Biotic adjustments to changing salinities in the Great Salt Lake,Utah, USA

The salinity of the Great Salt Lake, Utah has changed greatly over the past 23 years. The north arm of the lake has increased in salinity and decreased in overall biological diversity, whereas the south arm has decreased in salinity and increased markedly in biological diversity.     

Modeling Reduction of Uranium U(VI) under Variable Sulfate Concentrations by Sulfate-Reducing Bacteria

The kinetics for the reduction of sulfate alone and for concurrent uranium [U(VI)] and sulfate reduction, by mixed and pure cultures of sulfate-reducing bacteria (SRB) at 21 ± 3°C were studied. The mixed culture contained the SRB Desulfovibrio vulgaris along with a Clostridium sp. determined via 16S ribosomal DNA analysis. The pure culture was Desulfovibrio desulfuricans (ATCC 7757). A zero-order model best fit the data for the reduction of sulfate from 0.1 to 10 mM. A lag time occurred below cell concentrations of 0.1 mg (dry weight) of cells/ml. For the mixed culture, average values for the maximum specific reaction rate, V_max, ranged from 2.4 ± 0.2 μmol of sulfate/mg (dry weight) of SRB · h⁻¹) at 0.25 mM sulfate to 5.0 ± 1.1 μmol of sulfate/mg (dry weight) of SRB · h⁻¹ at 10 mM sulfate (average cell concentration, 0.52 mg [dry weight]/ml). For the pure culture, V_max was 1.6 ± 0.2 μmol of sulfate/mg (dry weight) of SRB · h⁻¹ at 1 mM sulfate (0.29 mg [dry weight] of cells/ml). When both electron acceptors were present, sulfate reduction remained zero order for both cultures, while uranium reduction was first order, with rate constants of 0.071 ± 0.003 mg (dry weight) of cells/ml · min⁻¹ for the mixed culture and 0.137 ± 0.016 mg (dry weight) of cells/ml · min⁻¹ (U₀ = 1 mM) for the D. desulfuricans culture. Both cultures exhibited a faster rate of uranium reduction in the presence of sulfate and no lag time until the onset of U reduction in contrast to U alone. This kinetics information can be used to design an SRB-dominated biotreatment scheme for the removal of U(VI) from an aqueous source.     

Diversity of sulfate-reducing bacteria from an extreme hypersaline sediment, Great Salt Lake (Utah)

The diversity of sulfate-reducing bacteria (SRB) inhabiting the extreme hypersaline sediment (270 g L(-1) NaCl) of the northern arm of Great Salt Lake was studied by integrating cultivation and genotypic identification approaches involving PCR-based retrieval of 16S rRNA and dsrAB genes, the latter encoding major subunits of dissimilatory (bi) sulfite reductase. The majority (85%) of dsrAB sequences retrieved directly from the sediment formed a lineage of high (micro) diversity affiliated with the genus Desulfohalobium, while others represented novel lineages within the families Desulfohalobiaceae and Desulfobacteraceae or among Gram-positive SRB. Using the same sediment, SRB enrichment cultures were established in parallel at 100 and at 190 g L(-1) NaCl using different electron donors. After 5-6 transfers, dsrAB and 16S rRNA gene-based profiling of these enrichment cultures recovered a SRB community composition congruent with the cultivation-independent profiling of the sediment. Pure culture representatives of the predominant Desulfohalobium-related lineage and of one of the Desulfobacteraceae-affilated lineages were successfully obtained. The growth performance of these isolates and of the enrichment cultures suggests that the sediment SRB community of the northern arm of Great Salt Lake consists of moderate halophiles, which are salt-stressed at the in situ salinity of 27%.     

A microcosm study of nitrogen utilization in the Great Salt Lake,Utah

Microcosms were used to study the effects of two inorganic nitrogen sources (ammonia and nitrate) and two organic nitrogen sources (urea and glutamic acid) on the growth of algae and bacteria found in the Great Salt Lake, Utah. Ammonia, nitrate and urea stimulated bacterial growth indirectly through increased algal production of unknown organic substances. Glutamic acid, representing readily available organic carbon and nitrogen, stimulated the bacteria directly. No nitrification was observed in the microcosms although nitrite was found when the microcosms were supplemented with nitrate. Lake sediment contained a number of anaerobic bacteria producing hydrogen sulfide, methane and other gases. Production of these gases was stimulated in the columns with high algal and bacterial activity.     

Food-web modification by an invertebrate predator in the Great Salt Lake (USA)

Summary During unusually wet years the salinity of the Great Salt Lake (Utah) decreased from above 100 g/L to 50 g/L. This allowed the predaceous insect Trichocorixa verticalis to invade the pelagic region of the lake and reach a mean summer density of 52/m³. Concurrent changes in the pelagic ecosystem were: a decrease in the dry biomass of the previously dominant filter-feeding brine shrimp Artemia franciscana from 720 to 2 mg/m³, the invasion of three other zooplankton taxa, a 10 × decrease in community filtration rate, a 20 × increase in chlorophyll a concentration, a 4 × decrease in water clarity and perhaps a decrease in soluble nutrients. Trichocorixa abundance was also inversely correlated with the abundance of Artemia along a salinity gradient in the lake's estuary. In a 9-d microcosm experiment Trichocorixa preyed on nauplii and decreased the total density of Artemia from 103 to 6/L. The reduction in Artemia allowed protozoans to increase 10–100 ×. Changes in chlorophyll and clarity were consistent with those observed in the lake. These results suggest that invertebrate predation may be an important factor structuring simple food webs such as those found in moderately saline lakes.     

Life in extreme environments: microbial diversity in Great Salt Lake,Utah

Great Salt Lake (GSL) represents one of the world’s most hypersaline environments. In this study, the archaeal and bacterial communities at the North and South arms of the lake were surveyed by cloning and sequencing the 16S rRNA gene. The sampling locations were chosen for high salt concentration and the presence of unique environmental gradients, such as petroleum seeps and high sulfur content. Molecular techniques have not been systematically applied to this extreme environment, and thus the composition and the genetic diversity of microbial communities at GSL remain mostly unknown. This study led to the identification of 58 archaeal and 42 bacterial operational taxonomic units. Our phylogenetic and statistical analyses displayed a high biodiversity of the microbial communities in this environment. In this survey, we also showed that the majority of the 16S rRNA gene sequences within the clone library were distantly related to previously described environmental halophilic archaeal and bacterial taxa and represent novel phylotypes.     

Diversity, Activity, and Abundance of Sulfate-Reducing Bacteria in Saline and Hypersaline Soda Lakes

Soda lakes are naturally occurring highly alkaline and saline environments. Although the sulfur cycle is one of the most active element cycles in these lakes, little is known about the sulfate-reducing bacteria (SRB). In this study we investigated the diversity, activity, and abundance of SRB in sediment samples and enrichment cultures from a range of (hyper)saline soda lakes of the Kulunda Steppe in southeastern Siberia in Russia. For this purpose, a polyphasic approach was used, including denaturing gradient gel electrophoresis of dsr gene fragments, sulfate reduction rate measurements, serial dilutions, and quantitative real-time PCR (qPCR). Comparative sequence analysis revealed the presence of several novel clusters of SRB, mostly affiliated with members of the order Desulfovibrionales and family Desulfobacteraceae. We detected sulfate reducers and observed substantial sulfate reducing rates (between 12 and 423 μmol/dm³ day⁻¹) for most lakes, even at a salinity of 475 g/liter. Enrichments were obtained at salt saturating conditions (4 M Na⁺), using H₂ or volatile fatty acids as electron donors, and an extremely halophilic SRB, strain ASO3-1, was isolated. Furthermore, a high dsr gene copy number of 10⁸ cells per ml was detected in a hypersaline lake by qPCR. Our results indicate the presence of diverse and active SRB communities in these extreme ecosystems.     

Distribution of Methanogenic and Sulfate-Reducing Bacteria in Near-Shore Marine Sediments

The distribution of methanogenic and sulfate-reducing bacteria was examined in sediments from three sites off the coast of eastern Connecticut and five sites in Long Island Sound. Both bacterial groups were detected at all sites. Three distributional patterns were observed: (i) four sites exhibited methanogenic and sulfate-reducing populations which were restricted to the upper 10 to 20 cm, with a predominance of sulfate reducers; (ii) three sites in western Long Island Sound exhibited a methanogenic population most abundant in sediments deeper than those occupied by sulfate reducers; (iii) at one site that was influenced by fresh groundwater, methanogens and sulfate reducers were numerous within the same depths; however, the number of sulfate reducers varied vertically and temporally with sulfate concentrations. It was concluded that the distributions of abundant methanogenic and sulfate-reducing bacteria were mutually exclusive. Methanogenic enrichments yielded all genera of methanogens except Methanosarcina, with the methanobacteria predominating.     

Limnological control of brine shrimp population dynamics and cyst production in the Great Salt Lake, Utah

In the Great Salt Lake of Utah, the brine shrimp Artemia franciscanaKellogg is an important food resource for birds and they produce dormant cysts that are harvested and used extensively in the aquaculture industry. We analyzed the limnological factors controlling Artemia growth and cyst production over 12 months in 1994 and 1995. Laboratory experiments showed that inter-brood intervals were highly dependent on temperature and slightly on food level. At optimal temperatures and nutritious food, juveniles reached reproductive size within 7 d in the laboratory. In winter when temperatures were less than 3 °C, Artemia were absent from the lake, phytoplankton abundance was high (13 Chl a g l^–1), and the dominant grazers were ciliated protozoans. In the spring, cysts hatched when phytoplankton was abundant (15–30 g Chl a l^–1), and the Artemia grew and produced large clutches of ovoviviparous eggs. Estimated naupliar production from these eggs was 80 l^–1 from April to May. Despite the high production of nauplii, Artemia densities declined to 8 l^–1by June and the growing shrimp population grazed down the phytoplankton resource to <1 g Chl a l^–1. With the depleted phytoplankton food resource during the summer, Artemia growth slowed, lipid indices decreased, clutch sizes declined, and females switched primarily to oviparous cyst production. During the summer, there was limited production of ovoviviparous eggs, and limited recruitment of juveniles, probably due to low food. Although oviparous reproduction began in June, more than 90% of the cysts were produced after July when female densities had declined to 1.5 l^–1, but nearly all of them were producing cysts. Estimated cyst production was 650000 m^–2, or 4.54 × 10⁶ kg dry weight for the entire lake. The reported commercial harvest took 21% of the 1994 cyst production. That harvest had little impact on the subsequent year's population, as Artemia densities were ultimately controlled by algal production in the lake.     

Contrasting Patterns of Community Assembly in the Stratified Water Column of Great Salt Lake, Utah

Phylogenetic examinations of communities sampled along geochemical gradients provide a framework for inferring the relative importance of niche-based ecological interactions (competition, environmental filtering) and neutral-based evolutionary interactions in structuring biodiversity. Great Salt Lake (GSL) in Utah exhibits strong spatial gradients due to both seasonal variation in freshwater input into the watershed and restricted fluid flow within North America’s largest saline terminal lake ecosystem. Here, we examine the phylogenetic structure and composition of archaeal, bacterial, and eukaryal small subunit (SSU) rRNA genes sampled along a stratified water column (DWR3) in the south arm of GSL in order to infer the underlying mechanism of community assembly. Communities sampled from the DWR3 epilimnion were phylogenetically clustered (i.e., coexistence of close relatives due to environmental filtering) whereas those sampled from the DWR3 hypolimnion were phylogenetically overdispersed (i.e., coexistence of distant relatives due to competitive interactions), with minimal evidence for a role for neutral processes in structuring any assemblage. The shift from phylogenetically clustered to overdispersed assemblages was associated with an increase in salinity and a decrease in dissolved O₂ (DO) concentration. Likewise, the phylogenetic diversity and phylogenetic similarity of assemblages was strongly associated with salinity or DO gradients. Thus, salinity and/or DO appeared to influence the mechanism of community assembly as well as the phylogenetic diversity and composition of communities. It is proposed that the observed patterns in the phylogenetic composition and structure of DWR3 assemblages are attributable to the meromictic nature of GSL, which prevents significant mixing between the epilimnion and the hypolimnion. This leads to strong physicochemical gradients at the halocline, which are capable of supporting a greater diversity. However, concomitant shifts in nutrient availability (e.g., DO) at and below the halocline drive competitive interactions leading to hypolimnion assemblages with minimal niche overlap.     

Sulfate-Reducing Bacteria and Their Activities in Cyanobacterial Mats of Solar Lake (Sinai, Egypt)

The sulfate-reducing bacteria within the surface layer of the hypersaline cyanobacterial mat of Solar Lake (Sinai, Egypt) were investigated with combined microbiological, molecular, and biogeochemical approaches. The diurnally oxic surface layer contained between 10⁶ and 10⁷ cultivable sulfate-reducing bacteria ml⁻¹ and showed sulfate reduction rates between 1,000 and 2,200 nmol ml⁻¹ day⁻¹, both in the same range as and sometimes higher than those in anaerobic deeper mat layers. In the oxic surface layer and in the mat layers below, filamentous sulfate-reducing Desulfonema bacteria were found in variable densities of 10⁴ to 10⁶ cells ml⁻¹. A Desulfonema-related, diurnally migrating bacterium was detected with PCR and denaturing gradient gel electrophoresis within and below the oxic surface layer. Facultative aerobic respiration, filamentous morphology, motility, diurnal migration, and aggregate formation were the most conspicuous adaptations of Solar Lake sulfate-reducing bacteria to the mat matrix and to diurnal oxygen stress. A comparison of sulfate reduction rates within the mat and previously published photosynthesis rates showed that CO₂ from sulfate reduction in the upper 5 mm accounted for 7 to 8% of the total photosynthetic CO₂ demand of the mat.     

U(VI) Reduction in Sulfate-Reducing Subsurface Sediments Amended with Ethanol or Acetate

An experiment was conducted with subsurface sediments from Oak Ridge National Laboratory to determine the potential for reduction of U(VI) under sulfate-reducing conditions with either ethanol or acetate as the electron donor. The results showed extensive U(VI) reduction in sediments supplied with either electron donor, where geochemical and microbiological analyses demonstrated active sulfate reduction.     

Reduction of Cr(VI) by a Consortium of Sulfate-Reducing Bacteria (SRB III)

A consortium of bacteria with tolerance to high concentrations of Cr(VI) (up to 2,500 ppm) and other toxic heavy metals has been obtained from metal-refinishing wastewaters in Chengdu, People's Republic of China. This consortium consists of a range of gram-positive and gram-negative rods and has the capacity to reduce Cr(VI) to Cr(III) as amorphous precipitates which are associated with the bacterial surfaces. An endospore-producing, gram-positive rod and a gram-negative rod accumulate the most metallic precipitates, and, over time, 80 to 95% of Cr can be removed from concentrations ranging from 50 to 2,000 ppm (0.96 to 38.45 mM). Kinetic studies revealed a first-order constant for Cr removal of 0.1518 h^-1 for an initial concentration of 1,000 ppm (19.3 mM), and the sorption isothermal data could be interpreted by the Freundlich relationship. The sorption was not entirely due to a passive interaction with reactive sites on the bacterial surfaces since gamma-irradiated, killed cells could not immobilize as much metal. When U or Zn was added with the Cr, it was also removed and could even increase the total amount of Cr immobilized. The consortium was tolerant to small amounts of oxygen in the headspace of tubes, but active growth of the bacteria was a requirement for Cr immobilization through Cr(VI) reduction, resulting in the lowering of E_h. Our data suggest that the reduction was via H₂S. This consortium has been named SRB III, and it may be useful for the bioremediation of fluid metal-refining wastes.     

Influence of Limnological Conditions on Clostridium Botulinum Type E Presence in Eastern Lake Erie Sediments (Great Lakes, USA)

Avian and fish botulism outbreaks have been recorded since 1999 in eastern Lake Erie. These outbreaks are caused by Clostridium botulinum type E, a toxin-producing bacteria that is found in anoxic substrates rich in organic material. We studied the environmental conditions present in eastern Lake Erie during 2002, a year when several botulism outbreaks were observed. We also tested for the presence of C. botulinum type E in lake sediments. Samples were taken at six stations from two sites of different depths in the Dunkirk (New York, USA) area. The depth of the sampling sites influenced physico-chemical and biological processes in the sediments. We used the quantitative polymerase chain reaction (Q-PCR) to quantify the levels of C. botulinum type E in the samples. Sediment samples contained a patchy distribution of type E spore concentrations (from not detectable to 5520 DNA copies/mg). Samples of benthic invertebrates tested positive for C. botulinum type E spores in tissues (Gammarus 2028 DNA copies/mg, oligochaetes 428 DNA copies/mg, chironomids 148 DNA copies/mg and dreissenid mussels 715 DNA copies/mg). Principal components analysis (PCA) from inshore stations indicated that a decrease in dissolved oxygen, pH and redox potential near the sediment was associated to an increase in specific conductance and the type E toxin gene in sediments. We also found that C. botulinum type E spores are present in sediments at different depths and at different times through the ice-free season.     

Enumeration and Relative Importance of Acetylene-Reducing (Nitrogen-Fixing) Bacteria in a Delaware Salt Marsh

Three groups of N₂-fixing bacteria were enumerated from the top 1 cm of the surface in four vegetational areas in a Delaware salt marsh. The results over the 9-month sampling period showed that there were no discernible seasonal patterns for any of the groups enumerated (Azotobacter sp., Clostridium sp., and Desulfovibrio sp.). Azotobacter sp. was present in numbers of 10⁷ per g of dry mud, whereas the two anaerobic fixers were present in much lower numbers (10³ to 10⁴ per g of dry mud). There were no differences in the numbers of each group among the different vegetational areas, indicating that there was a heterogeneous population of N₂ fixers present. Additional studies indicate that the activity of sulfate reducers (Desulfovibrio sp.) may account for as much as 50% of the total observed acetylene reduction activity. Oxygen was found to exert little effect on the observed acetylene reduction activity, indicating that stable aerobic and anaerobic microenvironments exist in the surface layer of marsh sediments.     

Evidence for Microbial Fe(III) Reduction in Anoxic, Mining-Impacted Lake Sediments (Lake Coeur d'Alene, Idaho)

Mining-impacted sediments of Lake Coeur d'Alene, Idaho, contain more than 10% metals on a dry weight basis, approximately 80% of which is iron. Since iron (hydr)oxides adsorb toxic, ore-associated elements, such as arsenic, iron (hydr)oxide reduction may in part control the mobility and bioavailability of these elements. Geochemical and microbiological data were collected to examine the ecological role of dissimilatory Fe(III)-reducing bacteria in this habitat. The concentration of mild-acid-extractable Fe(II) increased with sediment depth up to 50 g kg⁻¹, suggesting that iron reduction has occurred recently. The maximum concentrations of dissolved Fe(II) in interstitial water (41 mg liter⁻¹) occurred 10 to 15 cm beneath the sediment-water interface, suggesting that sulfidogenesis may not be the predominant terminal electron-accepting process in this environment and that dissolved Fe(II) arises from biological reductive dissolution of iron (hydr)oxides. The concentration of sedimentary magnetite (Fe₃O₄), a common product of bacterial Fe(III) hydroxide reduction, was as much as 15.5 g kg⁻¹. Most-probable-number enrichment cultures revealed that the mean density of Fe(III)-reducing bacteria was 8.3 × 10⁵ cells g (dry weight) of sediment⁻¹. Two new strains of dissimilatory Fe(III)-reducing bacteria were isolated from surface sediments. Collectively, the results of this study support the hypothesis that dissimilatory reduction of iron has been and continues to be an important biogeochemical process in the environment examined.     

Community Structure, Cellular rRNA Content, and Activity of Sulfate-Reducing Bacteria in Marine Arctic Sediments

The community structure of sulfate-reducing bacteria (SRB) of a marine Arctic sediment (Smeerenburgfjorden, Svalbard) was characterized by both fluorescence in situ hybridization (FISH) and rRNA slot blot hybridization by using group- and genus-specific 16S rRNA-targeted oligonucleotide probes. The SRB community was dominated by members of the Desulfosarcina-Desulfococcus group. This group accounted for up to 73% of the SRB detected and up to 70% of the SRB rRNA detected. The predominance was shown to be a common feature for different stations along the coast of Svalbard. In a top-to-bottom approach we aimed to further resolve the composition of this large group of SRB by using probes for cultivated genera. While this approach failed, directed cloning of probe-targeted genes encoding 16S rRNA was successful and resulted in sequences which were all affiliated with the Desulfosarcina-Desulfococcus group. A group of clone sequences (group SVAL1) most closely related to Desulfosarcina variabilis (91.2% sequence similarity) was dominant and was shown to be most abundant in situ, accounting for up to 54.8% of the total SRB detected. A comparison of the two methods used for quantification showed that FISH and rRNA slot blot hybridization gave comparable results. Furthermore, a combination of the two methods allowed us to calculate specific cellular rRNA contents with respect to localization in the sediment profile. The rRNA contents of Desulfosarcina-Desulfococcus cells were highest in the first 5 mm of the sediment (0.9 and 1.4 fg, respectively) and decreased steeply with depth, indicating that maximal metabolic activity occurred close to the surface. Based on SRB cell numbers, cellular sulfate reduction rates were calculated. The rates were highest in the surface layer (0.14 fmol cell⁻¹ day⁻¹), decreased by a factor of 3 within the first 2 cm, and were relatively constant in deeper layers.     

Comparative Analysis of Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in Anoxic Marine Sediments

The oxidation of methane in anoxic marine sediments is thought to be mediated by a consortium of methane-consuming archaea and sulfate-reducing bacteria. In this study, we compared results of rRNA gene (rDNA) surveys and lipid analyses of archaea and bacteria associated with methane seep sediments from several different sites on the Californian continental margin. Two distinct archaeal lineages (ANME-1 and ANME-2), peripherally related to the order Methanosarcinales, were consistently associated with methane seep marine sediments. The same sediments contained abundant ¹³C-depleted archaeal lipids, indicating that one or both of these archaeal groups are members of anaerobic methane-oxidizing consortia. ¹³C-depleted lipids and the signature 16S rDNAs for these archaeal groups were absent in nearby control sediments. Concurrent surveys of bacterial rDNAs revealed a predominance of δ-proteobacteria, in particular, close relatives of Desulfosarcina variabilis. Biomarker analyses of the same sediments showed bacterial fatty acids with strong ¹³C depletion that are likely products of these sulfate-reducing bacteria. Consistent with these observations, whole-cell fluorescent in situ hybridization revealed aggregations of ANME-2 archaea and sulfate-reducing Desulfosarcina and Desulfococcus species. Additionally, the presence of abundant ¹³C-depleted ether lipids, presumed to be of bacterial origin but unrelated to ether lipids of members of the order Desulfosarcinales, suggests the participation of additional bacterial groups in the methane-oxidizing process. Although the Desulfosarcinales and ANME-2 consortia appear to participate in the anaerobic oxidation of methane in marine sediments, our data suggest that other bacteria and archaea are also involved in methane oxidation in these environments.     

Effects of Metals on Methanogenesis, Sulfate Reduction, Carbon Dioxide Evolution, and Microbial Biomass in Anoxic Salt Marsh Sediments

The effects of several metals on microbial methane, carbon dioxide, and sulfide production and microbial ATP were examined in sediments from Spartina alterniflora communities. Anaerobically homogenized sediments were amended with 1,000 ppm (ratio of weight of metal to dry weight of sediment) of various metals. Time courses in controls were similar for CH₄, H₂S, and CO₂, with short initial lags (0 to 4 h) followed by periods of constant gas production (1 to 2 days) and declining rates thereafter. Comparisons were made between control and experimental assays with respect to initial rates of production (after lag) and overall production. Methane evolution was inhibited both initially and overall by CH₃HgCl, HgS, and NaAsO₂. A period of initial inhibition was followed by a period of overall stimulation with Hg, Pb, Ni, Cd, and Cu, all as chlorides, and with ZnSO₄, K₂CrO₄, and K₂Cr₂O₇. Production of CO₂ was generally less affected by the addition of metals. Inhibition was noted with NaAsO₂, CH₃HgCl, and Na₂MoO₄. Minor stimulation of CO₂ production occurred over the long term with chlorides of Hg, Pb, and Fe. Sulfate reduction was inhibited in the short term by all metals tested and over the long term by all but FeCl₂ and NiCl₂. Microbial biomass was decreased by FeCl₂, K₂Cr₂O₇, ZnSO₄, CdCl₂, and CuCl₂ but remained generally unaffected by PbCl₂, HgCl₂, and NiCl₂. Although the majority of metals produced an immediate inhibition of methanogenesis, for several metals this was only a transient phenomenon followed by an overall stimulation. The initial suppression of methanogenesis may be relieved by precipitation, complexation, or transformation of the metal (possibly by methylation), with the subsequent stimulation resulting from a sustained inhibition of competing organisms (e.g., sulfate-reducing bacteria). For several environmentally significant metals, severe metal pollution may substantially alter the flow of carbon in sediments.