UC Berkeley UC Berkeley Previously Published Works Title A new view of the tree of life. Permalink https://escholarship.org/uc/item/65h6718x Journal Nature microbiology, 1(5) ISSN 2058-5276 Authors Hug, Laura A Baker, Brett J Anantharaman, Karthik et al. Publication Date 2016-04-11 DOI 10.1038/nmicrobiol.2016.48 Peer reviewed eScholarship.org Powered by the California Digital Library University of California LETTERS PUBLISHED: 11 APRIL 2016 | ARTICLE NUMBER: 16048 | DOI: 10.1038/NMICROBIOL.2016.48 OPEN A new view of the tree of life Laura A. Hug1†, Brett J. Baker2, Karthik Anantharaman1, Christopher T. Brown3, Alexander J. Probst1, Cindy J. Castelle1,CristinaN.Butterfield1,AlexW.Hernsdorf3, Yuki Amano4,KotaroIse4, Yohey Suzuki5, Natasha Dudek6,DavidA.Relman7,8, Kari M. Finstad9, Ronald Amundson9, Brian C. Thomas1 and Jillian F. Banfield1,9* The tree of life is one of the most important organizing prin- Contributing to this expansion in genome numbers are single cell ciples in biology1. Gene surveys suggest the existence of an genomics13 and metagenomics studies. Metagenomics is a shotgun enormous number of branches2, but even an approximation of sequencing-based method in which DNA isolated directly from the the full scale of the tree has remained elusive. Recent depic- environment is sequenced, and the reconstructed genome fragments tions of the tree of life have focused either on the nature of are assigned to draft genomes14. New bioinformatics methods yield deep evolutionary relationships3–5 or on the known, well-classi- complete and near-complete genome sequences, without a reliance fied diversity of life with an emphasis on eukaryotes6. These on cultivation or reference genomes7,15. These genome- (rather than approaches overlook the dramatic change in our understanding gene) based approaches provide information about metabolic poten- of life’s diversity resulting from genomic sampling of previously tial and a variety of phylogenetically informative sequences that can unexamined environments. New methods to generate genome be used to classify organisms16. Here, we have constructed a tree sequences illuminate the identity of organisms and their meta- of life by making use of genomes from public databases and 1,011 bolic capacities, placing them in community and ecosystem con- newly reconstructed genomes that we recovered from a variety of texts7,8. Here, we use new genomic data from over 1,000 environments (see Methods). uncultivated and little known organisms, together with pub- To render this tree of life, we aligned and concatenated a set of 16 lished sequences, to infer a dramatically expanded version of ribosomal protein sequences from each organism. This approach the tree of life, with Bacteria, Archaea and Eukarya included. yields a higher-resolution tree than is obtained from a single gene, The depiction is both a global overview and a snapshot of the such as the widely used 16S rRNA gene16. The use of ribosomal pro- diversity within each major lineage. The results reveal the dom- teins avoids artefacts that would arise from phylogenies constructed inance of bacterial diversification and underline the importance using genes with unrelated functions and subject to different evol- of organisms lacking isolated representatives, with substantial utionary processes. Another important advantage of the chosen evolution concentrated in a major radiation of such organisms. ribosomal proteins is that they tend to be syntenic and co-located This tree highlights major lineages currently underrepresented in a small genomic region in Bacteria and Archaea, reducing in biogeochemical models and identifies radiations that are binning errors that could substantially perturb the geometry of probably important for future evolutionary analyses. the tree. Included in this tree is one representative per genus for Early approaches to describe the treeoflifedistinguishedorganisms all genera for which high-quality draft and complete genomes based on their physical characteristics and metabolic features. exist (3,083 organisms in total). Molecular methods dramatically broadened the diversity that could Despite the methodological challenges, we have included repre- be included in the tree because they circumvented the need for direct sentatives of all three domains of life. Our primary focus relates to observation and experimentation by relying on sequenced genes as the status of Bacteria and Archaea, as these organisms have been markers for lineages. Gene surveys, typically using the small subunit most difficult to profile using macroscopic approaches, and substan- ribosomal RNA (SSU rRNA) gene, provided a remarkable and novel tial progress has been made recently with acquisition of new genome view of the biological world1,9,10, but questions about the structure sequences7,8,13. The placement of Eukarya relative to Bacteria and and extent of diversity remain. Organisms from novel lineages have Archaea is controversial1,4,5,17,18. Eukaryotes are believed to be evol- eluded surveys, because many are invisible to these methods due to utionary chimaeras that arose via endosymbiotic fusion, probably sequence divergence relative to the primers commonly used for gene involving bacterial and archaeal cells19. Here, we do not attempt amplification7,11. Furthermore, unusual sequences, including those to confidently resolve the placement of the Eukarya. We position with unexpected insertions, may be discarded as artefacts7. them using sequences of a subset of their nuclear-encoded riboso- Wholegenomereconstructionwasfirst accomplished in 1995 mal proteins, an approach that classifies them based on the inheri- (ref. 12), with a near-exponential increase in the number of draft tance of their information systems as opposed to lipid or other genomes reported each subsequent year. There are 30,437 genomes cellular structures5. from all three domains of life—Bacteria, Archaea and Eukarya— Figure 1 presents a new view of the tree of life. This is one of a which are currently available in the Joint Genome Institute’s relatively small number of three-domain trees constructed from Integrated Microbial Genomes database (accessed 24 September 2015). molecular information so far, and the first comprehensive tree to 1Department of Earth and Planetary Science, UC Berkeley, Berkeley, California 94720, USA. 2Department of Marine Science, University of Texas Austin, Port Aransas, Texas 78373, USA. 3Department of Plant and Microbial Biology, UC Berkeley, Berkeley, California 94720, USA. 4Sector of Decommissioning and Radioactive Wastes Management, Japan Atomic Energy Agency, Ibaraki 319-1184, Japan. 5Graduate School of Science, The University of Tokyo, Tokyo 113-8654, Japan. 6Department of Ecology and Evolutionary Biology, UC Santa Cruz, Santa Cruz, California 95064, USA. 7Departments of Medicine and of Microbiology and Immunology, Stanford University, Stanford, California 94305, USA. 8Veterans Affairs Palo Alto Health Care System, Palo Alto, California 94304, USA. 9Department of Environmental Science, Policy, and Management, UC Berkeley, Berkeley, California 94720, USA. †Present address: Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada. *e-mail: jbanfi[email protected] NATURE MICROBIOLOGY | VOL 1 | MAY 2016 | www.nature.com/naturemicrobiology 1 © 2016 Macmillan Publishers Limited. All rights reserved LETTERS NATURE MICROBIOLOGY DOI: 10.1038/NMICROBIOL.2016.48 (Tenericutes) Bacteria Actinobacteria Armatimonadetes Nomurabacteria Kaiserbacteria Zixibacteria Atribacteria Adlerbacteria Cloacimonetes Aquificae Chloroflexi Campbellbacteria Fibrobacteres Calescamantes Gemmatimonadetes Caldiserica Firmicutes WOR-3 Dictyoglomi TA06 Thermotogae Cyanobacteria Poribacteria Deinococcus-Therm. Latescibacteria Synergistetes Giovannonibacteria BRC1 Fusobacteria Wolfebacteria Melainabacteria Jorgensenbacteria Marinimicrobia RBX1 Ignavibacteria Bacteroidetes WOR1 Chlorobi Caldithrix Azambacteria PVC Parcubacteria superphylum Yanofskybacteria Planctomycetes Moranbacteria Elusimicrobia Chlamydiae, Lentisphaerae, Magasanikbacteria Verrucomicrobia Uhrbacteria Falkowbacteria Candidate Omnitrophica Phyla Radiation SM2F11 Rokubacteria NC10 Aminicentantes Peregrinibacteria Acidobacteria Tectomicrobia, Modulibacteria Gracilibacteria BD1-5, GN02 Nitrospinae Absconditabacteria SR1 Nitrospirae Saccharibacteria Dadabacteria Berkelbacteria Deltaprotebacteria (Thermodesulfobacteria) Chrysiogenetes Deferribacteres Hydrogenedentes NKB19 Woesebacteria Spirochaetes Shapirobacteria Wirthbacteria Amesbacteria TM6 Collierbacteria Epsilonproteobacteria Pacebacteria Beckwithbacteria Roizmanbacteria Dojkabacteria WS6 Gottesmanbacteria CPR1 Levybacteria CPR3 Daviesbacteria Microgenomates Katanobacteria Curtissbacteria Alphaproteobacteria WWE3 Zetaproteo. Acidithiobacillia Betaproteobacteria Major lineages with isolated representative: italics Major lineage lacking isolated representative: 0.4 Gammaproteobacteria Micrarchaeota Diapherotrites Eukaryotes Nanohaloarchaeota Aenigmarchaeota Loki. Parvarchaeota Thor. Korarch. DPANN Crenarch. Pacearchaeota Bathyarc. Nanoarchaeota YNPFFA Woesearchaeota Aigarch. Opisthokonta Altiarchaeales Halobacteria Z7ME43 Methanopyri TACK Methanococci Excavata Archaea Hadesarchaea Thermococci Thaumarchaeota Archaeplastida Methanobacteria Thermoplasmata Chromalveolata Archaeoglobi Methanomicrobia Amoebozoa Figure 1 | A current view of the tree of life, encompassing the total diversity represented by sequenced genomes. The tree includes 92 named bacterial phyla, 26