Dataset Information

Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics.

ABSTRACT: High-throughput sequencing is expanding our knowledge of microbial diversity in the environment. Still, understanding the metabolic potentials and ecological roles of rare and uncultured microbes in natural communities remains a major challenge. To this end, we applied a 'divide and conquer' strategy that partitioned a massive metagenomic data set (>100?Gbp) into subsets based on K-mer frequency in sequence assembly to a low-diversity acid mine drainage (AMD) microbial community and, by integrating with an additional metatranscriptomic assembly, successfully obtained 11 draft genomes most of which represent yet uncultured and/or rare taxa (relative abundance <1%). We report the first genome of a naturally occurring Ferrovum population (relative abundance >90%) and its metabolic potentials and gene expression profile, providing initial molecular insights into the ecological role of these lesser known, but potentially important, microorganisms in the AMD environment. Gene transcriptional analysis of the active taxa revealed major metabolic capabilities executed in situ, including carbon- and nitrogen-related metabolisms associated with syntrophic interactions, iron and sulfur oxidation, which are key in energy conservation and AMD generation, and the mechanisms of adaptation and response to the environmental stresses (heavy metals, low pH and oxidative stress). Remarkably, nitrogen fixation and sulfur oxidation were performed by the rare taxa, indicating their critical roles in the overall functioning and assembly of the AMD community. Our study demonstrates the potential of the 'divide and conquer' strategy in high-throughput sequencing data assembly for genome reconstruction and functional partitioning analysis of both dominant and rare species in natural microbial assemblages.

SUBMITTER: Hua ZS

PROVIDER: S-EPMC4438317 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics.

Hua Zheng-Shuang ZS Han Yu-Jiao YJ Chen Lin-Xing LX Liu Jun J Hu Min M Li Sheng-Jin SJ Kuang Jia-Liang JL Chain Patrick S G PS Huang Li-Nan LN Shu Wen-Sheng WS

The ISME journal 20141107 6

High-throughput sequencing is expanding our knowledge of microbial diversity in the environment. Still, understanding the metabolic potentials and ecological roles of rare and uncultured microbes in natural communities remains a major challenge. To this end, we applied a 'divide and conquer' strategy that partitioned a massive metagenomic data set (>100 Gbp) into subsets based on K-mer frequency in sequence assembly to a low-diversity acid mine drainage (AMD) microbial community and, by integrat ...[more]

PMID: 25361395

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Project description:Svalbard, situated in the high Arctic, is an important past and present coal mining area. Dozens of abandoned waste rock piles can be found in the proximity of Longyearbyen. This environment offers a unique opportunity for studying the biological control over the weathering of sulphide rocks at low temperatures. Although the extension and impact of acid mine drainage (AMD) in this area is known, the native microbial communities involved in this process are still scarcely studied and uncharacterized. Several abandoned mining areas were explored in the search for active AMD and a culture-independent approach was applied with samples from two different runoffs for the identification and quantification of the native microbial communities. The results obtained revealed two distinct microbial communities. One of the runoffs was more extreme with regards to pH and higher concentration of soluble iron and heavy metals. These conditions favored the development of algal-dominated microbial mats. Typical AMD microorganisms related to known iron-oxidizing bacteria (Acidithiobacillus ferrivorans, Acidobacteria and Actinobacteria) dominated the bacterial community although some unexpected populations related to Chloroflexi were also significant. No microbial mats were found in the second area. The geochemistry here showed less extreme drainage, most likely in direct contact with the ore under the waste pile. Large deposits of secondary minerals were found and the presence of iron stalks was revealed by microscopy analysis. Although typical AMD microorganisms were also detected here, the microbial community was dominated by other populations, some of them new to this type of system (Saccharibacteria, Gallionellaceae). These were absent or lowered in numbers the farther from the spring source and they could represent native populations involved in the oxidation of sulphide rocks within the waste rock pile. This environment appears thus as a highly interesting field of potential novelty in terms of both phylogenetic/taxonomic and functional diversity.

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.

Dataset Information

Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics.

Publications

Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics.

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