Francis H. Chapelle

Deep subsurface microbial processes

Information on the microbiology of the deep subsurface is necessary in order to understand the factors controlling the rate and extent of the microbially catalyzed redox reactions that influence the geophysical properties of these environments. Furthermore, there is an increasing threat that deep aquifers, an important drinking water resource, may be contaminated by mans activities, and there is a need to predict the extent to which microbial activity may remediate such contamination. Metabolically active microorganisms can be recovered from a diversity of deep subsurface environments. The available evidence suggests that these microorganisms are responsible for catalyzing the oxidation of organic matter coupled to a variety of electron acceptors just as microorganisms do in surface sediments, but at much slower rates. The technical difficulties in aseptically sampling deep subsurface sediments and the fact that microbial processes in laboratory incubations of deep subsurface material often do not mimic in situ processes frequently necessitate that microbial activity in the deep subsurface be inferred through nonmicrobiological analyses of ground water. These approaches include measurements of dissolved H2, which can predict the predominant microbially catalyzed redox reactions in aquifers, as well as geochemical and groundwater flow modeling, which can be used to estimate the rates of microbial processes. Microorganisms recovered from the deep subsurface have the potential to affect the fate of toxic organics and inorganic contaminants in groundwater. Microbial activity also greatly influences the chemistry of many pristine groundwaters and contributes to such phenomena as porosity development in carbonate aquifers, accumulation of undesirably high concentrations of dissolved iron, and production of methane and hydrogen sulfide. Although the last decade has seen a dramatic increase in interest in deep subsurface microbiology, in comparison with the study of other habitats, the study of deep subsurface microbiology is still in its infancy.

A hydrogen-based subsurface microbial community dominated by methanogens

The search for extraterrestrial life may be facilitated if ecosystems can be found on Earth that exist under conditions analogous to those present on other planets or moons. It has been proposed, on the basis of geochemical and thermodynamic considerations, that geologically derived hydrogen might support subsurface microbial communities on Mars and Europa in which methanogens form the base of the ecosystem. Here we describe a unique subsurface microbial community in which hydrogen-consuming, methane-producing Archaea far outnumber the Bacteria. More than 90% of the 16S ribosomal DNA sequences recovered from hydrothermal waters circulating through deeply buried igneous rocks in Idaho are related to hydrogen-using methanogenic microorganisms. Geochemical characterization indicates that geothermal hydrogen, not organic carbon, is the primary energy source for this methanogen-dominated microbial community. These results demonstrate that hydrogen-based methanogenic communities do occur in Earths subsurface, providing an analogue for possible subsurface microbial ecosystems on other planets.

Redox Processes and Water Quality of Selected Principal Aquifer Systems

Reduction/oxidation (redox) conditions in 15 principal aquifer (PA) systems of the United States, and their impact on several water quality issues, were assessed from a large data base collected by the National Water-Quality Assessment Program of the USGS. The logic of these assessments was based on the observed ecological succession of electron acceptors such as dissolved oxygen, nitrate, and sulfate and threshold concentrations of these substrates needed to support active microbial metabolism. Similarly, the utilization of solid-phase electron acceptors such as Mn(IV) and Fe(III) is indicated by the production of dissolved manganese and iron. An internally consistent set of threshold concentration criteria was developed and applied to a large data set of 1692 water samples from the PAs to assess ambient redox conditions. The indicated redox conditions then were related to the occurrence of selected natural (arsenic) and anthropogenic (nitrate and volatile organic compounds) contaminants in ground water. For the natural and anthropogenic contaminants assessed in this study, considering redox conditions as defined by this framework of redox indicator species and threshold concentrations explained many water quality trends observed at a regional scale. An important finding of this study was that samples indicating mixed redox processes provide information on redox heterogeneity that is useful for assessing common water quality issues. Given the interpretive power of the redox framework and given that it is relatively inexpensive and easy to measure the chemical parameters included in the framework, those parameters should be included in routine water quality monitoring programs whenever possible.

Use of dissolved h2 concentrations to determine distribution of microbially catalyzed redox reactions in anoxic groundwater.

The potential for using concentrations of dissolved H 2 to determine the distribution of redox processes in anoxic groundwaters was evaluated. In pristine aquifers in which standard geochemical measurements indicated that Fe(III) reduction, sulfate reduction, or methanogenesis was the terminal electron accepting process (TEAP), the H 2 concentrations were similar to the H 2 concentrations that have previously been reported for aquatic sediments with the same TEAPs. In two aquifers containated with petroleum products, it was impossible with standard geochemical analyses to determine which TEAPs predominated in specific locations. However, the TEAPs predicted from measurements of dissolved H 2 were the same as those determined directly through measurements of microbial processes in incubated aquifer material

Temporal and spatial changes of terminal electron‐accepting processes in a petroleum hydrocarbon‐contaminated aquifer and the significance for contaminant biodegradation

Measurements of dissolved hydrogen and other biologically active solutes in groundwater from a shallow petroleum hydrocarbon-contaminated aquifer indicate that the distribution of microbial terminal electron-accepting processes (TEAPs), such as methanogenesis, sulfate reduction, and ferric iron (Fe (III)) reduction, is highly dynamic in both time and space. Delivery of sulfate to methanogenic zones by infiltrating recharge or lateral transport can result in a TEAP shift from methanogenesis to sulfate reduction. Conversely, lack of recharge and consumption of available sulfate can result in a shift from sulfate reduction to methanogenesis. Temporal shifts between sulfate and Fe (III) reduction were also observed. Time lags associated with TEAP shifts ranged from less than 10 days to about months. The relation between TEAP and biodegradation rates of a variety of organic compounds indicate that biodegradation rates of petroleum hydrocarbons probably vary temporally and spatially in a contaminated aquifer.

Geochemistry of dissolved inorganic carbon in a Coastal Plain aquifer. 1. Sulfate from confining beds as an oxidant in microbial CO2 production

A primary source of dissolved inorganic carbon (DIC) in the Black Creek aquifer of South Carolina is carbon dioxide produced by microbially mediated oxidation of sedimentary organic matter. Groundwater chemistry data indicate, however, that the available mass of inorganic electron acceptors (oxygen, Fe(III), and sulfate) and observed methane production is inadequate to account for observed CO2 production. Although sulfate concentrations are low (approximately 0.05–0.10 mM) in aquifer water throughout the flow system, sulfate concentrations are greater in confining-bed pore water (0.4–20 mM). The distribution of culturable sulfate-reducing bacteria in these sediments suggests that this concentration gradient is maintained by greater sulfate-reducing activity in sands than in clays. Calculations based on Ficks Law indicate that possible rates of sulfate diffusion to aquifer sediments are sufficient to explain observed rates of CO2 production (about 10−5 mmoll−1 year−1), thus eliminating the apparent electron-acceptor deficit. Furthermore, concentrations of dissolved hydrogen in aquifer water are in the range characteristic of sulfate reduction (2–6 nM), which provides independent evidence that sulfate reduction is the predominant terminal electron-accepting process in this system. The observed accumulation of pyrite- and calcite-cemented sandstones at sand-clay interfaces is direct physical evidence that these processes have been continuing over the history of these sediments.

Fe(III)-reducing bacteria in deeply buried sediments of the Atlantic Coastal Plain

The possibility that microorganisms are catalyzing the ongoing reduction of Fe(III) in the sediments of deep (20-250 m) aquifers was investigated. Acetate-oxidizing, Fe(III)-reducing bacteria were recovered from deep subsurface sediments, but only from sediments in which it appeared that Fe(III) reduction was the terminal electron-accepting process for oxidation of organic matter. The Fe(III)-reducing microorganisms were capable of reducing ferric oxides present in deep subsurface sediments. Although Fe(III) reduction in subsurface sediments is frequently regarded as an abiological reaction, the enzymatic reduction of Fe(III) by microorganisms reported here is the first mechanism of any kind actually shown to have the potential to couple the oxidation of organic matter to carbon dioxide with the reduction of Fe(III) under the environmental conditions typically found in deep aquifers. We propose that microbially catalyzed Fe(III) reduction is responsible for such late postdepositional phenomena as the formation of variegated red beds and the release of high concentrations of dissolved iron into anaerobic ground waters.

Biotransformation of caffeine, cotinine, and nicotine in stream sediments: Implications for use as wastewater indicators

Microbially catalyzed cleavage of the imadazole ring of caffeine was observed in stream sediments collected upstream and downstream of municipal wastewater treatment plants (WWTP) in three geographically separate stream systems. Microbial demethylation of the N-methyl component of cotinine and its metabolic precursor, nicotine, also was observed in these sediments. These findings indicate that stream sediment microorganisms are able to substantially alter the chemical structure and thus the analytical signatures of these candidate waste indicator compounds. The potential for in situ biotransformation must be considered if these compounds are employed as markers to identify the sources and track the fate of wastewater compounds in surface-water systems.

Methyl t-Butyl Ether Mineralization in Surface-Water Sediment Microcosms under Denitrifying Conditions

ABSTRACT Mineralization of [U-14C]methylt-butyl ether (MTBE) to 14CO2without accumulation of t-butyl alcohol (TBA) was observed in surface-water sediment microcosms under denitrifying conditions. Methanogenic activity and limited transformation of MTBE to TBA were observed in the absence of denitrification. Results indicate that bed sediment microorganisms can effectively degrade MTBE to nontoxic products under denitrifying conditions.

Factors affecting microbial 2,4,6-trinitrotoluene mineralization in contaminated soil

The influence of selected environmental factors on microbial TNT mineralization in soils collected from a TNT-contaminated site at Weldon Spring, MO, was examined using uniformly ring-labeled [ 14 C]TNT. Microbial TNT mineralization was significantly inhibited by the addition of cellobiose and syringate. This response suggests that the indigenous microorganisms are capable of metabolizing TNT but preferentially utilize less recalcitrant substrates when available. The observed inhibition of TNT mineralization by TNT concentrations higher than 100 μmol/kg of soil and by dry soil conditions suggests that toxic inhibition of microbial activity at high TNT concentrations and the periodic drying of these soils have contributed to the long-term persistence of TNT at Weldon Spring. In comparisonto aerobic microcosms, mineralization was inhibited in anaerobic microcosms and in microcosms with a headspace of air amended with oxygen, suggesting that a mosaic of aerobic and anaerobic conditions may optimize TNT degradation at this site.