Insights into the phylogeny and coding potential of microbial dark matter

Christian Rinke, Patrick Schwientek, Alexander Sczyrba, Natalia N. Ivanova, Iain J. Anderson, Jan-Fang Cheng, Aaron Darling, Stephanie Malfatti, Brandon K. Swan, Esther A. Gies, Jeremy A. Dodsworth, Brian P. Hedlund, George Tsiamis, Stefan M. Sievert, Wen-Tso Liu, Jonathan A. Eisen, Steven J. Hallam, Nikos C. Kyrpides, Ramunas Stepanauskas, Edward M. Rubin, Philip Hugenholtz () and Tanja Woyke ()
Additional contact information
Christian Rinke: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Patrick Schwientek: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Alexander Sczyrba: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Natalia N. Ivanova: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Iain J. Anderson: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Jan-Fang Cheng: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Aaron Darling: University of California Davis, Davis, California 95616, USA
Stephanie Malfatti: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Brandon K. Swan: Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine 04544-0380, USA
Esther A. Gies: University of British Columbia, Vancouver, British Columbia, V6T 1Z3 Canada
Jeremy A. Dodsworth: School of Life Sciences, University of Nevada, Las Vegas, Nevada 89154-4004, USA
Brian P. Hedlund: School of Life Sciences, University of Nevada, Las Vegas, Nevada 89154-4004, USA
George Tsiamis: University of Patras, Agrinio, T.K. 30100, Greece
Stefan M. Sievert: Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA
Wen-Tso Liu: University of Illinois at Urbana-Champaign, Urbana, Illinois 61802, USA
Jonathan A. Eisen: University of California Davis, Davis, California 95616, USA
Steven J. Hallam: University of British Columbia, Vancouver, British Columbia, V6T 1Z3 Canada
Nikos C. Kyrpides: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Ramunas Stepanauskas: Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine 04544-0380, USA
Edward M. Rubin: DOE Joint Genome Institute, Walnut Creek, California 94598, USA
Philip Hugenholtz: Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences and Institute for Molecular Bioscience, The University of Queensland
Tanja Woyke: DOE Joint Genome Institute, Walnut Creek, California 94598, USA

Nature, 2013, vol. 499, issue 7459, 431-437

Abstract: Abstract Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called ‘microbial dark matter’. With this additional genomic information, we are able to resolve many intra- and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.

Date: 2013
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DOI: 10.1038/nature12352

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