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Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage.

ABSTRACT: A legacy of coal mining in the Appalachians has provided a unique opportunity to study the ecological niches of iron-oxidizing microorganisms. Mine-impacted, anoxic groundwater with high dissolved-metal concentrations emerges at springs and seeps associated with iron oxide mounds and deposits. These deposits are colonized by iron-oxidizing microorganisms that in some cases efficiently remove most of the dissolved iron at low pH, making subsequent treatment of the polluted stream water less expensive. We used full-cycle rRNA methods to describe the composition of sediment communities at two geochemically similar acidic discharges, Upper and Lower Red Eyes in Somerset County, PA, USA. The dominant microorganisms at both discharges were acidophilic Gallionella-like organisms, “Ferrovum” spp., and Acidithiobacillus spp. Archaea and Leptospirillum spp. accounted for less than 2% of cells. The distribution of microorganisms at the two sites could be best explained by a combination of iron(II) concentration and pH. Populations of the Gallionella-like organisms were restricted to locations with pH>3 and iron(II) concentration of >4 mM, while Acidithiobacillus spp. were restricted to pH<3 and iron(II) concentration of <4 mM. Ferrovum spp. were present at low levels in most samples but dominated sediment communities at pH<3 and iron(II) concentration of >4 mM. Our findings offer a predictive framework that could prove useful for describing the distribution of microorganisms in acid mine drainage, based on readily accessible geochemical parameters.

SUBMITTER: Jones DS

PROVIDER: S-EPMC4309714 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage.

Jones Daniel S DS Kohl Courtney C Grettenberger Christen C Larson Lance N LN Burgos William D WD Macaladya Jennifer L JL

Applied and environmental microbiology 20150201 4

A legacy of coal mining in the Appalachians has provided a unique opportunity to study the ecological niches of iron-oxidizing microorganisms. Mine-impacted, anoxic groundwater with high dissolved-metal concentrations emerges at springs and seeps associated with iron oxide mounds and deposits. These deposits are colonized by iron-oxidizing microorganisms that in some cases efficiently remove most of the dissolved iron at low pH, making subsequent treatment of the polluted stream water less expen ...[more]

PMID: 25501473

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Project description:Natural attenuation of heavy metals occurs via coupled microbial iron cycling and metal precipitation in creeks impacted by acid mine drainage (AMD). Here, we describe the isolation, characterization, and genomic sequencing of two iron-oxidizing bacteria (FeOB) species: Thiomonas ferrovorans FB-6 and Thiomonas metallidurans FB-Cd, isolated from slightly acidic (pH 6.3), Fe-rich, AMD-impacted creek sediments. These strains precipitated amorphous iron oxides, lepidocrocite, goethite, and magnetite or maghemite and grew at a pH optimum of 5.5. While Thiomonas spp. are known as mixotrophic sulfur oxidizers and As oxidizers, the FB strains oxidized Fe, which suggests they can efficiently remove Fe and other metals via coprecipitation. Previous evidence for Thiomonas sp. Fe oxidation is largely ambiguous, possibly because of difficulty demonstrating Fe oxidation in heterotrophic/mixotrophic organisms. Therefore, we also conducted a genomic analysis to identify genetic mechanisms of Fe oxidation, other metal transformations, and additional adaptations, comparing the two FB strain genomes with 12 other Thiomonas genomes. The FB strains fall within a relatively novel group of Thiomonas strains that includes another strain (b6) with solid evidence of Fe oxidation. Most Thiomonas isolates, including the FB strains, have the putative iron oxidation gene cyc2, but only the two FB strains possess the putative Fe oxidase genes mtoAB The two FB strain genomes contain the highest numbers of strain-specific gene clusters, greatly increasing the known Thiomonas genetic potential. Our results revealed that the FB strains are two distinct novel species of Thiomonas with the genetic potential for bioremediation of AMD via iron oxidation.IMPORTANCE As AMD moves through the environment, it impacts aquatic ecosystems, but at the same time, these ecosystems can naturally attenuate contaminated waters via acid neutralization and catalyzing metal precipitation. This is the case in the former Ronneburg uranium-mining district, where AMD impacts creek sediments. We isolated and characterized two iron-oxidizing Thiomonas species that are mildly acidophilic to neutrophilic and that have two genetic pathways for iron oxidation. These Thiomonas species are well positioned to naturally attenuate AMD as it discharges across the landscape.

Project description:The Richmond Mine at Iron Mountain, Shasta County, California, USA provides an excellent opportunity to study the chemical and biological controls on acid mine drainage (AMD) generation in situ, and to identify key factors controlling solution chemistry. Here we integrate four years of field-based geochemical data with 16S rRNA gene clone libraries and rRNA probe-based studies of microbial population structure, cultivation-based metabolic experiments, arsenopyrite surface colonization experiments, and results of intermediate sulfur species kinetics experiments to describe the Richmond Mine AMD system. Extremely acidic effluent (pH between 0.5 and 0.9) resulting from oxidation of approximately 1 × 105 to 2 × 105 moles pyrite/day contains up to 24 g/1 Fe, several g/1 Zn and hundreds of mg/l Cu. Geochemical conditions change markedly over time, and are reflected in changes in microbial populations. Molecular analyses of 232 small subunit ribosomal RNA (16S rRNA) gene sequences from six sites during a sampling time when lower temperature (<32°C), higher pH (>0.8) conditions predominated show the dominance of Fe-oxidizing prokaryotes such as Ferroplasma and Leptospirillum in the primary drainage communities. Leptospirillum group III accounts for the majority of Leptospirillum sequences, which we attribute to anomalous physical and geochemical regimes at that time. A couple of sites peripheral to the main drainage, "Red Pool" and a pyrite "Slump," were even higher in pH (>1) and the community compositions reflected this change in geochemical conditions. Several novel lineages were identified within the archaeal Thermoplasmatales order associated with the pyrite slump, and the Red Pool (pH 1.4) contained the only population of Acidithiobacillus. Relatively small populations of Sulfobacillus spp. and Acidithiobacillus caldus may metabolize elemental sulfur as an intermediate species in the oxidation of pyritic sulfide to sulfate. Experiments show that elemental sulfur which forms on pyrite surfaces is resistant to most oxidants; its solublization by unattached cells may indicate involvement of a microbially derived electron shuttle. The detachment of thiosulfate () as a leaving group in pyrite oxidation should result in the formation and persistence of tetrathionate in low pH ferric iron-rich AMD solutions. However, tetrathionate is not observed. Although a -like species may form as a surface-bound intermediate, data suggest that Fe3+ oxidizes the majority of sulfur to sulfate on the surface of pyrite. This may explain why microorganisms that can utilize intermediate sulfur species are scarce compared to Fe-oxidizing taxa at the Richmond Mine site.

Project description:The microbial community of acid mine drainage (AMD) fascinates researchers by their adaption and roles in shaping the environment. Molecular surveys have recently helped to enhance the understanding of the distribution, adaption strategy, and ecological function of microbial communities in extreme AMD environments. However, the interactions between the environment and microbial community of extremely acidic AMD (pH <3) from different mining areas kept unanswered questions. Here, we measured physicochemical parameters and profiled the microbial community of AMD collected from four mining areas with different mineral types to provide a better understanding of biogeochemical processes within the extremely acidic water environment. The prominent physicochemical differences across the four mining areas were in SO4 2-, metal ions, and temperature, and distinct microbial diversity and community assemblages were also discovered in these areas. Mg2+ and SO4 2- were the predominant factors determining the microbial structure and prevalence of dominant taxa in AMD. Leptospirillum, Ferroplasma, and Acidithiobacillus were abundant but showed different occurrence patterns in AMD from different mining areas. More diverse communities and functional redundancy were identified in AMD of polymetallic mining areas compared with AMD of copper mining areas. Functional prediction revealed iron, sulfur, nitrogen, and carbon metabolisms driven by microorganisms were significantly correlated with Mg2+ and SO4 2-, Ca2+, temperature, and Fe2+, which distinguish microbial communities of copper mine AMD from that of polymetallic mine AMD. In summary, microbial diversity, composition, and metabolic potential were mainly shaped by Mg2+ and SO4 2- concentrations of AMD, suggesting that the substrate concentrations may contribute to the distinct microbiological profiles of AMD from different mining areas. These findings highlight the microbial community structure in extremely acidic AMD forming by types of minerals and the interactions of physicochemical parameters and microbiology, providing more clues of the microbial ecological function and adaptation mechanisms in the extremely acidic environment.

Dataset Information

Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage.

Publications

Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage.

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