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Title: RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria

Abstract

Metagenomic studies recently uncovered form II/III RubisCO genes, originally thought to only occur in archaea, from uncultivated bacteria of the candidate phyla radiation (CPR). There are no isolated CPR bacteria and these organisms are predicted to have limited metabolic capacities. Here we expand the known diversity of RubisCO from CPR lineages. We report a form of RubisCO, distantly similar to the archaeal form III RubisCO, in some CPR bacteria from the Parcubacteria (OD1), WS6 and Microgenomates (OP11) phyla. In addition, we significantly expand the Peregrinibacteria (PER) II/III RubisCO diversity and report the first II/III RubisCO sequences from the Microgenomates and WS6 phyla. To provide a metabolic context for these RubisCOs, we reconstructed near-complete ( > 93%) PER genomes and the first closed genome for a WS6 bacterium, for which we propose the phylum name Dojkabacteria. Genomic and bioinformatic analyses suggest that the CPR RubisCOs function in a nucleoside pathway similar to that proposed in Archaea. Detection of form II/III RubisCO and nucleoside metabolism gene transcripts from a PER supports the operation of this pathway in situ. We demonstrate that the PER form II/III RubisCO is catalytically active, fixing CO 2 to physiologically complement phototrophic growth in a bacterial photoautotrophic RubisCOmore » deletion strain. We propose that the identification of these RubisCOs across a radiation of obligately fermentative, small-celled organisms hints at a widespread, simple metabolic platform in which ribose may be a prominent currency.« less

Authors:
 [1];  [2];  [1];  [1];  [2];  [1];  [2];  [2];  [3];  [1];  [2]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1377559
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wrighton, Kelly C., Castelle, Cindy J., Varaljay, Vanessa A., Satagopan, Sriram, Brown, Christopher T., Wilkins, Michael J., Thomas, Brian C., Sharon, Itai, Williams, Kenneth H., Tabita, F. Robert, and Banfield, Jillian F. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. United States: N. p., 2016. Web. doi:10.1038/ismej.2016.53.
Wrighton, Kelly C., Castelle, Cindy J., Varaljay, Vanessa A., Satagopan, Sriram, Brown, Christopher T., Wilkins, Michael J., Thomas, Brian C., Sharon, Itai, Williams, Kenneth H., Tabita, F. Robert, & Banfield, Jillian F. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. United States. doi:10.1038/ismej.2016.53.
Wrighton, Kelly C., Castelle, Cindy J., Varaljay, Vanessa A., Satagopan, Sriram, Brown, Christopher T., Wilkins, Michael J., Thomas, Brian C., Sharon, Itai, Williams, Kenneth H., Tabita, F. Robert, and Banfield, Jillian F. Tue . "RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria". United States. doi:10.1038/ismej.2016.53. https://www.osti.gov/servlets/purl/1377559.
@article{osti_1377559,
title = {RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria},
author = {Wrighton, Kelly C. and Castelle, Cindy J. and Varaljay, Vanessa A. and Satagopan, Sriram and Brown, Christopher T. and Wilkins, Michael J. and Thomas, Brian C. and Sharon, Itai and Williams, Kenneth H. and Tabita, F. Robert and Banfield, Jillian F.},
abstractNote = {Metagenomic studies recently uncovered form II/III RubisCO genes, originally thought to only occur in archaea, from uncultivated bacteria of the candidate phyla radiation (CPR). There are no isolated CPR bacteria and these organisms are predicted to have limited metabolic capacities. Here we expand the known diversity of RubisCO from CPR lineages. We report a form of RubisCO, distantly similar to the archaeal form III RubisCO, in some CPR bacteria from the Parcubacteria (OD1), WS6 and Microgenomates (OP11) phyla. In addition, we significantly expand the Peregrinibacteria (PER) II/III RubisCO diversity and report the first II/III RubisCO sequences from the Microgenomates and WS6 phyla. To provide a metabolic context for these RubisCOs, we reconstructed near-complete ( > 93%) PER genomes and the first closed genome for a WS6 bacterium, for which we propose the phylum name Dojkabacteria. Genomic and bioinformatic analyses suggest that the CPR RubisCOs function in a nucleoside pathway similar to that proposed in Archaea. Detection of form II/III RubisCO and nucleoside metabolism gene transcripts from a PER supports the operation of this pathway in situ. We demonstrate that the PER form II/III RubisCO is catalytically active, fixing CO2 to physiologically complement phototrophic growth in a bacterial photoautotrophic RubisCO deletion strain. We propose that the identification of these RubisCOs across a radiation of obligately fermentative, small-celled organisms hints at a widespread, simple metabolic platform in which ribose may be a prominent currency.},
doi = {10.1038/ismej.2016.53},
journal = {The ISME Journal},
number = 11,
volume = 10,
place = {United States},
year = {Tue May 03 00:00:00 EDT 2016},
month = {Tue May 03 00:00:00 EDT 2016}
}

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Cited by: 14 works
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Works referenced in this record:

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