could grow on hydrogen and carbon dioxide greatly outnumbered those that could grow on organic compounds (Pedersen and Albinsson, 1992a; Stevens and McKinley, 1995; Kotelnikova and Pedersen, 1998b). In the deep granitic subsurface, both autotrophic groups—methanogens and acetogens, use hydrogen as their energy source. Thereby they may initiate a food chain. The data suggests that acetate-dependent methane production is mediated by homoacetogenesis. ‘‘Biogenic’’ methane has been found all over the world. On the basis of documented occurrences, gases in reservoirs and older sediments are similar and have the isotopic character of methane derived from CO2 reduction. Thus, microbial CO2 reduction to methane seems to be the main pathway for ancient ‘‘biogenic’’ gas formation. Groundwater representing the methanogenic end member are characterized by a relative

depletion of dissolved organic carbon in combination with an enrichment in 13C in inorganic carbon, which is consistent with the preferential reduction of 12CO2 by autotrophic methanogens or acetogens. Acetate may be proceeded then to methane by acetogenic methanogens. The heavy DIC values in deep groundwaters may be explained by the use of abiogenic electron donor (H2). The isotopic composition of methane formed via CO2 reduction is controlled by the d13C of the original CO2 substrate. CH4 as heavy as 40x or 50x can be produced by the microbial reduction of isotopically heavy CO2. Microbiological research of deep and ultradeep subsurface oil-field groundwaters, basaltic, granitic aquifers and dolomite formations showed presence of phylogenetically diverse methanotrophic populations which are well adapted to low concentrations of oxygen and organic carbon, tolerate high salt concentrations and may fix gaseous nitrogen. Methanotrophs have been found at depths from 15 to 3100 m below the surface. Attached methane-utilising populations appear to be more active than free-living populations. Methanotrophs survive in deep anaerobic groundwater at low numbers and they are active. Methane oxidation is one of the dominating microbial mechanisms for oxygen consumption in deep granitic aquifers. Microbial methane oxidation modulates to a great extent methane emission from the deep subsurface. Anaerobic methane oxidation plays an important role in marine sediments. It has been detected in numerous methane-containing sediments. In same cases around 90% of subsurface methane is oxidized anaerobically before it reaches the upper layer of the sediments. However, the isolation of an anaerobic organism capable of extensive methane oxidation has proved unsuccessful despite numerous attempts. Several reports have observed a coincidence of methane oxidation and sulfate reduction in diverse marine environments, suggesting participation of sulfate reducers in the anaerobic oxidation of methane. Similar processes may take place in the deep subsurface and thus fuel the deep microbial community. Presumably, there are at least two different mechanisms of methane oxidation in the deep subsurface environments. The first, anaerobic methane oxidation, probably involves a consortium of methanogens and sulfate-reducing bacteria, which occur universally in

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

marine sediments (organic rich and anaerobic) but do not occur in freshwater (low sulfate) sediments. The second mechanism involves aerobic methane oxidation by methanotrophs, which assimilate methane via the ribulosomonophosphate (group I) or serine pathway (group II) associated with symbiotic anaerobes. The process of anaerobic methane oxidation in the subsurface remains to be studied. Most subterranean environments may be characterized as electron donor limited rather than electron acceptor limited. Such oxidized compounds as ferric iron, manganese and sulfate are widely present in deep groundwater. Methane theoretically could be oxidized by syntrophic association of methanotrophe and anaerobes respiring iron, manganese or sulfate. Under anaerobic conditions, methanotrophes might get rid of excess energy by producing H2 or formate that may be used further by anaerobic bacteria. Thus, if such processes take place in deep anaerobic environments, methane could serve as an energy source that supports the existence of microorganisms in the deep subsurface on Earth.

References Abramochkina, F.N., Bezrukova, L.V., Koshelev, A.V., Galchenko, V.F., Ivanov, M.V., 1987. Microbial oxidation of methane in a body of freshwater. Microbiologia 56, 464 – 471. Adriaens, P., Grabic Galic, D., 1994. Cometabolic transformation of mono- and dichlorobiphenyls and chlorohydroxybiphenyls by methanotrophic groundwater isolates. Environ. Sci. Technol. 28, 1325 – 1330. Albert, D.B., Martens, C.S., Alperin, M.J., 1998. Biogeochemical processes controlling methane in gassy coastal sediments: Part 2. Groundwater flow control of acoustic turbidity in Eckernfo¨rde Bay Sediments. Cont. Shelf Res. 18, 1771 – 1793. Alperin, M.J., Reeburgh, W.S., Whiticar, M.J., 1988. Carbon and hydrogen isotope fractionation resulting from anaerobic methane oxidation. Global Biochem. Cycles 2, 279 – 288. Amaral, J.A., Knowles, R., 1995. Growth of methanotrophs in oxygen and methane counter gradient. FEMS Microbiol. Lett. 126, 215 – 220. Anderson, R.T., Chapelle, F.H., Lovely, D.R., 1998. Evidence against hydrogen-based microbial ecosystem in basalt aquifers. Science 281, 976 – 977. Apps, A.A., Van de Kamp, P.C., 1993. Energy gases of a ‘‘biogenic’’ origin in the earth’s crust. In: Howell, D.G. (Ed.), The Future of Energy Gases. United States Government Printing Office, Washington, pp. 81 – 132. Aravena, R., Wassenaar, L.I., 1993. Dissolved organic carbon and methane in a regional confined aquifer, southern Ontario, Can-

389

ada: carbon isotope evidence for associated subsurface sources. Appl. Geochem. 8, 483 – 493. Balch, W.E., Fox, G.E., Magrum, L.J., Woese, C.R., Wolfe, R.S., 1979. Methanogens: reevalution of a unique biological group. Microbiol. Rev. 43, 246 – 273. Balkwill, D.L., Fredrickson, J.K., Thomas, J.M., 1989. Vertical and horizontal variations in the physiological diversity of the aerobic chemoheterotrophic bacterial microflora in deep Southeast coastal plain subsurface sediments. Appl. Environ. Microbiol. 55, 1058 – 1065. Banwart, S., 1995. SKB Technical Report 95-26. Swedish Nuclear Fuel and Waste Management, Stockholm. Banwart, S., Tullborg, E.L., Pedersen, K., Gustavsson, E., Laaksoharju, M., Nilsson, A.-C., Wallin, B., Wikberg, P., 1996. Organic carbon oxidation induced by large scale shallow water ¨ spo¨ Hard Rock intrusion into a vertical fracture zone at the A Laboratory (Sweden). J. Contam. Hydrol. 21, 115 – 125. Barker, J.F., Fritz, P., 1982. The occurrence and origin of methane in some ground water flow systems. Can. J. Earth Sci. 18, 1802 – 1816. Barker, J.F., Fritz, P., 1999. Carbon isotope fractionation during microbial methane oxidation. Nature 293, 289 – 291. Baylis, S.A., Cawley, S.J., Clayton, C.J., Savell, M.A., 1997. The origin of unusual gas seeps from onshore Papua New Guinea. Mar. Geol. 137, 109 – 120. Belyaev, S., 1996. Microbiology of deep subsurface water in oil fields. Abstract Book of ISSM-96. The Swiss Society of Microbiology, Davos, Switzerland. Belyaev, S., Ivanov, M.V., 1983. Bacterial methanogenesis in underground waters. In: Hallberg, R. (Ed.), Environmental Biochemistry Proc. 5th Int. Symp. Env. Biogeochem. (ISEB). Liber Tryck, Stockholm, pp. 273 – 280. Belyaev, S.S., Wolkin, R., Kenealy, W.R., DeNiro, M.J., Epstein, S.W., Zeikus, J.G., 1983. Methanogenic bacteria from Bondyuzhshoe oil field: General characterization and analysis of stable-carbon isotopic fractionation. Appl. Environ. Microbiol. 45, 691 – 697. Belyaev, S.S., Obraztcova, A.Y., Laurinavichus, K.S., Bezrukova, L.V., 1986. Characteristics of rod-shaped methane-producing bacteria from oil pool and description of Methanobacterium ivanovii sp.nov. Microbiology 55, 821 – 826. Bender, M., Conrad, R., 1995. Effect of methane concentrations and soil conditions on the induction of methane oxidizing activity. Soil Biol. Biochem. 27, 1517 – 1527. Bernard, B.B., 1980. Sources of ‘‘biogenic’’ methane in the Gulf of Mexico. In: Geyer, R.A. (Ed.), Marine Environmental Pollution. Elsevier, Amsterdam, pp. 107 – 132. Bernes, R.O., Goldberg, E.D., 1976. Methane production and consumption in anoxic marine sediments. Geology 4, 297 – 300. Bidle, K.A., Kastner, M., Bartlett, D.H., 1999. A phylogenetic analysis of microbial communities associated with methane hydrate containing marine fluids and sediments in the Cascadia margin (ODP site 892B). FEMS Microbiol. Lett. 177, 101 – 108. Blair, N., 1998. The 13C of ‘‘biogenic’’ methane in marine sediments: the influence of Corg deposition rate. Chem. Geol. 152, 139 – 150.

390

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

Blair, N.E., Aller, R.C., 1995. Anaerobic methane oxidation on the Amazon shelf. Geochim. Cosmochim. Acta 18, 3707 – 3715. Bodrossy, I., Murrell, J.C., Dalton, H., Kalman, M., Puskas, L.G., Kovacs, K.L., 1995. Heat-tolerant methanotrophic bacteria from the hot water effluent of a natural gas field. Appl. Environ. Microbiol. 61 (10), 3549 – 3555. Boone, D.R., Whitman, W.B., Rouviere, P., 1993. Diversity and taxonomy of methanogens. In: Ferry, J.G. (Ed.), Methanogenesis. Chapman & Hall, London, pp. 35 – 81. Borowski, W.S., Paull, C.K., Ussler, I.W., 1997. Carbon cycling within the upper methanogenic zone of continental rise sediments: an example from the methane-rich sediments overlying the Blake Ridge gas hydrate deposits. Mar. Chem. 57, 299 – 311. Borzenkov, I.A., Telichenko, M.M., Milekhina, E.I., Belyaev, S.S., Ivanov, M.V., 1991. Bacteria oxidising methane and their activity in stratal water of oil-bearing deposits in Tataria. Microbiologia 60 (3), 558 – 564. Boston, P.J., Ivanov, M.V., Mckay, C.P., 1992. Icarus 95, 300 – 308. Bowman, J.P., Jimenez, L., Rosario, I., Hazen, T.C., Sayler, G.S., 1993. Characterization of the methanotrophic bacterial community present in a trichloroethylene-contaminated subsurface groundwater site. Appl. Environ. Microbiol. 59 (8), 2380 – 2387. Brockman, F.J., Denovan, R.J., Hicks, R.J., Fredrickson, J.K., 1989. Isolation and characterization of Quinoline-degrading bacteria from subsurface sediments. Appl. Environ. Microbiol. 55, 1029 – 1032. Brockman, F.J., Kieft, T.J., Fredrickson, J.K., Bjornstad, B.N., Li, S.W., Spangenburg, W., Long, P.E., 1992. Microbiology of vadose zone paleosols in south-central Washington state. Microb. Ecol. 23, 279 – 301. Burruss, R.C., 1993. Stability and Flux of Methane in the deep Crust—a review. In: Howell, D.G. (Ed.), The Future of Energy Gases. United States Government Printing Office, Washington, pp. 21 – 29. Chapelle, F.H., Zelibor, J.L.J., Grimes, D.J., Konbel, L.L., 1987. Bacteria in deep coastal plain sediments of Maryland: a possible source of CO2 to groundwater. Water Resour. Res. 23, 1625 – 1632. Christiansen, T.R., Cox, P., 1995. Response of methane emission from arctic tundra to climatic change:results from a model stimulation. Tellus, Ser. B. 47 (B), 301 – 309. Cicerone, R.J., Oremland, R.S., 1988. Biogeochemical aspects of atospheric methane. Global Biochem. 2, 299 – 327. Claypool, G.E., Kaplan, I.R., 1974. The origin and distribution of methane in marine sediments. Natural Gases in Marine Sediments. Plenum, New York, pp. 99 – 139. Coleman, D.D., Risatti, J.B., Schoell, M., 1981. Fractionation of carbon and hydrogen isotopes by methane-oxidizing bacteria. Geochim. Cosmochim. Acta 45, 1033 – 1037. Conrad, R., 1988. Biochemistry and Ecophysiology of atmospheric CO and H2. Adv. Microb. Ecol. 10, 231 – 283. Conrad, R., Seiler, W., 1980. The role of microbiological processes for the atmospheric hydrogen cycle. Forum Mikrobiol. 3, 219 – 225.

Conrad, R., Aragno, M., Seiler, W., 1983a. Production and consumption of hydrogen in a eutrophic lake. Appl. Environ. Microbiol. 45, 502 – 510. Conrad, R., Aragno, M., Seiler, W., 1983b. The inability of hydrogen bacteria to utilise atmospheric hydrogen is due to thresfold and affinity for hydrogen. FEMS Microbiol. Lett. 18, 207 – 210. Conrad, R., Bonjour, F., Aragno, M., 1985. Aerobic and anaerobic microbial consumption of hydrogen in geothermal spring water. FEMS Microbiol. Lett. 29, 201 – 205. Craig, H., 1953. The geochemistry of the stable carbon isotopes. Geochim. Cosmochim. Acta 3, 53 – 92. Crutzen, P., 1991. Methane’s sinks and sources. Nature 350, 380 – 381. Dahm, C.N., Baross, J.A., Ward, A.K., Lilley, M.D., Sedell, J.R., 1983. Initial effects of the Mount St. Helens eruption on nitrogen cycle and related chemical processes in Ryan Lake. Appl. Environ. Microbiol. 45, 1633 – 1645. Dalton, H., Leak, D.J., 1985. Methane oxidation by microorganisms. In: Polle, R.K., Dow, C.S. (Eds.), Microbial Gas Metabolism. Academic Press, New York, pp. 173 – 200. Daniels, L., Belay, N., Rajagopal, B.S., Weimar, P.J., 1987. Bacterial methanogenesis and the growth of CO2 with elemental iron as a sole source of electrons. Science 237, 509 – 511. Daumas, S., Lombart, R., Bianchi, A., 1986. A bacteriological study of geothermal spring water dating from the Dogger and Trias period in the Paris basin France. Geomicrobiology 4, 423 – 433. Devol, A.H., 1983. Methane oxidation rates in the anaerobic sediments of Saanich Inlet. Limnol. Oceanogr. 28, 738 – 742. Devol, A.H., Anderson, J.J., Kuivila, K., Murray, J.W., 1984. A model for coupled sulfate reduction and methane oxidation in the sediments of Saanich Inlet. Geochim. Cosmochim. Acta 48, 993 – 1004. Diekert, G., Wohlfarth, G., 1994. Energetic of Acetogenesis from C1 units. In: Drake, H. (Ed.), Acetogenesis. Chapman & Hall, New York, pp. 157 – 179. Drake, H., 1994. Introduction to acetogenesis. In: Drake, H. (Ed.), Acetogenesis. Chapman & Hall, New York, pp. 3 – 63. Ekendahl, S., Arlinger, J., Stahl, F., Pedersen, K., 1994. Characterization of attached bacterial populations in deep granitic groundwater from the Stripa research mine by 16S rRNA gene sequencing and scanning electron microscopy. Microbiology 140, 1575 – 1583. Ekern, O.F., 1986. Late Oligocene gas accumulations, Block 2/2, Norway. In: Graham, T. (Ed.), Habitat of Hydrocarbons on the Norwegian Continental Shelf. Norwedian Petrolium Society, Oslo, pp. 143 – 149. Flo¨den, T., So¨derberg, P., 1994. Shallow gas trap and gas migrations in crystalline bedrock areas offshore Sweden. Baltica 8, 50 – 56. Fredrickson, J.K., Onstott, T.C., 1996. Microbes deep inside the earth. Sci. Am. 275, 42 – 47. Fredrickson, J.K., Garland, T.R., Hicks, R.J., Thomas, J.M., Li, S.W., McFadden, K.M., 1989. Lithotrophic and heterotrophic bacteria in deep subsurface sediments and their relation to sediment properties. Geomicrobiol. J. 7, 53 – 66. Fredrickson, J.K., Balkwill, D.L., Zachara, J.M., Li, S.M., Brock-

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395 man, F.J., Simmons, M.A., 1991a. Physiological diversity and distribution of heterotrophic bacteria in deep Cretaceouse sediments. Appl. Environ. Microbiol. 57, 402 – 411. Fredrickson, J.K., Brockman, F.J., Workman, D.J., Li, S.W., Stevens, T.O., 1991b. Isolation and characterization of a subsurface bacterium capable of growth on toluene, naphthalene, and other aromatic compounds. Appl. Environ. Microbiol. 57, 796 – 803. Freund, F., 1998. Rock versus atmosphere; sources of Mars oxidant. In American Geophysical Union 1998 spring meeting. Freund, F., Gupta, A.D., Kumar, D., 1999. Origins Life Evol. Biosphere 29, 489 – 509. Fritz, P., Barker, J.F., Gale, J.E., 1979. Geochemistry and isotope hydrology of groundwaters in the Stripa granite. Results and preliminary interpretation. Report LBL-8285. Lawrence Berkeley Laboratory, Berkeley, CA. Galchenko, V.F., Abramochkina, F.N., Bezrukova, L.V., Sokolova, E.N., Ivanov, M.V., 1988. Species composition of aerobic methanotrophic microflora in the Black Sea. Microbiologia 57, 305 – 311. Galushko, A.S., Ivanova, A.E., 1988. Methane oxidation in the critical zone of a discharge well in the Apsheron oil-bearing stratum. Microbiology 57 (3), 348 – 349. Galushko, A.S., Ivanova, A.E., 1989. Methane oxidation in near bottom zone of a injection well of the Apsheron oil-bearing stratum. Microbiologia 58 (2), 348 – 349. Gascoyne, M., Frost, L.H., Haveman, S.A., Stroes-Gascoyne S., Thorne, G.A., Vilks, P., Clarke, D.J., Watson, R.L., 1997. Chemical evolution of rapidely recharging groundwaters in shield environments. Technical Record TR-677 COG-97, AECL Geochemistry Research Branch Whiteshell Laboratories, Pinawa, Manitoba. Geodekyan, A.A., Trocyk, V.Y., Berlin, Y.M., Marina, M.M., 1983. ‘‘Biogenic’’ methane and hydrogen in ultradeep sediments of Imperators Gulf. Oceanology 273 (4), 982 – 984 (Rus). Godsy, E.M., 1980. Isolation of Methanobacterium bryantii from a deep aquifer by using a novel broth-antibiotic disk method. Appl. Environ. Microbiol. 39, 1074 – 1075. Gold, T., 1992. The deep, hot biosphere. Natl. Acad. Sci. U. S. A. 89, 6045 – 6049. Gold, T., 1993. The origin of methane in the crust of the Earth. In: Howell, D.G. (Ed.), The Future of Energy Gases. United States Government Printing Office, Washington, pp. 57 – 81. Grenthe, I., Stumm, W., Laaksoharju, M., Nilsson, A.-C., Wikberg, P., 1992. Redox potentials and redox reactions in deep ground water systems. Chem. Geol. 98, 131 – 150. Grigoriev, M., Utting, J., 1998. Sedimentology, palynostratigraphy, palynofacies and thermal maturity of Upper Permian rocks of Kolguyev Island, Barents Sea, Russia. Bulletin of Canadian Petroleum Geology 46, 1 – 11. Hansen, L.B., Finster, K., Fossing, H., Iversen, N., 1998. Anaerobic methane oxidation in sulfate depleted sediments: effects of sulfate and molybdate additions. Aquat. Microbiol. Ecol. 14, 195 – 204. Hanson, R.S., Hanson, T.E., 1996. Methanotrophic bacteria. Microbiol. Rev. 60 (2), 439 – 471. Harder, J., 1997. Anaerobic methane oxidation by bacteria employ-

391

ing 14C-methane uncontaminated with 14C-carbon monoxide. Mar. Geol. 137, 13 – 23. Harrits, S.M., Hanson, R.S., 1980. Stratification of aerobic methane-oxidizing organisms in Lake Mendota, Wisconsin. Limnol. Oceanogr. 25, 412 – 421. Haveman, S.A., Pedersen, K., Ruotsalainen, P., 1998. Geomicrobial investigations of groundwater from Olkiluoto, Ha¨stholmen, Kivetty and Romuvaara. Work Report 98-55, Posiva OY, Helsinki. Haveman, S.A., Pedersen, K., 2001. Regional distribution of culturable microrganisms in Fennoscandian Shield groundwater. Geomicrobiol. J. (submitted for publication). Haveman, S.A., Pedersen, K., Ruotsalainen, P., 1999. Distribution and metabolic diversity of microorganisms in deep igneous rock aquifers of Finland. Geomicrobiology 16, 277 – 294. Hindrichs, K.U., Hayes, J.M., Sylva, S.P., Brewer, P.G., DeLong, E.F., 1999. Methane-consuming archaeabacteria in marine sediments. Nature 398 (29), 802 – 805. Hoehler, T.M., Alperin, M.J., Albert, D.B., Martens, C.S., 1994. Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen-sulfate reducer consortium. Global Biochem. Cycles 8, 451 – 463. Hogan, K.B., Hoffman, J.S., Thompson, A.M., 1991. Methane on greenhouse agenda. Nature 354, 181 – 182. Horita, J., Berndt, M.E., 1999. A ‘‘biogenic’’ methane formation and isotopic fractionation under hydrothermal conditions. Science 285, 1055 – 1057. Huber, H., Huber, R., Lo¨dermann, H.-D., Stetter, O.K., 1994. Search for hyperhermophilic microorganisms in fluids obtained from the KTB pump test. Sci. Drill. 4, 127 – 129. Ivanov, M.V., 1990. USSR Life Sci. Dig. 21, 38 – 40. Ivanov, M.B., Belyaev, C.C., Laurinavichus, K.C., 1979. Methane oxidation in gas bearing strata in Volgograd, Russia. Microbiology 48 (1), 129 – 134. Ivanov, M.V., Belyaev, S.S., Laurinavichus, K.S., Obraztsova, A.Y., Gorlatov, S.H., Bondar, V.A., 1985. Development dynamic of microbiological processes after oxidation of oil field aquifers. Mikrobiologiia 54, 293 – 300. Ivanov, M.V., Lein, A.Y., Gal’chenko, V.F., 1993. The global methane cycle in the oceans. Geochem. Int. 30 (2), 114 – 124. Iversen, N., Jorgensen, B.B., 1985. Anaerobic methane oxidation rates at the sulfate – methane transition in marine sediments from Kattegat and Skagerrak (Denmark). Limnol. Oceanogr. 30, 944 – 955. Iversen, N., Oremland, R.S., Klug, M.J., 1987. Big Soda Lake (Nevada): 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol. Oceanogr. 32, 804 – 814. Jenden, P.D., Kaplan, I.R., 1986. Comparison of microbial gases from the middle America trench and scripps canyon—implications for the origin of natural gas. Appl. Geochem. 1, 631 – 646. Jimenez, L., Rosario, I., Werner, C., Koh, S., Sayler, G.S., 1992. Molecular environmental diagnostics in contaminated subsurface sites. In: Roy, S.J. (Ed.), Abstracts of the 92nd General Meeting of American Society of Microbiology. ASM, Washington, p. 371. Joulian, C., Escoffier, S., Le Mer, J., Neue, H.U., Roger, P.A., 1997. Populations and potential activities of methanogens and methanotrophs in rice fields: relations with soil properties. Eur. J. Soil Biol. 33, 105 – 116.

392

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

Juniper, S.K., Sibuet, M., 1987. Cold seep benthic communities in Japan: spartial organization, tropic strategies, and evidence for temporal evolution. Mar. Ecol.: Prog. Ser. 40, 115 – 126. Kalyuzhnaya, M.G., Khmelenina, V.N., Kotelnikova, S.V., Pedersen, K., Holmquis, L., Trotsenko, Y., 1999. Methylomonas scandinavica, a new psychrophilic methanotrophic bacterium isolated from deep igneous rock aquifer, Sweden. Syst. Appl. Microbiol. 22, 565 – 572. Karlsson, F., Wikberg, P., 1987. Some highlights on the isotope geochemistry studies within the Swedish research program on radioactive waste disposal. Appl. Geochem. 2, 25 – 31. Kennicutt, J.C., Brooks, J.M., Bidigare, R.R., Fay, R.R., Wade, T.L., McDonald, T.J., 1985. Vent-type taxa in a hydrocarbon seep region on the Louisiana slope. Nature 317, 351 – 353. Kotelnikova, S., Pedersen, K., 1996. Program Abstr. The 1996 International Symposium on Subsurface Microbiology. Abstr. 51, Davos. Kotelnikova, S., Pedersen, K., 1997. Evidence for methanogenic Archaea and homoacetogenic Bacteria in deep granitic rock aquifers. FEMS Microbiol. Rev. 20, 327 – 339. Kotelnikova, S., Pedersen, K., 1998a. Presence and activity of meth¨ spo¨ Hard ane-oxidising bacteria in deep granitic aquifers at A Rock Laboratory. Abstract Book of Eight International Symposium on Microbial Ecology, p. 205. Halifax, Nova Scotia, Canada. Kotelnikova, S.V., Pedersen, K., 1998b. Distribution and activity of methanogens and homoacetogens in deep granitic aquiferes at ¨ spo¨ Hard Rock Laboratory, Sweden. FEMS Microbiol. Ecol. A 26, 121 – 134. Kotelnikova, S.V., Pedersen, K., 1998c. Microbial oxygen con¨ spo¨ tunnel environments. SKB PR HRL-98-11. sumption in A Swedish Nuclear Fuel Waste Dept., SKB, Stockholm. Kotelnikova, S., Pedersen, K., 1999. Microbe-REX project: micro¨ spo¨ tunnel. SKB Technical bial oxygen consumption in the A Report. Swedish Nuclear Fuel and Waste Management, Stockholm, pp. 1 – 75. Kotelnikova, S., Pedersen, K., 2000. Microbial oxygen reduction during the REX field experiment. International progress report. Swedish Nuclear Fuel and Waste Management, SKB, Stockholm, pp. 1 – 66. Kotelnikova, S.V., Macario, A.J.A., Pedersen, K., 1998. Methanobacterium subterraneum, a new alcalophilic, eurythermic and halotolerant methanogen isolated from deep granitic groundwater. Int. J. Syst. Bacteriol. 48, 357 – 367. Kotelnikova, S.V., Pedersen, K., Mosert, D., Onstott, T.C., 1999. The Witwatersrand Deep Microbiology project: methane and hydrogen dependent metal reduction. In: Ghiorose, W. (Ed.), Abstract Book of the 4th International Symposium on Subsurface Microbiology, August 22 – 27. ASM, Vail, CO, USA, p. 22. Kotelnikova, S., Khemelina, V.N., Kalyuznaya, M., Trotsenko, Y.A., Pedersen, K., 2000. Methane oxidation in deep igneous rock groundwaters. FEMS Microbiol. Ecol., 1 – 12 (submitted for publication). Krajick, K., 1999. To hell and back. Journey to the center of the Earth. Discover 20 (7), 76 – 82. Kuivila, K.M., Murray, J.W., Devol, A.H., Lindstrom, M.E., Reim-

ers, C.E., 1988. Methane cycling in the sediments of Lake Washington. Limnol. Oceanogr. 33, 571 – 581. Liu-Xiaozeng, C., Schneider, W.B., Tan, W.C., 1988. ‘‘Biogenic’’ methane and burrowing as important controlling factors in the early diagenesis of Permian carbonate rocks in South Sichuan/ China. Facies/Erlangen Institute 18, 289 – 302. Lovely, D.R., Coates, J.D., Blunt-Harris, E.L., Philllips, E.J.P., Woodward, J.C., 1996. Humic acids as electron acceptors for microbial respiration. Nature 382, 445 – 448. Madsen, E.L., Bollag, J.M., 1989. Aerobic and anaerobic microbial activity in deep subsurface sediments from the savannah River Plant. Geomicrobiol. J. 7, 93 – 101. Mann, C.J., Wetzel, R.G., 1995. Dissolved organic carbon and its utilization in a riverrine wetland ecosystem. Biogeochemistry 31, 99 – 120. Martens, S.M., Chanton, J.P., Paull, C.K., 1991. ‘‘Biogenic’’ methane from abyssal brine seeps at the base of the Florida escarpment. Geology 19, 851 – 854. Martini, A., Budai, J.M., Walter, L.M., Schoell, M., 1996. Microbial generation of economic accumulations of methane within a shallow organic-rich shale. Nature 383, 155 – 158. Martini, A.M., Walter, L.M., Budai, J.M., Ku, T.C.W., Kaiser, C.J., Schoell, M., 1998. Genetic and temporal relations between formation waters and ‘‘biogenic’’ methane: upper Devonian Antrim Shale, Michigan, USA. Geochim. Cosmochim. Acta 62 (10), 1699 – 1720. Mattavelli, L., Novelli, L., 1988. Geochemistry and habitat of natural gases in Italy. In: Mattavelli, L., Novelli, L. (Eds.), Advances in Organic Geochemistry. Pergamon, New York, pp. 1 – 13. Mattavelli, L., Ricchiuto, T., Martinenghi, C., 1992. Deep isotopic light methane in Northern Italy. In: R., V. (Ed.), Bacterial Gas. Technip., pp. 121 – 132. Miyajima, T., Wada, E., 1998. Sulfate-induced isotopic variation in ‘‘biogenic’’ methane from a tropical swamp without anaerobic methane oxidation. Hydrobiologia 382, 113 – 118. Moran, B.N., Hickey, W.J., 1997. Trichlorethylene biodegradation by mesophilic and psychrophilic ammonia oxidizers and methanotrophs in groundwater microcosms. Appl. Environ. Microbiol. 63 (10), 3866 – 3871. Moser, D., 1999. The Witwatersrand Deep Microbiology project: A Window into the extreme environment of deep subsurface microbial communities. In: Ghiorose, W.C. (Ed.), Abstract Book of the 4th International Symposium on Subsurface Microbiology, August 22 – 27. ASM, Colorado, USA, p. 21. Murphy, E.M., Schramke, J.A., Fredrickson, J.K., Bledsoe, H.W., Francis, A.J., Sklarew, D.S., Linehan, J.C., 1992. The influence of microbial activity and sedimentary organic carbon on the isotope geochemistry of the Middendorf aquifer. Water Resour. Res. 28, 723 – 740. Nakai, N., 1960. Carbon isotope fractionation of natural gas in Japan. Nihon Univ. Med. J. 8, 174 – 180. Neal, C., Stanger, G., 1983. Hydrogen generation from mantle source rocks in Oman. Earth Planet. Sci. Lett. 66, 315 – 320. Nelson, C.S., Lawrence, M.F., 1984. Methane-derived high-Mg calcite submarine cement in Holocene nodules from the Fraser Delta, British Columbia, Canada. Sedimentology 31, 645 – 654. Niewo¨hner, C., Hensen, C., Zabel, M., Schulz, H.D., 1998. Deep

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395 sulfate reduction completely mediated by anaerobic methane oxidation in sediments of the upwelling area off Namibia. Geochim. Cosmochim. Acta 63 (3), 455 – 464. Novelli, P.C., Scranton, M.I., Michener, R.H., 1987. Hydrogen distribution in marine sediments. Limnol. Oceanogr. 32, 565 – 576. Nozhevnikova, A.N., Nekrasova, V.K., Lebedev, V.S., Lifshits, A.B., 1993. Microbial processes in landfills. Water Sci. Technol. 27, 243 – 252. Nozhevnikova, A.N., Nekrasova, V.K., Lebedev, V.S., 1999. Lowtemperature production and oxidation of methane by the microflora of sludge checks. Mikrobiologiia 68 (2), 267 – 272. Obraztsova, A.Y., Shipin, O.B., Belyaev, C.C., Ivanov, M.B., 1984. Biological properties of coccoid methanogen isolated from oil field. Dokl. Akad. Nauk SSSR 278 (1), 227 – 230. Okyar, M., Ediger, V., 1999. Seismic evidence of shallow gas in the sediment on the shelf off Trabzon, southeastern Black Sea. Cont. Shelf Res. 19, 575 – 587. Olson, G.J., Dockins, W.S., McFetters, G.A., 1981. Sulfate-reducing and methanogenic bacteria from deep aquifers in Montana. Geomicrobiology 2, 327 – 340. Oremland, R.S., 1988. Biochemistry of methanogenic bacteria. In: Zehnder, A.J.B. (Ed.), Biology of Anaerobic Microorganisms. Wiley, New York, pp. 641 – 707. Oremland, R.S., Des Marais, D.J., 1983. Distribution, abundance and carbon isotope composition of gaseous hydrocarbons in Big Soda Lake, Nevada: an alcaline, meromictic lake. Geochim. Cosmochim. Akta 47, 2107 – 2114. Oremland, R.S., Policin, S., 1982. Methanogenesis and sulfate reduction: Competitive and noncompetitive substrates in estuarine sediments. Appl. Environ. Microbiol. 44, 1270 – 1276. Ovsyannikov, V.M., Lebedev, V.S., 1967. Isotopic composition of carbon in gases of biochemical origin. Geochem. Int. 4, 453 – 458. Pedersen, K., 1996. Investigations of subterranean bacteria in deep crystalline bedrock and their importance for the disposal of nuclear waste. Can. J. Microbiol. 42, 382 – 391. Pedersen, K., 1997. Micribial life in deep granitic rock. FEMS Microbiol. Rev. 20, 399 – 414. Pedersen, K., 1999. Subterranean microorganisms and radioactive waste disposal in Sweden. Eng. Geol. 52, 163 – 176. Pedersen, K., Albinsson, Y., 1992. Possible effects of bacteria on trace element migration in crystalline bed-rock. Radiochim. Acta 58/59, 365 – 369. Pedersen, K., Ekendahl, S., 1992. Assimilation of CO2 and introduced organic compounds by bacterial communities in ground water from Southeastern Sweden deep crystalline bedrock. Microb. Ecol. 22, 1 – 14. Pedersen, K., Arlinger, J., Ekendahl, S., Hallbeck, L., 1996a. 16S rRNA gene diversity of attached and unattached bacteria in ¨ spo¨ hard rock laboboreholes along the access tunnel to the A ratory, Sweden. FEMS Microbiol. Ecol. 19, 249 – 262. Pedersen, K., Arlinger, J., Hallbeck, L., Pettersson, C., 1996b. Diversity and distribution of subterranean bacteria in groundwater at Oklo in Gabon, Africa, as determined by 16S rRNA sequencing technique. Mol. Ecol. 5, 427 – 436. Peters, V., Conrad, R., 1995. Methanogenic and other strictly anae-

393

robic bacteria in desert soil and other oxic soil. Appl. Environ. Microbiol. 61, 1673 – 1676. Pettersson, K.J., Ephraim, B., Allard, B., Boren, H., 1990. Characterization of humic substences from deep groundwaters in granitic bedrock in Sweden. In: Pettersson, K.J. (Ed.), SKB Technical Report 90-29. SKB, Stockholm, pp. 22 – 30. Pfiffner, S.M., Mackovski, R., White, D.C., Phelps, T.J., 1993. In: Roy, R.J. (Ed.), Monitoring of Microbial Populations and Activities from Groundwater for in Situ Trichloroethylene Bioremediation. Abstracts of 93rd General meeting of American Society of Micribiology. American Society of Microbiology, Washington. Phelps, T.J., Raione, E.G., White, D.C., Fliermans, C.B., 1989. Microbial activities in deep subsurface environments. Geomicrobiology 7, 79 – 91. Pond, D.W., Bell, M.V., Dixon, D.R., Fallick, A.E., Segonzac, M., Sargent, J.R., 1998. Stable-carbon-isotope composition of fatty acids in hydrothermal vent mussels containing methanotrophic and thiotrophic bacterial endosymbionts. Appl. Environ. Microbiol. 64, 370 – 375. Preuss, A., Schauder, R., Fuchs, G., Stichler, W., 1989. Carbon isotope fractionation by autotrophic bacteria with three different CO2 fixation pathways. Z. Naturforsch., A 44c, 397 – 402. Prieme, A., Sitaula, J., Klemedtsson, A., Bakken, L., 1996. Extraction of methane-oxidizing bacteria from soil particles. FEMS Microbiol. Ecol. 21, 59 – 68. Raiswell, R., 1988. Chemical model for the origin of minor limestone shale cycles by anaerobic methane oxidation. Geology 16, 641 – 644. Reeburgh, W.S., 1976. Methane consumption in Cariaco Trench ater and sediments. Earth Planet. Sci. Lett. 28, 337 – 344. Reeburgh, W.S., 1980. Anaerobic methane oxidation: rate distributions in Skan Bay sediments. Earth Planet. Sci. Lett. 47, 345 – 352. Reeburgh, W.S., Alperin, M.J., 1988. Studies on anaerobic methane oxidation. Sci. Am. 66, 367 – 375. Reeburgh, W.S., Heggie, D.T., 1977. Microbial methane consumption reactions and their effect on methane distributions in freshwater and marine environments. Limnol. Oceanogr. 22, 1 – 12. Reeburgh, W.S., Ward, B.B., Whalen, S.C., Sandbeck, K.A., Kilpatrick, K.A., Kerkhof, L.J., 1991. Black Sea marine geochemistry. Deep-Sea Res. 38 (S2), S1189 – S1210. Rice, D.D., 1993. ‘‘Biogenic’’ gas: controls, habitats, and resource potential. In: Howell, D.G. (Ed.), The Future of Energy Gases. United States government printing office, Washington, pp. 583 – 606. Risatti, J.B., 1987. Biogeochemistry of a temperate zone peatbog. Geol. Soc. Am. Bull. 19, 821. Roffey, R., 1990. The Swedish final repository and the possible risk of interactions by microbial activities. Experientia 46, 792 – 794. Roffey, R., Nordqvist, A., 1991. Biodegradation of bitumen used for nuclear waste disposal. Experientia 47, 539 – 542. Romero, L., Moreno, L., Neretnieks, I., 1995. Movement of redox front around a repository for high-level nuclear waste. Nucl. Technol. 110, 238 – 249. Rosenfeld, W.M., Silverman, S.R., 1959. Carbon isotope fractio-

394

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395

nation in bacterial production of methane. Science 130, 1658 – 1659. Roslev, P., King, G.M., 1994. Survival and recovery of methanotrophic bacteria starved under oxic and anoxic conditions. Appl. Environ. Microbiol. 60 (7), 2602 – 2608. Rozanova, E.P., Galushko, A.S., 1987. Formate production by Methylosinus trichosporium and its utilization by Desulfovibrio desulfuricans. Microbiology 56, 886 – 887. Rozanova, E., Ivanov, M., 1996. Accumulation of acetate and methanogenesis in West-Siberian oil-field flooded with water containing complex organic matter. In: Bachofen, R. (Ed.), The Symposium on Subsurface Microbiology (ISSM-96). Swiss Society of Microbiology, Zurich, p. 134. Rozanova, E.P., Khydyakova, A.I., 1974. A new nonspore-forming thermophilic sulfate-reducing organism, Desulfovibrio thermophilus sp. nov. Microbiology 43, 908 – 912. Sackett, W.M., 1978. Carbon and hydrogen isotope effects during the thermocatalytic production of hydrocarbons in laboratory simulation experiments. Geochim. Cosmochim. Acta 42, 571 – 580. Sarkar, A., Ray, A.K., Bhattacharya, S.K., 1996. Stable isotope studies of fossiliferous Palaeogene sequence of Kutch, Western India: palaeoenviromental implications. Palaeo 121, 65 – 77. Sassen, R., Roberts, H.H., Aharon, P., Larkin, J., Chinn, E.W., Carney, R., 1993. Chemosynthetic bacterial mats at cold hydrocarbon seeps, Gulf of Mexico continental slope. Org. Geochem. 20, 77 – 89. Schoell, M., 1980. The hydrogen and carbon isotopic composition of methane from natural gases of various origins. Geochim. Cosmochim. Acta 44, 649 – 661. Schoell, M., 1988. Multiple origins of methane in the Earth. Chem. Geol. 71, 1 – 10. Scott, A.R., 1997. Bacterially mediated reactions in coal beds. Geol. Soc. Am. Bull. 29, 363 – 369. Scranton, M.I., McSchane, K., 1991. Methane fluxes in the Southern North Sea: the role of European rivers. Cont. Shelf Res. 11, 37 – 52. Sherwood Lollar, B., Frape, S.K., Fritz, P., Macko, S.A., Welhan, R., Blomqist, R., Lahermo, P.W., 1993a. Evidence for bacterially generated hydrocarbon gas in Canadian shield and Fennoscandian shield rocks. Geochim. Cosmochim. Acta 57, 5073 – 5085. Sherwood Lollar, B., Frape, S.M., Weise, S.M., Fritz, P., Macko, S.A., Welhan, A., 1993b. A’’biogenic’’ methanogenesis in crystalline rocks. Geochim. Cosmochim. Acta 57, 5087 – 5097. Stenhouse, M.J., Grogan, H., 1991. Review of reactions of hydrogen and methane in the geosphere and biosphere. Intera Sciences Report No IG2646-V6. Intera Information Technologies, Leicestershire, England. Stetter, K.O., 1981. Methanothermus fervidus sp. nov., novel extremely thermophilicmethanogen isolated from an Icelandic hot spring. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. C 2, 166 – 178. Stetter, K.O., 1992. Life at upper temperature border. In: Tran Tranh Van, J.K., Mounlou, J.C., Schneider, C., McKay, C. (Eds.), Frontiers of Life. Colloque Interdisciplinaire Comite National de la recherche Scientifique, Gif-sur-Yvette, France, pp. 195 – 219.

Stevens, T.O., McKinley, J.P., 1995. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450 – 454. Stevens, T.O., McKinley, J.P., 2000. Environ. Sci. Technol. 34, 826 – 831. Stevens, T.O., McKinley, J.P., Fredrickson, J.K., 1993. Bacteria associated with deep, alkaline, anaerobic groundwaters in Southeast Washington. Microb. Ecol. 25, 35 – 50. Travis, B.J., Rosenberg, N.D., 1997. Modeling in situ bioremediation of TCE at Savannah River: effects of product toxicity and microbial interactions on TCE degradation. Environ. Sci. Technol. 31, 3093 – 3102. Traynor, J.J., Sladen, C., 1997. Seepage in Vietnam—onshore and offshore examples. Mar. Petrol. Geol. 14, 345 – 362. Vogel, T.M., Oremland, R.S., Kvenvolden, K.A., 1982. Low-temperature formation of hydrocarbon gases in San Francisco Bay sediment (California, U.S.A.). Chem. Geol. 37, 289 – 298. Wallin, B., Tullborg, E.L., Petterson, C., 1995. Carbon cycling in the fracture zone. In: Banwart, S. (Ed.), The redox experiment in block scale. SKB Progress report 25-95-06, Stokholm, pp. 102 – 117. Ward, B.B., Kilpatrick, K.A., Novelli, P.C., Scranton, M.I., 1987. Methane oxidation and methane fluxes in the ocean surface layers and deep anoxic waters. Nature 327 (21), 226 – 229. Welhan, J.A., Craig, H., 1979. Methane and hydrogen in East Pacific Rise hydrothermal fluids. Geophys. Res. Lett. 6, 829 – 831. Whiticar, M.J., Faber, E., 1985. Methane oxidation in sediments and water column environments: isotope evidence. Org. Geochem. 10, 759 – 768. Whiticar, M.J., Faber, E., Schoell, M., 1986. ‘‘Biogenic’’ methane formation in marine and freshwater environments: CO2 reduction vs. acetate fermentation-isotopic evidence. Geochim. Cosmochim. Acta 50, 693 – 709. Whitman, W.B., Bowen, T.L., Boon, D.R., 1991. The methanogenic bacteria. In: Balows, A., Truper, H.G., Dworkin, M., Harder, W., Schleifer, K.-H. (Eds.), The Procariotes. Springer-Verlag, New York, pp. 719 – 767. Whitman, W.B., Coleman, D.C., Wiebe, W.J., 1998. Procaryotes: the unseen majority. Proc. Natl. Acad. Sci. U. S. A. 95, 6578 – 6583. Wikberg, P., 1987. The chemisty of deep groundwaters in crystalline rocks. Thesis, KTH, Department of Inorganic Chemistry, 123 pp. Winberg, A., Andersson, P., Hermansson, J., Stenberg, L., 1996. Investigation program for selection of experimental sites for the operation phase. Results from SELECT project. In: Banwart, S. (Ed.), Zˇsp’’ Progress report HRL 96-01. Can be ordered from: Swedish Nuclear Fuel and Waste Management, Box 5864, S10240, Stockholm, p. 78. Winfrey, M.R., Nelson, D.R., Klevickis, S.C., Zeikus, J.G., 1977. Association of hydrogen metabolism with methanogenesis in lake Mendota sediments. Appl. Environ. Microbiol. 33, 312 – 318. Woese, C.R., Kandler, O., Wheelis, M.L., 1990. Towards to a natural system of organisms. Proposal for the domains Archaea, Bacteria and Eucaria. Proc. Natl. Acad. Sci. U. S. A. 87, 44576 – 44579. Zeikus, J.G., Wolfe, R.S., 1972. Methanobacteriun thermoautotrophicum, sp. nov., an anaerobic, extreme thermophilie. J. Bacteriol. 109, 707 – 713.

S. Kotelnikova / Earth-Science Reviews 58 (2002) 367–395 Zinder, S.H, 1993. Physiological ecology of methanogens. In: Ferry, J.G. (Ed.), Methanogenesis. Chapman & Hall, New York, pp. 128 – 206. Zobell, C.E., 1958. Ecology sulfate-reducing bacteria. Prod. Mon. 2, 12 – 29. ¨ ., Lundberg, E., Norrman, B., 1995. Zweifel, U.L., Hagstro¨m, O Dynamics of dissolved organic carbon in a costal ecosystem. Limnol. Oceanogr. 40, 299 – 305.

395

Graduating from Nizhniy Novgorod University (Russia) in 1985 with a degree in Microbiology and Immunology, Svetlana Kotelnikova (born in 1962) studied catabolic enzymes of oxygen-limited Methylomonas methanica in the laboratory of Methylotrophy of the G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, in Russia. She then continued with research on the enzymes of the electron transport chain of hydrogen-oxidizing bacteria in the Institute of Biophysics of the Siberian Academy of Science, in Russia. She then studied strict anaerobic methanogenic Archaea in the Russian Bacterial Culture Collection of the Russian Academy of Science in collaboration with Department of Anaerobic Microorganisms, where she isolated and characterized three new species and six new strains of methanogens. She studied the cell wall composition, biochemistry, physiology and phylogeny of thermophilic methane-producing Archaea, including her own isolates from Far-East hydrothermal vents. After she defended her PhD thesis in 1994, she moved to the Deep Biosphere Laboratory, Gothenburg’s University (September, 1994) as postdoctoral researcher. She has been working on microbiology of deep ¨ spo¨ Hard Rock laboratory, in Sweden, for igneous rock aquifers at A the past five years, in the frame of a scientific project directed towards the understanding of using hard rock as a site for final disposal of high redioactive waste. Here, her publications include description of subterranean methanotrophs, homoacetogens and methanogens, interaction of homoacetogenesis and methanogenesis in deep crystalline bedrock and microbial mechanisms of oxygen reduction in deep subsurface. She has been invoved in microbiological studies of ultradeep Witwatersrand Gold mines (South Africa) in 1998 – 1999. Later, Dr. Kotelnikova studied and modelled microbial reduction of oxygen in deep granitic environments (1998 – 2000). Now she has the position of assocoate professor in St. George’s University, Grenada, in West Indies.