Physiology and phylogeny of the candidate phylum “Atribacteria” (formerly OP9/JS1) inferred from single-cell genomics and metagenomics

Jeremy A Dodsworth1,2, Senthil Murugapiran3, Paul C Blainey4, Masaru Nobu5, Christian Rinke6, Patrick Schwientek6, Esther Gies7, Gordon Webster8, Peter Kille8, Andrew Weightman8, Wen-Tso Liu5, Steven James Hallam7, George Tsiamis9, Wesley Swingley10, Christian Ross11, Susannah G Tringe12, Patrick SG Chain13,14, Matthew B Scholz6,15, Chien-Chi Lo13,14, Jason Raymond16, Stephen R Quake17, Tanja Woyke6 and Brian P Hedlund11, (1)California State University, San Bernardino, San Bernardino, United States, (2)California State University San Bernardino, Department of BIology, San Bernardino, CA, United States, (3)University of Minnesota Twin Cities, Minneapolis, MN, United States, (4)Broad Institute, Cambridge, MA, United States, (5)University of Illinois at Urbana Champaign, Urbana, IL, United States, (6)DOE Joint Genome Institute, Walnut Creek, CA, United States, (7)University of British Columbia, Department of Microbiology and Immunology, Vancouver, BC, Canada, (8)Cardiff University, Cardiff, United Kingdom, (9)University of Patras, Patras, Greece, (10)Northern Illinois University, DeKalb, IL, United States, (11)University of Nevada Las Vegas, Las Vegas, NV, United States, (12)DOE Joint Genome Institute, Berkeley, CA, United States, (13)Los Alamos National Laboratory, Los Alamos, United States, (14)Los Alamos National Laboratory, Genomic Science Group, Los Alamos, United States, (15)Los Alamos National Laboratory, Genomic Science Group, Los Alamos, NM, United States, (16)Arizona State University, School of Earth and Space Exploration, Tempe, AZ, United States, (17)Stanford University, Department of Bioengineering, Stanford, CA, United States
Abstract:
Single-cell sequencing and metagenomics have extended the genomics revolution to yet-uncultivated microorganisms and provided insights into the coding potential of this so-called "microbial dark matter", including microbes belonging candidate phyla with no cultivated representatives. As more datasets emerge, comparison of individual genomes from different lineages and habitats can provide insight into the phylogeny, conserved features, and potential metabolic diversity of candidate phyla. The candidate bacterial phylum OP9 was originally found in Obsidian Pool, Yellowstone National Park, and it has since been detected in geothermal springs, petroleum reservoirs, and engineered thermal environments worldwide. JS1, another uncultivated bacterial lineage affiliated with OP9, is often abundant in marine sediments associated with methane hydrates, hydrocarbon seeps, and on continental margins and shelves, and is found in other non-thermal marine and subsurface environments. The phylogenetic relationship between OP9, JS1, and other Bacteria has not been fully resolved, and to date no axenic cultures from these lineages have been reported. Recently, 31 single amplified genomes (SAGs) from six distinct OP9 and JS1 lineages have been obtained using flow cytometric and microfluidic techniques. These SAGs were used to inform metagenome binning techniques that identified OP9/JS1 sequences in several metagenomes, extending genomic coverage in three of the OP9 and JS1 lineages. Phylogenomic analyses of these SAG and metagenome bin datasets suggest that OP9 and JS1 constitute a single, deeply branching phylum, for which the name "Atribacteria" has recently been proposed. Overall, members of the "Atribacteria" are predicted to be heterotrophic anaerobes without the capacity for respiration, with some lineages potentially specializing in secondary fermentation of organic acids. A set of signature "Atribacteria" genes was tentatively identified, including components of a bacterial microcompartments gene cluster that may be involved in carbohydrate catabolism. The "Atribacteria" may play important roles in biomass processing in anaerobic geothermal and subsurface environments.
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