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Open Access Highly Accessed Research article

Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea

Alexis P Yelton15, Luis R Comolli2, Nicholas B Justice3, Cindy Castelle2, Vincent J Denef46, Brian C Thomas4 and Jillian F Banfield14*

Author Affiliations

1 Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720, USA

2 Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

3 Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA

4 Department of Earth and Planetary Sciences, University of California, Berkeley, CA 94720, USA

5 Current address: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

6 Current address: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA

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BMC Genomics 2013, 14:485  doi:10.1186/1471-2164-14-485

Published: 17 July 2013

Abstract

Background

Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order.

Results

We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis.

Conclusion

The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.

Keywords:
Metagenomics; Acid mine drainage; Thermoplasmatales; Ferroplasma; Iron oxidation; Comparative genomics