Phylogeny and physiology of candidate phylum 'Atribacteria' (OP9/JS1) inferred from cultivation-independent genomics

Masaru K. Nobu, Jeremy A. Dodsworth, Senthil K. Murugapiran, Christian Rinke, Esther A. Gies, Gordon Webster, Patrick Schwientek, Peter Kille, R. John Parkes, Henrik Sass, Bo B. Jørgensen, Andrew J. Weightman, Wen Tso Liu, Steven J. Hallam, George Tsiamis, Tanja Woyke, Brian P. Hedlund

Research output: Contribution to journalArticlepeer-review

85 Scopus citations

Abstract

The 'Atribacteria' is a candidate phylum in the Bacteria recently proposed to include members of the OP9 and JS1 lineages. OP9 and JS1 are globally distributed, and in some cases abundant, in anaerobic marine sediments, geothermal environments, anaerobic digesters and reactors and petroleum reservoirs. However, the monophyly of OP9 and JS1 has been questioned and their physiology and ecology remain largely enigmatic due to a lack of cultivated representatives. Here cultivation-independent genomic approaches were used to provide a first comprehensive view of the phylogeny, conserved genomic features and metabolic potential of members of this ubiquitous candidate phylum. Previously available and heretofore unpublished OP9 and JS1 single-cell genomic data sets were used as recruitment platforms for the reconstruction of atribacterial metagenome bins from a terephthalate-degrading reactor biofilm and from the monimolimnion of meromictic Sakinaw Lake. The single-cell genomes and metagenome bins together comprise six species- to genus-level groups that represent most major lineages within OP9 and JS1. Phylogenomic analyses of these combined data sets confirmed the monophyly of the 'Atribacteria' inclusive of OP9 and JS1. Additional conserved features within the 'Atribacteria' were identified, including a gene cluster encoding putative bacterial microcompartments that may be involved in aldehyde and sugar metabolism, energy conservation and carbon storage. Comparative analysis of the metabolic potential inferred from these data sets revealed that members of the 'Atribacteria' are likely to be heterotrophic anaerobes that lack respiratory capacity, with some lineages predicted to specialize in either primary fermentation of carbohydrates or secondary fermentation of organic acids, such as propionate.

Original languageEnglish (US)
Pages (from-to)273-286
Number of pages14
JournalISME Journal
Volume10
Issue number2
DOIs
StatePublished - Feb 1 2016

Bibliographical note

Funding Information:
We thank Lars Schreiber, Karen Lloyd, Ramunas Stepa-nauskas and the Single Cell Genomics Center at the Bigelow Laboratory for Ocean Sciences for single-cell sorting and providing access to the Aarhus SAGs. This research is supported by NASA Exobiology grant EXO-NNX11AR78G to BPH and JAD; US National Science Foundation grants MCB 0546865 and OISE 0968421 to BPH; US Department of Energy (DOE) grants DE-EE-0000716 and DE-SC0006771 to BPH; the Nevada Renewable Energy Consortium, funded by the DOE, to BPH; an Amazon Web Services Education Research Grant award to BPH and SKM; Natural Environment Research Council, UK grant NE/J011177/1 to AJW, PK, RJP and HS; Cardiff University Research Leave Fellowship to AJW; Tula Foundation, Natural Sciences and Engineering Research Council (NSERC) of Canada, Canada Foundation for Innovation (CFI) and the Canadian Institute for Advanced Research (CIFAR) through grants awarded to SJH; a 4-year fellowship from the University of British Columbia awarded to EAG. Sampling and sorting of the Aarhus Bay SAGs was funded by the Danish National Research Foundation given to the Center for Geomicro-biology, Aarhus University and their sequencing funded by NERC NBAF awards 628 and 744 to AJW. The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported under Contract No. DE-AC02-05CH11231. BPH acknowledges the generous support of Greg Fullmer through the UNLV Foundation.

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