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

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.

doi:10.1038/ismej.2016.53

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

Journal Article · Tue May 03 00:00:00 EDT 2016 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2016.53· OSTI ID:1377559

Wrighton, Kelly C. ^[1]; Castelle, Cindy J. ^[2]; Varaljay, Vanessa A. ^[1]; Satagopan, Sriram ^[1]; Brown, Christopher T. ^[2]; Wilkins, Michael J. ^[1]; Thomas, Brian C. ^[2]; Sharon, Itai ^[2]; Williams, Kenneth H. ^[3]; Tabita, F. Robert ^[1]; Banfield, Jillian F. ^[2]

The Ohio State Univ., Columbus, OH (United States)
Univ. of California, Berkeley, CA (United States)
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.

View Accepted Manuscript (DOE)

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, Journal Name: The ISME Journal Journal Issue: 11 Vol. 10; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism Ormerod, John G.; Ormerod, Kari S.; Gest, Howard Archives of Biochemistry and Biophysics, Vol. 94, Issue 3 https://doi.org/10.1016/0003-9861(61)90073-x	journal	September 1961
“Candidatus Sonnebornia yantaiensis”, a member of candidate division OD1, as intracellular bacteria of the ciliated protist Paramecium bursaria (Ciliophora, Oligohymenophorea) Gong, Jun; Qing, Yao; Guo, Xiaohong Systematic and Applied Microbiology, Vol. 37, Issue 1 https://doi.org/10.1016/j.syapm.2013.08.007	journal	February 2014
Classifying the uncultivated microbial majority: A place for metagenomic data in the Candidatus proposal Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon Systematic and Applied Microbiology, Vol. 38, Issue 4 https://doi.org/10.1016/j.syapm.2015.01.001	journal	June 2015
On the Origin of Heterotrophy Schönheit, Peter; Buckel, Wolfgang; Martin, William F. Trends in Microbiology, Vol. 24, Issue 1 https://doi.org/10.1016/j.tim.2015.10.003	journal	January 2016
Positive and Negative Selection of Mutant Forms of Prokaryotic (Cyanobacterial) Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Smith, Stephanie A.; Tabita, F. Robert Journal of Molecular Biology, Vol. 331, Issue 3 https://doi.org/10.1016/s0022-2836(03)00786-1	journal	August 2003
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
A Rubisco Mutant That Confers Growth under a Normally “Inhibitory” Oxygen Concentration Satagopan, Sriram; Scott, Stephanie S.; Smith, Todd G. Biochemistry, Vol. 48, Issue 38 https://doi.org/10.1021/bi9006385	journal	September 2009
Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J. The ISME Journal, Vol. 8, Issue 7 https://doi.org/10.1038/ismej.2013.249	journal	March 2014
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
A pentose bisphosphate pathway for nucleoside degradation in Archaea Aono, Riku; Sato, Takaaki; Imanaka, Tadayuki Nature Chemical Biology, Vol. 11, Issue 5 https://doi.org/10.1038/nchembio.1786	journal	March 2015
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3120	journal	August 2013
Diverse uncultivated ultra-small bacterial cells in groundwater Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7372	journal	February 2015
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Deep-sea striving Walker, Alan Nature Reviews Microbiology, Vol. 11, Issue 6 https://doi.org/10.1038/nrmicro3037	journal	May 2013
Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria McKinlay, J. B.; Harwood, C. S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 26 https://doi.org/10.1073/pnas.1006175107	journal	June 2010
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
Substitutions at Methionine 295 of Archaeoglobus fulgidus Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Affect Oxygen Binding and CO ₂ /O ₂ Specificity Kreel, Nathaniel E.; Tabita, F. Robert Journal of Biological Chemistry, Vol. 282, Issue 2 https://doi.org/10.1074/jbc.m609399200	journal	October 2006
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
UniRef: comprehensive and non-redundant UniProt reference clusters Suzek, B. E.; Huang, H.; McGarvey, P. Bioinformatics, Vol. 23, Issue 10 https://doi.org/10.1093/bioinformatics/btm098	journal	March 2007
Infernal 1.0: inference of RNA alignments Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Bioinformatics, Vol. 25, Issue 10 https://doi.org/10.1093/bioinformatics/btp157	journal	March 2009
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO Ashida, H.; Saito, Y.; Nakano, T. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern104	journal	June 2007
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
KEGG for integration and interpretation of large-scale molecular data sets Kanehisa, M.; Goto, S.; Sato, Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr988	journal	November 2011
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Archaeal Type III RuBisCOs Function in a Pathway for AMP Metabolism Sato, T.; Atomi, H.; Imanaka, T. Science, Vol. 315, Issue 5814 https://doi.org/10.1126/science.1135999	journal	February 2007
Expanding the Known Diversity and Environmental Distribution of an Uncultured Phylogenetic Division of Bacteria Dojka, M. A.; Harris, J. K.; Pace, N. R. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/aem.66.4.1617-1621.2000	journal	April 2000
Complementation analysis and regulation of CO2 fixation gene expression in a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum. Falcone, D. L.; Tabita, F. R. Journal of Bacteriology, Vol. 175, Issue 16 https://doi.org/10.1128/jb.175.16.5066-5077.1993	journal	August 1993
Interactive Control of Rhodobacter capsulatus Redox-Balancing Systems during Phototrophic Metabolism Tichi, M. A.; Tabita, F. R. Journal of Bacteriology, Vol. 183, Issue 21 https://doi.org/10.1128/jb.183.21.6344-6354.2001	journal	November 2001
Synthesis of Catalytically Active Form III Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase in Archaea Finn, M. W.; Tabita, F. R. Journal of Bacteriology, Vol. 185, Issue 10 https://doi.org/10.1128/jb.185.10.3049-3059.2003	journal	May 2003
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling Hug, Laura A.; Castelle, Cindy J.; Wrighton, Kelly C. Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/2049-2618-1-22	journal	January 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
Basic Local Alignment Search Tool Altschul, S. Journal of Molecular Biology, Vol. 215, Issue 3 https://doi.org/10.1006/jmbi.1990.9999	journal	October 1990
Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism Ormerod, John G.; Ormerod, Kari S.; Gest, Howard Archives of Biochemistry and Biophysics, Vol. 94, Issue 3 https://doi.org/10.1016/0003-9861(61)90073-X	journal	September 1961
Positive and Negative Selection of Mutant Forms of Prokaryotic (Cyanobacterial) Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Smith, Stephanie A.; Tabita, F. Robert Journal of Molecular Biology, Vol. 331, Issue 3 https://doi.org/10.1016/S0022-2836(03)00786-1	journal	August 2003
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Genomic Expansion of Domain Archaea Highlights Roles for Organisms from New Phyla in Anaerobic Carbon Cycling Castelle, Cindy J.; Wrighton, Kelly C.; Thomas, Brian C. Current Biology, Vol. 25, Issue 6 https://doi.org/10.1016/j.cub.2015.01.014	journal	March 2015
Predominant archaea in marine sediments degrade detrital proteins Lloyd, Karen G.; Schreiber, Lars; Petersen, Dorthe G. Nature, Vol. 496, Issue 7444 https://doi.org/10.1038/nature12033	journal	March 2013
Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula Roggero, Paola; Liotto, Nadia; Pozzi, Chiara Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16582-1	journal	June 2020
A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation Joshi, H. M.; Tabita, F. R. Proceedings of the National Academy of Sciences, Vol. 93, Issue 25 https://doi.org/10.1073/pnas.93.25.14515	journal	December 1996
Substrate-induced Assembly of Methanococcoides burtonii d-Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Dimers into Decamers Alonso, Hernán; Blayney, Michelle J.; Beck, Jennifer L. Journal of Biological Chemistry, Vol. 284, Issue 49 https://doi.org/10.1074/jbc.M109.050989	journal	October 2009
Structure-Function Studies with the Unique Hexameric Form II Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) from Rhodopseudomonas palustris Satagopan, Sriram; Chan, Sum; Perry, L. Jeanne Journal of Biological Chemistry, Vol. 289, Issue 31 https://doi.org/10.1074/jbc.M114.578625	journal	June 2014
Substitutions at Methionine 295 of Archaeoglobus fulgidus Ribulose-1,5-bisphosphate Carboxylase/Oxygenase Affect Oxygen Binding and CO ₂ /O ₂ Specificity Kreel, Nathaniel E.; Tabita, F. Robert Journal of Biological Chemistry, Vol. 282, Issue 2 https://doi.org/10.1074/jbc.M609399200	journal	October 2006
Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater Williams, Kenneth H.; Long, Philip E.; Davis, James A. Geomicrobiology Journal, Vol. 28, Issue 5-6 https://doi.org/10.1080/01490451.2010.520074	journal	June 2011
ProtTest: selection of best-fit models of protein evolution Abascal, F.; Zardoya, R.; Posada, D. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti263	journal	January 2005
Infernal 1.0: inference of RNA alignments Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Bioinformatics, Vol. 25, Issue 13 https://doi.org/10.1093/bioinformatics/btp326	journal	June 2009
Gene and translation initiation site prediction in metagenomic sequences Hyatt, Doug; LoCascio, Philip F.; Hauser, Loren J. Bioinformatics, Vol. 28, Issue 17 https://doi.org/10.1093/bioinformatics/bts429	journal	July 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships Tabita, F. R.; Satagopan, S.; Hanson, T. E. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/erm361	journal	June 2007
Carbon dioxide fixation in ‘Archaeoglobus lithotrophicus’: are there multiple autotrophic pathways?: Autotrophic CO2 fixation in Archaeoglobus Estelmann, Sebastian; Ramos-Vera, Walter Hugo; Gad'on, Nasser FEMS Microbiology Letters, Vol. 319, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02268.x	journal	April 2011
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
Expanding the Known Diversity and Environmental Distribution of an Uncultured Phylogenetic Division of Bacteria Dojka, M. A.; Harris, J. K.; Pace, N. R. Applied and Environmental Microbiology, Vol. 66, Issue 4 https://doi.org/10.1128/AEM.66.4.1617-1621.2000	journal	April 2000
Enzymatic Characterization of AMP Phosphorylase and Ribose-1,5-Bisphosphate Isomerase Functioning in an Archaeal AMP Metabolic Pathway Aono, R.; Sato, T.; Yano, A. Journal of Bacteriology, Vol. 194, Issue 24 https://doi.org/10.1128/JB.01335-12	journal	October 2012
Interactive Control of Rhodobacter capsulatus Redox-Balancing Systems during Phototrophic Metabolism Tichi, M. A.; Tabita, F. R. Journal of Bacteriology, Vol. 183, Issue 21 https://doi.org/10.1128/JB.183.21.6344-6354.2001	journal	November 2001
Synthesis of Catalytically Active Form III Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase in Archaea Finn, M. W.; Tabita, F. R. Journal of Bacteriology, Vol. 185, Issue 10 https://doi.org/10.1128/JB.185.10.3049-3059.2003	journal	May 2003
Modified Pathway To Synthesize Ribulose 1,5-Bisphosphate in Methanogenic Archaea Finn, M. W.; Tabita, F. R. Journal of Bacteriology, Vol. 186, Issue 19 https://doi.org/10.1128/JB.186.19.6360-6366.2004	journal	September 2004
Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs Tabita, F. R.; Hanson, T. E.; Li, H. Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4 https://doi.org/10.1128/MMBR.00015-07	journal	December 2007
Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla Kantor, Rose S.; Wrighton, Kelly C.; Handley, Kim M. mBio, Vol. 4, Issue 5 https://doi.org/10.1128/mBio.00708-13	journal	October 2013
Community-wide analysis of microbial genome sequence signatures Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J. Genome Biology, Vol. 10, Issue 8 https://doi.org/10.1186/gb-2009-10-8-r85	journal	January 2009
Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria Baker, Brett J.; Lazar, Cassandre Sara; Teske, Andreas P. Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0077-6	journal	April 2015

Cited By (23)

Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.39	journal	March 2017
Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 36, Issue 7 https://doi.org/10.1038/nbt0718-660a	journal	July 2018
Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments Dombrowski, Nina; Teske, Andreas P.; Baker, Brett J. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07418-0	journal	November 2018
The distinction of CPR bacteria from other bacteria based on protein family content Méheust, Raphaël; Burstein, David; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12171-z	journal	September 2019
Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation Castelle, Cindy J.; Brown, Christopher T.; Thomas, Brian C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep40101	journal	January 2017
RNA-Dependent Cysteine Biosynthesis in Bacteria and Archaea Mukai, Takahito; Crnković, Ana; Umehara, Takuya mBio, Vol. 8, Issue 3, Article No. e00561-17 https://doi.org/10.1128/mbio.00561-17	journal	May 2017
Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities Danczak, R. E.; Johnston, M. D.; Kenah, C. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0331-1	journal	September 2017
Additional file 2 of Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin Jaffe, Alexander L.; Bardot, Corinne; Le Jeune, Anne-Hélène figshare https://doi.org/10.6084/m9.figshare.22615967.v1	dataset	January 2023
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota Liu, Yang; Zhou, Zhichao; Pan, Jie The ISME Journal, Vol. 12, Issue 4 https://doi.org/10.1038/s41396-018-0060-x	journal	February 2018
Functional shifts in microbial mats recapitulate early Earth metabolic transitions Gutiérrez-Preciado, Ana; Saghaï, Aurélien; Moreira, David Nature Ecology & Evolution, Vol. 2, Issue 11 https://doi.org/10.1038/s41559-018-0683-3	journal	October 2018
Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche Bulzu, Paul-Adrian; Andrei, Adrian-Ştefan; Salcher, Michaela M. Nature Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/s41564-019-0404-y	journal	April 2019
Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism Spang, Anja; Stairs, Courtney W.; Dombrowski, Nina Nature Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/s41564-019-0406-9	journal	April 2019
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium Frolov, Evgenii N.; Kublanov, Ilya V.; Toshchakov, Stepan V. Proceedings of the National Academy of Sciences, Vol. 116, Issue 37 https://doi.org/10.1073/pnas.1904225116	journal	August 2019
Carbon Fixation by Marine Ultrasmall Prokaryotes Lannes, Romain; Olsson-Francis, Karen; Lopez, Philippe Genome Biology and Evolution, Vol. 11, Issue 4 https://doi.org/10.1093/gbe/evz050	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 Thomas, Phaedra J.; Boller, Amanda J.; Satagopan, Sriram Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14423	journal	November 2018
Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO ₂ concentrating mechanisms Iñiguez, Concepción; Capó‐Bauçà, Sebastià; Niinemets, Ülo The Plant Journal, Vol. 101, Issue 4 https://doi.org/10.1111/tpj.14643	journal	January 2020
The Prodigal Compound: Return of Ribosyl 1,5-Bisphosphate as an Important Player in Metabolism Hove-Jensen, Bjarne; Brodersen, Ditlev E.; Manav, M. Cemre Microbiology and Molecular Biology Reviews, Vol. 83, Issue 1 https://doi.org/10.1128/mmbr.00040-18	journal	December 2018
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B. BMC Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12915-020-00804-5	journal	June 2020
A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments Vavourakis, Charlotte D.; Andrei, Adrian-Stefan; Mehrshad, Maliheh Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0548-7	journal	September 2018
Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria Mukai, Takahito; Reynolds, Noah; Crnković, Ana Life, Vol. 7, Issue 1 https://doi.org/10.3390/life7010008	journal	February 2017
Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche Bulzu, Paul-Adrian; Andrei, Adrian-Ştefan; Salcher, Michaela M. Nature Publishing Group https://doi.org/10.5167/uzh-183773	text	January 2019

Similar Records

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla

Journal Article · Sat Dec 31 23:00:00 EST 2011 · Science · OSTI ID:1092314

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla

Journal Article · Thu Sep 27 00:00:00 EDT 2012 · Science, 337(6102):1661-1665 · OSTI ID:1052946

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (63)

Cited By (23)

Similar Records

Related Subjects