Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations

Abstract

Candidate phyla radiation (CPR) bacteria and DPANN (an acronym of the names of the first included phyla) archaea are massive radiations of organisms that are widely distributed across Earth’s environments, yet we know little about them. Initial indications are that they are consistently distinct from essentially all other bacteria and archaea owing to their small cell and genome sizes, limited metabolic capacities and often episymbiotic associations with other bacteria and archaea. In this Analysis, we investigate their biology and variations in metabolic capacities by analysis of approximately 1,000 genomes reconstructed from several metagenomics-based studies. We find that they are not monolithic in terms of metabolism but rather harbour a diversity of capacities consistent with a range of lifestyles and degrees of dependence on other organisms. Notably, however, certain CPR and DPANN groups seem to have exceedingly minimal biosynthetic capacities, whereas others could potentially be free living. Understanding of these microorganisms is important from the perspective of evolutionary studies and because their interactions with other organisms are likely to shape natural microbiome function.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Phylogenetic trees of Bacteria and Archaea.
Fig. 2: The size ranges for CPR and DPANN genomes compared with size ranges for the genomes of known bacterial symbionts as well as other bacteria and archaea.

Adapted from ref.61, Annual Reviews.

Fig. 3: Profile of presence or absence of certain metabolic or biosynthetic capacities.
Fig. 4: Maximum likelihood phylogenetic trees constructed for the catalytic subunits of NiFe hydrogenases and Rubisco.
Fig. 5: Central metabolism of some CPR and DPANN, examples of typical configurations.
Fig. 6: Central metabolism of some CPR and DPANN, examples of exceptions.

Part b adapted from ref.71, Springer Nature Limited. Part d adapted with permission from ref.2, Elsevier.

Fig. 7: Maximum likelihood phylogenetic tree of the catalytic subunit Elp3, which is found in genomes of some CPR bacteria and DPANN archaea.
Fig. 8: Examples of tRNA introns identified in some CPR bacteria genomes.

Change history

  • 04 October 2018

    In the original online version of this manuscript, the ORCID links for Cindy J. Castelle, Karthik Anantharaman, Alexander J. Probst and Jillian F. Banfield were omitted. These have now been added.

References

  1. 1.

    Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    CAS  Google Scholar 

  2. 2.

    Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015).

    CAS  Google Scholar 

  3. 3.

    Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208–211 (2015).

    CAS  Google Scholar 

  4. 4.

    Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).

    CAS  Google Scholar 

  5. 5.

    Anantharaman, K. et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat. Commun. 7, 13219 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661–1665 (2012).

    CAS  Google Scholar 

  7. 7.

    Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).

    CAS  Google Scholar 

  8. 8.

    Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).

    CAS  Google Scholar 

  9. 9.

    Baker, B. J. et al. Lineages of acidophilic archaea revealed by community genomic analysis. Science 314, 1933–1935 (2006).

    CAS  Google Scholar 

  10. 10.

    Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).

    CAS  Google Scholar 

  11. 11.

    Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).

    CAS  Google Scholar 

  12. 12.

    Probst, A. J. et al. Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations. Environ. Microbiol. 19, 459–474 (2017).

    CAS  Google Scholar 

  13. 13.

    Williams, T. A. et al. Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc. Natl Acad. Sci. USA 114, E4602–E4611 (2017).

    CAS  Google Scholar 

  14. 14.

    Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J. 11, 2407–2425 (2017).

    PubMed  PubMed Central  Google Scholar 

  15. 15.

    Aouad, M. et al. Extreme halophilic archaea derive from two distinct methanogen Class II lineages. Mol. Phylogenet. Evol. 127, 46–54 (2018).

    CAS  Google Scholar 

  16. 16.

    Petitjean, C., Deschamps, P., López-García, P. & Moreira, D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204 (2014).

    PubMed  PubMed Central  Google Scholar 

  17. 17.

    Hua, Z.-S. et al. Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. ISME J. 9, 1280–1294 (2015).

    CAS  Google Scholar 

  18. 18.

    Suzuki, S. et al. Microbial diversity in The Cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem. Proc. Natl Acad. Sci. USA 110, 15336–15341 (2013).

    CAS  Google Scholar 

  19. 19.

    Narasingarao, P. et al. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J. 6, 81–93 (2012).

    CAS  Google Scholar 

  20. 20.

    Andrade, K. et al. Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem. ISME J. 9, 2697–2711 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Ortiz-Alvarez, R. & Casamayor, E. O. High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ. Microbiol. Rep. 8, 210–217 (2016).

    CAS  Google Scholar 

  22. 22.

    Linz, A. M. et al. Bacterial community composition and dynamics spanning five years in freshwater bog lakes. mSphere 2, e00169–00117 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Merkley, E. D. et al. Changes in protein expression across laboratory and field experiments in Geobacter bemidjiensis. J. Proteome Res. 14, 1361–1375 (2015).

    CAS  Google Scholar 

  24. 24.

    Ludington, W. B. et al. Assessing biosynthetic potential of agricultural groundwater through metagenomic sequencing: a diverse anammox community dominates nitrate-rich groundwater. PLOS One 12, e0174930 (2017).

    PubMed  PubMed Central  Google Scholar 

  25. 25.

    Lin, X., Kennedy, D., Fredrickson, J., Bjornstad, B. & Konopka, A. Vertical stratification of subsurface microbial community composition across geological formations at the Hanford Site. Environ. Microbiol. 14, 414–425 (2012).

    CAS  Google Scholar 

  26. 26.

    Tully, B. J., Graham, E. D. & Heidelberg, J. F. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci. Data 5, 170203 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Wright, J. J., Konwar, K. M. & Hallam, S. J. Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381–394 (2012).

    CAS  Google Scholar 

  28. 28.

    Li, M. et al. Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat. Commun. 6, 8933 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Dombrowski, N., Seitz, K. W., Teske, A. P. & Baker, B. J. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 5, 106 (2017).

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Schauer, C., Thompson, C. L. & Brune, A. The bacterial community in the gut of the Cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Appl. Environ. Microbiol. 78, 2758–2767 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Biedermann, L. et al. Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLOS One 8, e59260 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Camanocha, A. & Dewhirst, F. E. Host-associated bacterial taxa from Chlorobi, Chloroflexi, GN02, Synergistetes, SR1, TM7, and WPS-2 Phyla/candidate divisions. J. Oral Microbiol. 6, 25468 (2014).

    Google Scholar 

  33. 33.

    Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Koskinen, K. et al. First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. MBio 8, e00824–00817 (2017).

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Bruno, A. et al. Exploring the under-investigated “microbial dark matter” of drinking water treatment plants. Sci. Rep. 7, 44350 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Bautista-de los Santos, Q. M. et al. Emerging investigators series: microbial communities in full-scale drinking water distribution systems — a meta-analysis. Environ. Sci. Water Res. Technol. 2, 631–644 (2016).

    CAS  Google Scholar 

  37. 37.

    Pinto, A. J., Schroeder, J., Lunn, M., Sloan, W. & Raskin, L. Spatial-temporal survey and occupancy-abundance modeling to predict bacterial community dynamics in the drinking water microbiome. MBio 5, e01135–01114 (2014).

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Dewhirst, F. E. et al. The human oral microbiome. J. Bacteriol. 192, 5002–5017 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    He, X. et al. Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle. Proc. Natl Acad. Sci. USA 112, 244–249 (2015).

    CAS  Google Scholar 

  40. 40.

    Ling, Z. et al. Altered fecal microbiota composition associated with food allergy in infants. Appl. Environ. Microbiol. 80, 2546–2554 (2014).

    PubMed  PubMed Central  Google Scholar 

  41. 41.

    Kuehbacher, T. et al. Intestinal TM7 bacterial phylogenies in active inflammatory bowel disease. J. Med. Microbiol. 57, 1569–1576 (2008).

    CAS  Google Scholar 

  42. 42.

    Kowarsky, M. et al. Numerous uncharacterized and highly divergent microbes which colonize humans are revealed by circulating cell-free DNA. Proc. Natl Acad. Sci. USA 114, 9623–9628 (2017).

    CAS  Google Scholar 

  43. 43.

    Dudek, N. K. et al. Novel microbial diversity and functional potential in the marine mammal oral microbiome. Curr. Biol. 27, 3752–3762 (2017).

    CAS  Google Scholar 

  44. 44.

    Golyshina, O. V. et al. ‘ARMAN’ archaea depend on association with euryarchaeal host in culture and in situ. Nat. Commun. 8, 60 (2017).

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Youssef, N. H. et al. Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’. ISME J. 9, 447–460 (2014).

    PubMed  PubMed Central  Google Scholar 

  46. 46.

    Nelson, W. C. & Stegen, J. C. The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle. Front. Microbiol. 6, 713 (2015).

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Kantor, R. S. et al. Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. MBio 4, e00708–e00713 (2013).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Wrighton, K. C. et al. Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. ISME J. 8, 1452–1463 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Campbell, J. H. et al. UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc. Natl Acad. Sci. USA 110, 5540–5545 (2013).

    CAS  Google Scholar 

  50. 50.

    Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533–538 (2013).

    CAS  Google Scholar 

  51. 51.

    Erickson, H. P. & Osawa, M. Cell division without FtsZ — a variety of redundant mechanisms. Mol. Microbiol. 78, 267–270 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Luef, B. et al. Diverse uncultivated ultra-small bacterial cells in groundwater. Nat. Commun. 6, 6372 (2015).

    CAS  Google Scholar 

  53. 53.

    Huber, H., Hohn, M. J., Rachel, R. & Fuchs, T. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. 417, 63–67 (2002).

  54. 54.

    Junglas, B. et al. Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190, 395–408 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Burghardt, T. et al. The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells. Biochem. Soc. Trans. 37, 127–132 (2009).

    CAS  Google Scholar 

  56. 56.

    Wurch, L. et al. ARTICLE Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment. Nat. Commun. 7, 12115 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Comolli, L. R. & Banfield, J. F. Inter-species interconnections in acid mine drainage microbial communities. Front. Microbiol. 5, 367 (2014).

    PubMed  PubMed Central  Google Scholar 

  58. 58.

    Soro, V. et al. Axenic culture of a candidate division TM7 bacterium from the human oral cavity and biofilm interactions with other oral bacteria. Appl. Environ. Microbiol. 80, 6480–6489 (2014).

    PubMed  PubMed Central  Google Scholar 

  59. 59.

    Brown, C. T., Olm, M. R., Thomas, B. C. & Banfield, J. F. Measurement of bacterial replication rates in microbial communities. Nat. Biotechnol. 34, 1256–1263 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Moran, N. A. & Wernegreen, J. J. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15, 321–326 (2000).

    CAS  Google Scholar 

  61. 61.

    Moran, N. A. & Bennett, G. M. The tiniest tiny genomes. Annu. Rev. Microbiol. 68, 195–215 (2014).

    CAS  Google Scholar 

  62. 62.

    Lenhart, J. S. et al. RecO and RecR are necessary for RecA loading in response to DNA damage and replication fork stress. J. Bacteriol. 196, 2851–2860 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. 63.

    Burstein, D. et al. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. Nat. Commun. 7, 10613 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Chen, I. & Dubnau, D. DNA uptake during bacterial transformation. Nat. Rev. Microbiol. 2, 241–249 (2004).

    CAS  Google Scholar 

  65. 65.

    Brasen, C., Esser, D., Rauch, B. & Siebers, B. Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol. Mol. Biol. Rev. 78, 89–175 (2014).

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Silva, P. J. et al. Enzymes of hydrogen metabolism in Pyrococcus furiosus. Eur. J. Biochem. 267, 6541–6551 (2000).

    CAS  Google Scholar 

  67. 67.

    Wrighton, K. C. et al. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. ISME J. 10, 2702–2714 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Aono, R. et al. Enzymatic characterization of AMP phosphorylase and ribose-1,5-bisphosphate isomerase functioning in an archaeal AMP metabolic pathway. J. Bacteriol. 194, 6847–6855 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Hernsdorf, A. W. et al. Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. ISME J. 11, 1915–1929 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Anantharaman, K. et al. Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum. PeerJ 4, e1607 (2016).

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Castelle, C. J., Brown, C. T., Thomas, B. C., Williams, K. H. & Banfield, J. F. Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation. Sci. Rep. 7, 40101 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Danczak, R. E. et al. Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities. Microbiome 5, 112 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. 73.

    León-Zayas, R. et al. The metabolic potential of the single cell genomes obtained from the Challenger Deep, Mariana Trench within the Candidate Superphylum Parcubacteria (OD1). Environ. Microbiol. 19, 2769–2784 (2017).

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Coursolle, D. & Gralnick, J. A. Reconstruction of extracellular respiratory pathways for iron(III) reduction in Shewanella Oneidensis strain MR-1. Front. Microbiol. 3, 56 (2012).

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Liu, J. et al. Identification and characterization of MtoA: a Decaheme c-Type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front. Microbiol. 3, 37 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Jiao, Y. & Newman, D. K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765–1773 (2007).

    CAS  Google Scholar 

  77. 77.

    Yan, Z, Wang, M. & Ferry, J. G. A ferredoxin-and F 420 H 2-dependent, electron-bifurcating, heterodisulfide reductase with homologs in the domains Bacteria and Archaea. 8, 2285–2301 (2017).

  78. 78.

    Yan, Z. & Ferry, J. G. Electron bifurcation and confurcation in methanogenesis and reverse methanogenesis. Front. Microbiol. 9, 1322 (2018).

    PubMed  PubMed Central  Google Scholar 

  79. 79.

    Castelle, C. J. & Banfield, J. F. Major new microbial groups expand diversity and alter our understanding of the Tree of Life. Cell 172, 1181–1197 (2018).

    CAS  Google Scholar 

  80. 80.

    Gross, C. A. et al. The functional and regulatory roles of sigma factors in transcription. Cold Spring Harb. Symp. Quant. Biol. 63, 141–155 (1998).

    CAS  Google Scholar 

  81. 81.

    Paget, M. Bacterial sigma factors and anti-sigma factors: structure, function and distribution. Biomolecules 5, 1245–1265 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Merrick, M. J. In a class of its own—the RNA polymerase sigma factor sigma 54 (sigma N). Mol. Microbiol. 10, 903–909 (1993).

    CAS  Google Scholar 

  83. 83.

    Mukai, T., Reynolds, N., Crnkovic´, A. & Söll, D. Bioinformatic analysis reveals archaeal tRNATyr and tRNATrp identities in bacteria. Life 7, 8 (2017).

    PubMed  PubMed Central  Google Scholar 

  84. 84.

    Armengod, M.-E. et al. Enzymology of tRNA modification in the bacterial MnmEG pathway. Biochimie 94, 1510–1520 (2012).

    CAS  Google Scholar 

  85. 85.

    Selvadurai, K., Wang, P., Seimetz, J. & Huang, R. H. Archaeal Elp3 catalyzes tRNA wobble uridine modification at C5 via a radical mechanism. Nat. Chem. Biol. 10, 810–812 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Krogan, N. J. & Greenblatt, J. F. Characterization of a six-subunit holo-elongator complex required for the regulated expression of a group of genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 8203–8212 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Glatt, S. et al. Structural basis for tRNA modification by Elp3 from Dehalococcoides mccartyi. Nat. Struct. Mol. Biol. 23, 794–802 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Guo, H., Arambula, D., Ghosh, P. & Miller, J. F. Diversity-generating retroelements in phage and bacterial genomes. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.MDNA3-0029-2014 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Paul, B. G. et al. Targeted diversity generation by intraterrestrial archaea and archaeal viruses. Nat. Commun. 6, 6585 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Paul, B. G. et al. Retroelement-guided protein diversification abounds in vast lineages of Bacteria and Archaea. Nat. Microbiol. 2, 17045 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Salman, V., Amann, R., Shub, D. A. & Schulz-Vogt, H. N. Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria. Proc. Natl Acad. Sci. USA 109, 4203–4208 (2012).

    CAS  Google Scholar 

  92. 92.

    Baker, B. J., Hugenholtz, P., Dawson, S. C. & Banfield, J. F. Extremely acidophilic protists from acid mine drainage host Rickettsiales-lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl. Environ. Microbiol. 69, 5512–5518 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Jay, Z. J. & Inskeep, W. P. The distribution, diversity, and importance of 16S rRNA gene introns in the order Thermoproteales. Biol. Direct 10, 35 (2015).

    PubMed  PubMed Central  Google Scholar 

  94. 94.

    Griffiths-Jones, S., Bateman, A., Marshall, M., Khanna, A. & Eddy, S. R. Rfam: an RNA family database. Nucleic Acids Res. 31, 439–441 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Tanaka, N., Meineke, B. & Shuman, S. RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J. Biol. Chem. 286, 30253–30257 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Shah, N. H. & Muir, T. W. Inteins: nature’s gift to protein chemists. Chem. Sci. 5, 446–461 (2014).

    CAS  Google Scholar 

  97. 97.

    Gong, J., Qing, Y., Guo, X. & Warren, A. ‘Candidatus Sonnebornia yantaiensis’, a member of candidate division OD1, as intracellular bacteria of the ciliated protist Paramecium bursaria (Ciliophora. Oligohymenophorea). Syst. Appl. Microbiol. 37, 35–41 (2014).

    CAS  Google Scholar 

  98. 98.

    Zetsche, B. et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163, 759–771 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Burstein, D. et al. New CRISPR–Cas systems from uncultivated microbes. Nature 542, 237–241 (2016).

    PubMed  PubMed Central  Google Scholar 

  100. 100.

    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Support was provided by grants from the Lawrence Berkeley National Laboratory’s Genomes-to-Watershed Scientific Focus Area. The US Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research funded the work under contract DE-AC02-05CH11231, the DOE carbon cycling programme DOE-SC10010566, the Sloan Foundation Deep Life (grant number G-2016-20166041), the Innovative Genomics Institute at the University of California, Berkeley and the Chan Zuckerberg Biohub. Sequencing was conducted by the DOE Joint Genome Institute, a DOE Office of Science User Facility, supported under contract number DE-AC02-05CH11231.

Reviewer information

Nature Reviews Microbiology thanks B. Baker, P. López-García, M. Strous and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

Authors

Contributions

C.J.C., J.F.B. and C.T.B. conducted new data analysis. C.T.B., K.A. and R.H.H. contributed to the discussion of content. C.J.C. and J.F.B. wrote the article, and J.F.B, C.J.C., C.T.B., K.A., A.J.P. and R.H.H. reviewed and edited the manuscript before submission.

Corresponding author

Correspondence to Jillian F. Banfield.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related link

ggKbase database: https://ggkbase.berkeley.edu/genome_summaries/1437-DPANN_CPR_overall_analyses_NRM_updated

Supplementary information

Glossary

Candidate phyla

A phylum that is defined on the basis of sequence information and lacks any isolated representative.

Monophyletic

A group of organisms that arose from a common ancestor.

Episymbionts

Symbionts that are attached to the surface of another cell.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Castelle, C.J., Brown, C.T., Anantharaman, K. et al. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat Rev Microbiol 16, 629–645 (2018). https://doi.org/10.1038/s41579-018-0076-2

Download citation

Further reading