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Community structure and metabolism through reconstruction of microbial genomes from the environment

Abstract

Microbial communities are vital in the functioning of all ecosystems; however, most microorganisms are uncultivated, and their roles in natural systems are unclear. Here, using random shotgun sequencing of DNA from a natural acidophilic biofilm, we report reconstruction of near-complete genomes of Leptospirillum group II and Ferroplasma type II, and partial recovery of three other genomes. This was possible because the biofilm was dominated by a small number of species populations and the frequency of genomic rearrangements and gene insertions or deletions was relatively low. Because each sequence read came from a different individual, we could determine that single-nucleotide polymorphisms are the predominant form of heterogeneity at the strain level. The Leptospirillum group II genome had remarkably few nucleotide polymorphisms, despite the existence of low-abundance variants. The Ferroplasma type II genome seems to be a composite from three ancestral strains that have undergone homologous recombination to form a large population of mosaic genomes. Analysis of the gene complement for each organism revealed the pathways for carbon and nitrogen fixation and energy generation, and provided insights into survival strategies in an extreme environment.

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Figure 1: The pink biofilm.
Figure 2: Segment of the Ferroplasma type II composite genome.
Figure 3
Figure 4: Cell metabolic cartoons constructed from the annotation of 2,180 ORFs identified in the Leptospirillum group II genome (63% with putative assigned function) and 1,931 ORFs in the Ferroplasma type II genome (58% with assigned function).

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Acknowledgements

This research was funded by the US Department of Energy Microbial Genomics Program and the National Science Foundation Biocomplexity Program. We would like to thank M. Power, W. Getz, R. Blake, J. Handlesman, B. Baker, I. Lo, J. Flanagan, D. Dodds and R. Carver for their contributions to this work. We also thank C. Detter and members of his laboratory at JGI for help with library construction, and T. Arman (Iron Mountain Mines) and R. Sugarek (EPA) for access to the Richmond mine.

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Correspondence to Jillian F. Banfield.

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Tyson, G., Chapman, J., Hugenholtz, P. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43 (2004). https://doi.org/10.1038/nature02340

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