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

Journal Article · · The ISME Journal
 [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)

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1377559
Journal Information:
The ISME Journal, Vol. 10, Issue 11; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 65 works
Citation information provided by
Web of Science

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Cited By (22)

Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments journal March 2017
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea journal August 2017
Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments journal November 2018
The distinction of CPR bacteria from other bacteria based on protein family content journal September 2019
Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche journal April 2019
Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism journal April 2019
Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium journal August 2019
Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities journal September 2017
A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments journal September 2018
Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria journal February 2017
Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota journal February 2018
Functional shifts in microbial mats recapitulate early Earth metabolic transitions journal October 2018
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal September 2018
Carbon Fixation by Marine Ultrasmall Prokaryotes journal March 2019
Isotope discrimination by form IC RubisCO from Ralstonia eutropha and Rhodobacter sphaeroides , metabolically versatile members of ‘ Proteobacteria ’ from aquatic and soil habitats: Isotope discrimination by form IC RubisCO journal November 2018
Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO 2 concentrating mechanisms journal January 2020
The Prodigal Compound: Return of Ribosyl 1,5-Bisphosphate as an Important Player in Metabolism journal December 2018
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation journal June 2020
Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche text January 2019
Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea journal July 2018
Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation journal January 2017
RNA-Dependent Cysteine Biosynthesis in Bacteria and Archaea journal May 2017