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Unusual biology across a group comprising more than 15% of domain Bacteria
Open accessAbstract
A prominent feature of the bacterial domain is a radiation of major lineages that are defined as candidate phyla because they lack isolated representatives. Bacteria from these phyla occur in diverse environments and are thought to mediate carbon and hydrogen cycles. Genomic analyses of a few representatives suggested that metabolic limitations have prevented their cultivation. Here we reconstructed 8 complete and 789 draft genomes from bacteria representing >35 phyla and documented features that consistently distinguish these organisms from other bacteria. We infer that this group, which may comprise >15% of the bacterial domain, has shared evolutionary history, and describe it as the candidate phyla radiation (CPR). All CPR genomes are small and most lack numerous biosynthetic pathways. Owing to divergent 16S ribosomal RNA (rRNA) gene sequences, 50-100% of organisms sampled from specific phyla would evade detection in typical cultivation-independent surveys. CPR organisms often have self-splicing introns and proteins encoded within their rRNA genes, a feature rarely reported in bacteria. Furthermore, they have unusual ribosome compositions. All are missing a ribosomal protein often absent in symbionts, and specific lineages are missing ribosomal proteins and biogenesis factors considered universal in bacteria. This implies different ribosome structures and biogenesis mechanisms, and underlines unusual biology across a large part of the bacterial domain.
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“Trees visualized at https://itol.embl.de/itol.cgiusing Netwick files from Hug et al. (2016) concatenated ribosomal proteins in place of 16S rRNA genes (Fig. 3B) indicate that a large radiation of predominantly uncultured mesophilic taxa, which are comprised of potentially symbiotic organisms with small cells and genomes and are referred to as the bacterial candidate phyla radiation (CPR) and the”
From The Emergence of Life (2019) · cites this paper as Brown et al. 2015
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Poorly known microbial taxa dominate the microbiome of permafrost thaw ponds
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“In all the pond stages, both the universal and the bacterial markers identified members of candidate phylum Omnitrophica (candidate division OP3) and taxa from the ‘candidate phyla radiation’ (CPR, Brown et al., 2015), in particular Parcubacteria (candidate division OD1) as dominant taxa.”
BackgroundProtein engineering: Beating the odds.
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Molecular Ecology of Hypersaline Microbial Mats: Current Insights and New Directions
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“This group has successfully reconstructed complete genomes of Parcubacteria (OD1), Microgenomates (OP11), Saccharibacteria (TM7), Berkelbacteria (ACD58) and the Kazan phyla, expanding genomic information in the bacteria domain [62].”
BackgroundInfluentialTen Years of Collaborative Progress in the Quest for Orthologs
Linard, B., Ebersberger, I., McGlynn, S. E., Glover, N., Mochizuki, T., Patricio, M., Lecompte, O., Nevers, Y., Thomas, P. D., Gabaldón, T., et al. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab098 · Cited by 45
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The endolithic bacterial diversity of shallow bedrock ecosystems.
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Comparative genomics of the DNA damage‐inducible network in the Patescibacteria
Sánchez-Osuna, M., Barbé, J., & Erill, I. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13826 · Cited by 44
Evaluating de Novo Assembly and Binning Strategies for Time Series Drinking Water Metagenomes
Vosloo, S., Huo, L.-X., Anderson, C. L., Dai, Z.-H., Sevillano, M., & Pinto, A. (2021) · bioRxiv · doi:10.1128/spectrum.01434-21 · Cited by 43
An evolutionary path to altered cofactor specificity in a metalloenzyme
Barwinska‐Sendra, A., Garcia, Y. M., Sendra, K. M., Baslé, A., Mackenzie, E. S., Tarrant, E., Card, P., Tabares, L. C., Bicep, C., Un, S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16478-0 · Cited by 51
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Searching for Life on Mars Before It Is Too Late
Fairén, A. G., Parro, V., Schulze‐Makuch, D., & Whyte, L. G. (2017) · Astrobiology · doi:10.1089/ast.2017.1703 · Cited by 59
“As an analog to Earth investigations, hundreds of new types of microorganisms were recently found in understudied terrestrial environments and they ended up comprising more than 15% of all known groups of Bacteria and nine new groups of Archaea, representing tens of new phyla about which very little was previously kno…”
BackgroundUnveiling microbial interactions in stratified mat communities from a warm saline shallow pond
Saghai, A., Gutiérrez-Preciado, A., Deschamps, P., Moreira, D., Bertolino, P., Ragon, M., & López-García, P. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13754 · Cited by 43
“Aminice- nantes is one of the bacterial candidate divisions harboring members with small genomes, suggesting that they are involved in symbiotic relationships (e.g., parasitism, syntro- phy) with others organisms (Kantor et al., 2013; Rinke et al., 2013; Wrighton et al., 2014; Brown et al., 2015).”
BackgroundTuraev, D., & Rattei, T. (2016) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2016.04.011 · Cited by 35
Microbial Nitrogen Metabolism in Chloraminated Drinking Water Reservoirs
Potgieter, S., Dai, Z.-H., Venter, S., Sigudu, M., & Pinto, A. (2019) · Msphere · doi:10.1128/msphere.00274-20 · Cited by 42
“…Marker gene based taxonomic and phylogenetic analysis Small subunit (SSU) rRNA gene sequences were identified using a Hidden Markov Model (HMM) search using the Infernal package (Nawrocki et al., 2009) with domain specific covariance models and corrected as outlined previously (Brown et al., 2015).”
MethodTaubert, M., Stähly, J., Kolb, S., & Küsel, K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0212937 · Cited by 42
A metagenomic perspective on the microbial prokaryotic genome census
Wu, D., Seshadri, R., Kyrpides, N. C., & Ivanova, N. (2025) · Science Advances · doi:10.1126/sciadv.adq2166 · Cited by 43
Heme auxotrophy in abundant aquatic microbial lineages
Kim, S., Kang, I., Lee, J.-W., Jeon, C., Giovannoni, S., & Cho, J.-C. (2021) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1101/2021.01.11.426183 · Cited by 41
Metabolic relationships of uncultured bacteria associated with the microalgae Gambierdiscus
Rambo, I. M., Dombrowski, N., Constant, L., Erdner, D. L., & Baker, B. J. (2019) · Environmental Microbiology · doi:10.1111/1462-2920.14878 · Cited by 47
To Dereplicate or Not To Dereplicate?
Evans, J. T., & Denef, V. J. (2020) · mSphere · doi:10.1128/msphere.00971-19 · Cited by 48
“While initially, the reconstruction of MAGs was only achievable in lower-diversity or highly uneven communities (1), in the past five years reports on the reconstruction of hundreds to thousands of MAGs have become routine (2-5).”
BackgroundChen, L.-X., Al-Shayeb, B., Méheust, R., Li, W.-J., Doudna, J., & Banfield, J. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00928 · Cited by 40
Self-citationDahlhausen, K. E., Doroud, L., Firl, A. J., Polkinghorne, A., & Eisen, J. A. (2018) · PeerJ · doi:10.7717/peerj.4452 · Cited by 56
“456 457 Potential confounding variables that may have influenced our results are sample storage [42], 458 DNA extraction method [43], PCR [44][45], and sequencing [46].”
BackgroundInfluentialZhang, W., Ding, W., Yang, B., Tian, R., Gu, S., Luo, H., & Qian, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01825 · Cited by 40
Exploring the global vaginal microbiome and its impact on human health
Chacra, L. A., & Fenollar, F. (2021) · Microbial Pathogenesis · doi:10.1016/j.micpath.2021.105172 · Cited by 47
Saccharibacteria as Organic Carbon Sinks in Hydrocarbon-Fueled Communities
Figueroa-Gonzalez, P. A., Bornemann, T., Adam, P., Plewka, J., Révész, F., von Hagen, C. A., Táncsics, A., & Probst, A. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.587782 · Cited by 39
“Saccharibacteria belong to the so-called CPR, a phylogenetic cluster of bacteria that comprises about 25% of this domain (Brown et al., 2015; Hug et al., 2016) and contains at least 73 phyla (Bor et al.”
BackgroundDeeg, C. M., Zimmer, M., George, E. E., Husník, F., Keeling, P., & Suttle, C. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007801 · Cited by 39
Narrowe, A. B., Spang, A., Stairs, C. W., Caceres, E., Baker, B. J., Miller, C. S., & Ettema, T. J. G. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy154 · Cited by 42
Erives, A. J. (2017) · Epigenetics & Chromatin · doi:10.1186/s13072-017-0162-0 · Cited by 66
“Conclusions There has been some speculation that new domains of life may be discovered in the era of massive genomic sequencing and analysis [41], but so far this has been mainly served to expand the number of known bacterial phyla [42].”
Resilience of the prokaryotic microbial community of Acropora digitifera to elevated temperature
Gajigan, A. P., Diaz, L. A., & Conaco, C. (2017) · MicrobiologyOpen · doi:10.1002/mbo3.478 · Cited by 40
“In addition to the primer coverage limitation, this primer set results in underrepresentation of the SAR11 clade (Apprill, McNally, Parsons, & Weber, 2015) and Thaumarchaeota (Parada, Needham, & Fuhrman, 2016) and limits detection of phyla under candidate phyla radiation (CPR) (Brown et al., 2015).”
BackgroundAguilar, P., Acosta, E., Dorador, C., & Sommaruga, R. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00976 · Cited by 43
“Further, it is important to highlight the presence in all samples of different OTUs considered part of the recently described candidate phyla radiation (CPR, e.g., OD1, OP11, SR1, and TM7; Brown et al., 2015) and also others described as microbial dark matter (e.g., OP3 and TM6; Rinke et al., 2013).”
BackgroundDefining eukaryotes to dissect eukaryogenesis
Donoghue, P. C. J., Kay, C., Spang, A., Szöllősi, G. J., Nenarokova, A., Moody, E. R. R., Pisani, D., & Williams, T. A. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.048 · Cited by 46
Critical assessment of pan-genomic analysis of metagenome-assembled genomes
Li, T., & Yin, Y. (2022) · Briefings in Bioinformatics · doi:10.1093/bib/bbac413 · Cited by 45
“The term ‘MAG’ first appeared in the literature in 2015 [22, 23], when the first large-scale MAG study was published [24].”
BackgroundJaffe, A. L., Thomas, A. D., He, C., Keren, R., Valentin-Alvarado, L. E., Munk, P., Bouma‐Gregson, K., Farag, I., Amano, Y., Sachdeva, R., et al. (2021) · mBio · doi:10.1128/mbio.00521-21 · Cited by 50
“We then computed contamination and completeness for the genome set using a set of 43 marker genes sensitive to described lineage-specific losses in the CPR bacteria (31, 33) using the custom workflow in CheckM (102).”
MethodResultSelf-citationSchulze-Makuch, D., Lipus, D., Arens, F., Baqué, M., Bornemann, T., de Vera, J. D., Flury, M., Frösler, J., Heinz, J., Hwang, Y., et al. (2021) · Microorganisms · doi:10.3390/microorganisms9051038 · Cited by 38
“Binned genomes were manually curated using taxonomy, GC content, and coverage of scaffolds prior to scaffolding error correction using ra2 [60] and an additional manual curation iteration.”
MethodAtribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor
Vuillemin, A., Vargas, S., Coskun, Ö. K., Pockalny, R. A., Murray, R. W., Smith, D. C., D'Hondt, S. L., & Orsi, W. D. (2020) · mBio · doi:10.1128/mbio.01937-20 · Cited by 43
Metabolic network percolation quantifies biosynthetic capabilities across the human oral microbiome
Bernstein, D. B., Dewhirst, F. E., & Segrè, D. (2019) · eLife · doi:10.7554/elife.39733 · Cited by 44
“…community structure is highlighted by the recent identification of the candidate phyla radiation – a large branch of the tree of life consisting mainly of uncultivated organisms with small genomes and unique metabolic properties ( Kantor et al., 2013 ; Brown et al., 2015 ; Hug et al., 2016 ).”
BackgroundSavio, D., Stadler, P., Reischer, G., Demeter, K., Linke, R., Blaschke, A. P., Mach, R., Kirschner, A., Stadler, H., & Farnleitner, A. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00028 · Cited by 38
“The available information on their physiology based on these metagenomic and single cell sequencing studies suggests generally small genomes with severely reduced metabolic capabilities as well as a potential ectosymbiotic or parasitic lifestyle (Kantor et al., 2013; Rinke et al., 2013; Wrighton et al., 2014; Brown et…”
BackgroundIn it for the long haul: evolutionary consequences of persistent endosymbiosis.
Wernegreen, J. J. (2017) · Current Opinion in Genetics and Development · doi:10.1016/j.gde.2017.08.006 · Cited by 38
“in certain members of Prochlorococcus [31], as well as very old bacterial lineages in which small genome size is likely ancestral [32].”
BackgroundEditorial: Virus Discovery by Metagenomics: The (Im)possibilities
Dutilh, B., Reyes, A., Hall, R. J., & Whiteson, K. L. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01710 · Cited by 38
“Second, this reflects the diversity in the microbial world itself that includes giant viruses (Halary et al., 2016), tiny bacteria (Brown et al., 2015), and everything in between.”
BackgroundReis, M., Dias, M. F., Costa, P., Ávila, M. P., Leite, L. R., de Araújo, F. M. G., Salim, A., Bucciarelli-Rodriguez, M., Oliveira, G., Chartone-Souza, E., et al. (2016) · Chemosphere · doi:10.1016/j.chemosphere.2016.06.097 · Cited by 38
Wehbi, S., Wheeler, A. L., Morel, B., Manepalli, N., Minh, B. Q., LAURETTA, D. S., & Masel, J. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2410311121 · Cited by 36
“C and H are the most frequently used amino acids for binding iron, zinc, copper, and molybdenum, and H, aspartic acid (D) and glutamic acid (E or Glu) for binding manganese and cobalt [Fig.”
Gios, E., Mosley, O. E., Weaver, L., Close, M. E., Daughney, C., & Handley, K. M. (2023) · ISME Communications · doi:10.1038/s43705-023-00223-x · Cited by 41
“The vast majority of these auxotrophies, and involvement in symbiotic or parasitic relationships, are predictions [6, 9].”
BackgroundResultInfluentialFast and persistent responses of alpine permafrost microbial communities to in situ warming
Perez-Mon, C., Stierli, B., Plötze, M. L., & Frey, B. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.150720 · Cited by 49
Single-virus genomics and beyond
Martínez, J. M., Martinez‐Hernández, F., & Martínez‐García, M. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00444-0 · Cited by 46
Metagenomics Strain Resolution on Assembly GraphsPreprint
Quince, C., Nurk, S., Raguideau, S., James, R., Soyer, O. S., Summers, J., Limasset, A., Eren, A., Chikhi, R., & Darling, A. E. (2020) · bioRxiv · doi:10.1101/2020.09.06.284828 · Cited by 37
“…to be extracted de novo from metagenomes, and are becoming crucial for studying unculturable organisms, contributing to many exciting discoveries, such as the description of the Candidate Phyla Radiation [9] or an improved understanding of the diversity of nitrogen fixers in the open ocean [14].”
BackgroundA method for achieving complete microbial genomes and improving bins from metagenomics data
Lui, L., Nielsen, T., & Arkin, A. (2020) · bioRxiv · doi:10.1371/journal.pcbi.1008972 · Cited by 37
“During this process we found that many of the 16S included large introns with 300 LAGLIDADG homing endonucleases, an observation that has been noted in other CPR studies 301 [17].”
MethodThe generality of Constructive Neutral Evolution
Brunet, T. D. P., & Doolittle, W. F. (2018) · Biology & Philosophy · doi:10.1007/s10539-018-9614-6 · Cited by 69
Lesaulnier, C., Herbold, C. W., Pelikan, C., Berry, D., Gérard, C., Coz, X. L., Gagnot, S., Niggemann, J., Dittmar, T., Singer, G. A., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0344-9 · Cited by 55
“Early after bottling, Water 2 had higher phylum/class/family-‐level diversities than Water 1, 381 with considerable representation of 16S rRNA genes from the Alpha-‐, and Gammaproteobacteria, 382 Bacteroidetes, Elusimicrobia, and the candidate phyla radiation lineage OD1 (Parcubacteria) (Figure 1) [50].”
Stolz, J. F. (2016) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiw247 · Cited by 71
“Similarly, they have usedmetagenomics to explore diversity in CP revealing evidence that theymay actually represent greater than 15%of bacterial diversity (Brown et al. 2015) or even a separate lineage known as the candidate phyla radiation (Hug et al. 2016).”
BackgroundDelafont, V., Samba‐Louaka, A., Bouchon, D., Moulin, L., & Héchard, Y. (2015) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12343 · Cited by 44
Suzuki, S., Nealson, K. H., & Ishii, S. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.03141 · Cited by 36
Sereika, M., Kirkegaard, R., Karst, S., Michaelsen, T., Sørensen, E. A., Wollenberg, R., & Albertsen, M. (2021) · bioRxiv · doi:10.1101/2021.10.27.466057 · Cited by 36
“However, 65 they rely heavily on good reference databases and assumptions about universal essential single copy 66 genes that are known not to be truly universal (19, 20).”
BackgroundLemos, L., Manoharan, L., Mendes, L., Venturini, A., Pylro, V., & Tsai, S. (2020) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12880 · Cited by 36
Baricz, A., Chiriac, M., Andrei, A., Bulzu, P., Levei, E. A., Cadar, O., Battes, K. P., Cîmpean, M., Șenilă, M., Cristea, A., et al. (2020) · Environmental Microbiology · doi:10.1111/1462-2920.14909 · Cited by 41
“CPR bacteria have small genome size (often < 1 Mb) and exhibit multiple metabolic limitations, such as partial tricarboxylic acid cycle, lack of electron transport chain complexes, incomplete biosynthetic pathways for nucleotides and amino acids (Brown et al., 2015).”
BackgroundInfluentialXie, F., Zhao, S., Zhan, X., Zhou, Y., Li, Y., Zhu, W., Pope, P. B., Attwood, G. T., Jin, W., & Mao, S. (2024) · Genome biology · doi:10.1186/s13059-024-03167-0 · Cited by 43
“A set of 26 ribosomal proteins [35, 113] and 118 archaeal marker proteins [36] were downloaded from the Pfam [114] (v.35.0) and TIGRFAM [115] (v.15.0) databases according to previous studies that covered a wide range of bacterial and archaeal diver - sity.”
MethodInfluential
Metadata
- Authors
- Brown, C. T., Hug, L. A., Thomas, B. C., Sharon, I., Castelle, C. J., Singh, A., Wilkins, M. J., Wrighton, K. C., Williams, K. H., & Banfield, J. F.
- Affiliations
- University of California, Berkeley (US)
- The Ohio State University (US)
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Banfield, Jillian F.
- ORCID
- Venue
- Nature
- Published
- 2015-06-15
- Volume
- 523
- Issue
- 7559
- Pages
- 208-211
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1528357204
- Cited by
- 1,216
- References
- 63
- Citations by year
- 2026: 56 · 2025: 100 · 2024: 95 · 2023: 125 · 2022: 108 · 2021: 120 · 2020: 144 · 2019: 121 · 2018: 116 · 2017: 104 · 2016: 101 · 2015: 26
- FWCI
- 50.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.osti.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Energy (DESC0004918, DE AC02 05CH11231)
- Joint Genome Institute
- Office of Science
- Biological and Environmental Research
- Pacific Northwest National Laboratory
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Candidate Phyla Radiation, uncultured bacteria, bacterial evolution, ribosome composition, ribosome biogenesis, self-splicing introns, small genomes, groundwater bacteria, metagenome-assembled genomes, symbionts
- MeSH terms
- Bacteria, Environmental Microbiology, Introns, Phylogeny, Ribosomal Proteins, RNA, Ribosomal, 16S, Genome, Bacterial
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