Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment

Nature Communications

Volumn 7, Issue , 2016, Pages

  Wurch, Louie ^a,b,d   Giannone, Richard J ^a   Belisle, Bernard S ^a,b   Swift, Carolyn ^a,b   Utturkar, Sagar ^a   Hettich, Robert L ^a,b   Reysenbach, Anna Louise ^c   Podar, Mircea ^a,b  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c PORTLAND STATE UNIVERSITY   (United States)

^d JAMES MADISON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BACTERIUM; BIOCHEMISTRY; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; GENOMICS; GEOTHERMAL SYSTEM; PHYSIOLOGICAL RESPONSE; RESPIRATION; SYMBIONT;

AMINO ACID SEQUENCE; ARTICLE; CARBOHYDRATE METABOLISM; CELLULAR ORGANISM; COCULTURE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE SEQUENCE; GENOMICS; GLUCONEOGENESIS; GLYCOLYSIS; GLYCOSYLATION; HOST; INFORMATION PROCESSING; NANOARCHAEOTA; NANOARCHAEUM EQUITANS; NONHUMAN; PROTEOMICS; SYNTHESIS; TERRESTRIAL SURFACE WATERS; THERMAL SPRING; ARCHAEAL GENOME; CHROMOSOMAL MAPPING; CLASSIFICATION; CRENARCHAEOTA; EVOLUTION; GENE EXPRESSION; GENETICS; METABOLISM; PHYLOGENY; PROCEDURES; SYMBIOSIS; ULTRASTRUCTURE;

ACIDILOBUS; CRENARCHAEOTA; NANOARCHAEOTA; NANOARCHAEUM EQUITANS;

ARCHAEAL PROTEIN;

ARCHAEAL PROTEINS; BIOLOGICAL EVOLUTION; CHROMOSOME MAPPING; CRENARCHAEOTA; GENE EXPRESSION; GENOME, ARCHAEAL; GENOMICS; HOT SPRINGS; NANOARCHAEOTA; PHYLOGENY; SYMBIOSIS;

EID: 84977263419     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12115     Document Type: Article

References (56)

1. Brown, C. T. et al. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523, 208-211 (2015).
2. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437 (2013).
3. Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661-1665 (2012).
4. 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).
5. Comolli, L. R. & Banfield, J. F. Inter-species interconnections in acid mine drainage microbial communities. Front. Microbiol. 5, 367 (2014).
6. Probst, A. J. et al. Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nat. Commun. 5, 5497 (2014).
7. Pernthaler, A. et al. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc. Natl Acad. Sci. USA 105, 7052-7057 (2008).
8. Tyson, G. W. et al. Genome-directed isolation of the key nitrogen fixer Leptospirillum ferrodiazotrophum sp. nov. from an acidophilic microbial community. Appl. Environ. Microbiol. 71, 6319-6324 (2005).
9. Bomar, L., Maltz, M., Colston, S. & Graf, J. Directed culturing of microorganisms using metatranscriptomics. mBio 2, e00012-00011 (2011).
10. Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63-67 (2002).
11. Casanueva, A. et al. Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments. Extremophiles 12, 651-656 (2008).
12. Clingenpeel, S. et al. Yellowstone lake nanoarchaeota. Front. Microbiol. 4, 274 (2013).
13. Flores, G. E. et al. Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ. Microbiol. 13, 2158-2171 (2011).
14. Flores, G. E. et al. Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin. Geobiology 10, 333-346 (2012).
15. Hohn, M. J., Hedlund, B. P. & Huber, H. Detection of 16S rDNA sequences representing the novel phylum "Nanoarchaeota": indication for a wide distribution in high temperature biotopes. Syst. Appl. Microbiol. 25, 551-554 (2002).
16. McCliment, E. A. et al. Colonization of nascent, deep-sea hydrothermal vents by a novel Archaeal and Nanoarchaeal assemblage. Environ. Microbiol. 8, 114-125 (2006).
17. Giannone, R. J. et al. Proteomic characterization of cellular and molecular processes that enable the Nanoarchaeum equitans-Ignicoccus hospitalis relationship. PLoS One 6, e22942 (2011).
18. Giannone, R. J. et al. Life on the edge: functional genomic response of Ignicoccus hospitalis to the presence of Nanoarchaeum equitans. ISME J. 9, 101-114 (2015).
19. Jahn, U. et al. Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two archaea. J. Bacteriol. 190, 1743-1750 (2008).
20. 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).
21. Waters, E. et al. The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl Acad. Sci. USA 100, 12984-12988 (2003).
22. Podar, M. et al. Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol. Direct 8, 9 (2013).
23. Forterre, P. The universal tree of life: an update. Front. Microbiol. 6, 717 (2015).
24. Petitjean, C., Deschamps, P., Lopez-Garcia, P. & Moreira, D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191-204 (2015).
25. Munson-McGee, J. H. et al. Nanoarchaeota, their sulfolobales host, and Nanoarchaeota virus distribution across Yellowstone National Park Hot Springs. Appl. Environ. Microbiol. 81, 7860-7868 (2015).
26. Brock, T. D., Brock, K. M., Belly, R. T. &Weiss, R. L. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch. Mikrobiol. 84, 54-68 (1972).
27. Luef, B. et al. Diverse uncultivated ultra-small bacterial cells in groundwater. Nat. Commun. 6, 6372 (2015).
28. Boyd, E. S. et al. Isolation, characterization, and ecology of sulfur-respiring Crenarchaea inhabiting acid-sulfate-chloride-containing geothermal springs in yellowstone national park. Appl. Environ. Microbiol. 73, 6669-6677 (2007).
29. Prokofeva, M. I. et al. Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. Int. J. Syst. Evol. Microbiol. 59, 3116-3122 (2009).
30. Prokofeva, M. I. et al. Acidilobus aceticus gen. nov., sp. nov., a novel anaerobic thermoacidophilic archaeon from continental hot vents in Kamchatka. Int. J. Syst. Evol. Microbiol. 50(Pt 6): 2001-2008 (2000).
31. Jay, Z. J. et al. Predominant acidilobus-like populations from geothermal environments in Yellowstone National Park exhibit similar metabolic potential in different hypoxic microbial communities. Appl. Environ. Microbiol. 80, 294-305 (2014).
32. Boyd, E. S. & Druschel, G. K. Involvement of intermediate sulfur species in biological reduction of elemental sulfur under acidic, hydrothermal conditions. Appl. Environ. Microbiol. 79, 2061-2068 (2013).
33. Mardanov, A. V. et al. The genome sequence of the crenarchaeon Acidilobus saccharovorans supports a new order, Acidilobales, and suggests an important ecological role in terrestrial acidic hot springs. Appl. Environ. Microbiol. 76, 5652-5657 (2010).
34. Randau, L., Munch, R., Hohn, M. J., Jahn, D. & Soll, D. Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5'-and 3'-halves. Nature 433, 537-541 (2005).
35. 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).
36. Imanaka, H., Yamatsu, A., Fukui, T., Atomi, H. & Imanaka, T. Phosphoenolpyruvate synthase plays an essential role for glycolysis in the modified Embden-Meyerhof pathway in Thermococcus kodakarensis. Mol. Microbiol. 61, 898-909 (2006).
37. Tjaden, B., Plagens, A., Dorr, C., Siebers, B. & Hensel, R. Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism. Mol. Microbiol. 60, 287-298 (2006).
38. Eichler, J. Extreme sweetness: protein glycosylation in archaea. Nat. Rev. Microbiol. 11, 151-156 (2013).
39. Maruyama, H. et al. Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis. Mol. Biol. Cell 22, 386-398 (2011).
40. Lewalter, K. & Muller, V. Bioenergetics of archaea: ancient energy conserving mechanisms developed in the early history of life. Biochim. Biophys. Acta 1757, 437-445 (2006).
41. Mohanty, S. et al. Structural basis for a unique ATP Synthase Core Complex from Nanoarchaeum equitans. J. Biol. Chem. 290, 27280-27296 (2015).
42. Bennett, G. M. & Moran, N. A. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a Phloem-feeding insect. Genome Biol. Evol. 5, 1675-1688 (2013).
43. McCutcheon, J. P. & Moran, N. A. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2, 708-718 (2010).
44. Oshima, K., Maejima, K. & Namba, S. Genomic and evolutionary aspects of phytoplasmas. Front. Microbiol. 4, 230 (2013).
45. Angelov, A. & Liebl, W. Insights into extreme thermoacidophily based on genome analysis of Picrophilus torridus and other thermoacidophilic archaea. J. Biotechnol. 126, 3-10 (2006).
46. Podar, M. et al. A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol. 9, R158 (2008).
47. 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).
48. Shakya, M. et al. Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities. Environ. Microbiol. 15, 1882-1899 (2013).
49. Karlovsky, P. & de Cock, A. W. Buoyant density of DNA-Hoechst 33258 (bisbenzimide) complexes in CsCl gradients: Hoechst 33258 binds to single AT base pairs. Anal. Biochem. 194, 192-197 (1991).
50. Utturkar, S. M. et al. Evaluation and validation of de novo and hybrid assembly techniques to derive high quality genome sequences. Bioinformatics 30, 2709-2716 (2014).
51. Wolf, Y. I., Makarova, K. S., Yutin, N. & Koonin, E. V. The updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol. Direct 7, 46 (2012).
52. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).
53. Tabb, D. L., Fernando, C. G. & Chambers, M. C. MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661 (2007).
54. Ma, Z. Q. et al. IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J. Proteome Res. 8, 3872-3881 (2009).
55. Xu, Q. et al. Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities. Sci. Adv. 2, e1501254 (2016).
56. Taverner, T. et al. DanteR: an extensible R-based tool for quantitative analysis of-omics data. Bioinformatics 28, 2404-2406 (2012).