Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling

Current Biology

Volumn 25, Issue 6, 2015, Pages 690-701

  Castelle, Cindy J ^a   Wrighton, Kelly C ^b   Thomas, Brian C ^a   Hug, Laura A ^a   Brown, Christopher T ^c   Wilkins, Michael J ^b   Frischkorn, Kyle R ^d   Tringe, Susannah G ^e   Singh, Andrea ^a   Markillie, Lye Meng ^f   Taylor, Ronald C ^f   Williams, Kenneth H ^g   Banfield, Jillian F ^a,h  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Department of Earth and Environmental Sciences   (United States)

^e DOE JOINT GENOME INSTITUTE   (United States)

^f PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^g LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS);

ANAEROBIC GROWTH; ARCHAEAL GENOME; ARCHAEON; BIODIVERSITY; BIOLOGICAL MODEL; CARBON CYCLE; CLASSIFICATION; GENETICS; METABOLISM; METAGENOMICS; PHYLOGENY;

ANAEROBIOSIS; ARCHAEA; BIODIVERSITY; CARBON CYCLE; GENOME, ARCHAEAL; METAGENOMICS; MODELS, BIOLOGICAL; MODELS, GENETIC; PHYLOGENY;

EID: 84926417610     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.01.014     Document Type: Article

References (59)

1. C.R. Woese, O. Kandler, and M.L. Wheelis Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya Proc. Natl. Acad. Sci. USA 87 1990 4576 4579
2. S.M. Barns, C.F. Delwiche, J.D. Palmer, and N.R. Pace Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences Proc. Natl. Acad. Sci. USA 93 1996 9188 9193
3. J.G. Elkins, M. Podar, D.E. Graham, K.S. Makarova, Y. Wolf, L. Randau, B.P. Hedlund, C. Brochier-Armanet, V. Kunin, and I. Anderson A korarchaeal genome reveals insights into the evolution of the Archaea Proc. Natl. Acad. Sci. USA 105 2008 8102 8107
4. M. Könneke, A.E. Bernhard, J.R. de la Torre, C.B. Walker, J.B. Waterbury, and D.A. Stahl Isolation of an autotrophic ammonia-oxidizing marine archaeon Nature 437 2005 543 546
5. C. Brochier-Armanet, B. Boussau, S. Gribaldo, and P. Forterre Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota Nat. Rev. Microbiol. 6 2008 245 252
6. T. Nunoura, Y. Takaki, J. Kakuta, S. Nishi, J. Sugahara, H. Kazama, G.J. Chee, M. Hattori, A. Kanai, and H. Atomi Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group Nucleic Acids Res. 39 2011 3204 3223
7. L. Guy, and T.J. Ettema The archaeal 'TACK' superphylum and the origin of eukaryotes Trends Microbiol. 19 2011 580 587
8. J. Meng, J. Xu, D. Qin, Y. He, X. Xiao, and F. Wang Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses ISME J. 8 2014 650 659
9. K.G. Lloyd, L. Schreiber, D.G. Petersen, K.U. Kjeldsen, M.A. Lever, A.D. Steen, R. Stepanauskas, M. Richter, S. Kleindienst, and S. Lenk Predominant archaea in marine sediments degrade detrital proteins Nature 496 2013 215 218
10. H. Huber, M.J. Hohn, R. Rachel, T. Fuchs, V.C. Wimmer, and K.O. Stetter A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont Nature 417 2002 63 67
11. B.J. Baker, G.W. Tyson, R.I. Webb, J. Flanagan, P. Hugenholtz, E.E. Allen, and J.F. Banfield Lineages of acidophilic archaea revealed by community genomic analysis Science 314 2006 1933 1935
12. B.J. Baker, L.R. Comolli, G.J. Dick, L.J. Hauser, D. Hyatt, B.D. Dill, M.L. Land, N.C. Verberkmoes, R.L. Hettich, and J.F. Banfield Enigmatic, ultrasmall, uncultivated Archaea Proc. Natl. Acad. Sci. USA 107 2010 8806 8811
13. P. Narasingarao, S. Podell, J.A. Ugalde, C. Brochier-Armanet, J.B. Emerson, J.J. Brocks, K.B. Heidelberg, J.F. Banfield, and E.E. Allen De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities ISME J. 6 2012 81 93
14. C. Rinke, P. Schwientek, A. Sczyrba, N.N. Ivanova, I.J. Anderson, J.F. Cheng, A. Darling, S. Malfatti, B.K. Swan, and E.A. Gies Insights into the phylogeny and coding potential of microbial dark matter Nature 499 2013 431 437
15. B.J. Baker, and G.J. Dick Omic approaches in microbial ecology: Charting the unknown Microbe 8 2013 353 360
16. E. Waters, M.J. Hohn, I. Ahel, D.E. Graham, M.D. Adams, M. Barnstead, K.Y. Beeson, L. Bibbs, R. Bolanos, and M. Keller The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism Proc. Natl. Acad. Sci. USA 100 2003 12984 12988
17. M. Podar, K.S. Makarova, D.E. Graham, Y.I. Wolf, E.V. Koonin, and A.L. Reysenbach 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 2013 9
18. L.R. Comolli, and J.F. Banfield Inter-species interconnections in acid mine drainage microbial communities Front. Microbiol. 5 2014 367
19. G.W. Tyson, J. Chapman, P. Hugenholtz, E.E. Allen, R.J. Ram, P.M. Richardson, V.V. Solovyev, E.M. Rubin, D.S. Rokhsar, and J.F. Banfield Community structure and metabolism through reconstruction of microbial genomes from the environment Nature 428 2004 37 43
20. A.P. Yelton, L.R. Comolli, N.B. Justice, C. Castelle, V.J. Denef, B.C. Thomas, and J.F. Banfield Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea BMC Genomics 14 2013 485
21. C.J. Castelle, L.A. Hug, K.C. Wrighton, B.C. Thomas, K.H. Williams, D. Wu, S.G. Tringe, S.W. Singer, J.A. Eisen, and J.F. Banfield Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment Nat. Commun. 4 2013 2120
22. L.A. Hug, C.J. Castelle, K.C. Wrighton, B.C. Thomas, I. Sharon, K.R. Frischkorn, K.H. Williams, S.G. Tringe, and J.F. Banfield Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling Microbiome 1 2013 22
23. K.C. Wrighton, B.C. Thomas, I. Sharon, C.S. Miller, C.J. Castelle, N.C. VerBerkmoes, M.J. Wilkins, R.L. Hettich, M.S. Lipton, and K.H. Williams Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla Science 337 2012 1661 1665
24. Y. Peng, H.C. Leung, S.M. Yiu, and F.Y. Chin IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Bioinformatics 28 2012 1420 1428
25. R. Sorek, Y. Zhu, C.J. Creevey, M.P. Francino, P. Bork, and E.M. Rubin Genome-wide experimental determination of barriers to horizontal gene transfer Science 318 2007 1449 1452
26. D. Wu, A. Hartman, N. Ward, and J.A. Eisen An automated phylogenetic tree-based small subunit rRNA taxonomy and alignment pipeline (STAP) PLoS ONE 3 2008 e2566
27. D.E. Holmes, L. Giloteaux, R. Orellana, K.H. Williams, M.J. Robbins, and D.R. Lovley Methane production from protozoan endosymbionts following stimulation of microbial metabolism within subsurface sediments Front. Microbiol. 5 2014 366
28. B. Dridi, M.L. Fardeau, B. Ollivier, D. Raoult, and M. Drancourt Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces Int. J. Syst. Evol. Microbiol. 62 2012 1902 1907
29. G. Borrel, N. Parisot, H.M.B. Harris, E. Peyretaillade, N. Gaci, W. Tottey, O. Bardot, K. Raymann, S. Gribaldo, and P. Peyret Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine BMC Genomics 15 2014 679
30. V. Iverson, R.M. Morris, C.D. Frazar, C.T. Berthiaume, R.L. Morales, and E.V. Armbrust Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota Science 335 2012 587 590
31. P. Hugenholtz, C. Pitulle, K.L. Hershberger, and N.R. Pace Novel division level bacterial diversity in a Yellowstone hot spring J. Bacteriol. 180 1998 366 376
32. G.J. Dick, A.F. Andersson, B.J. Baker, S.L. Simmons, B.C. Thomas, A.P. Yelton, and J.F. Banfield Community-wide analysis of microbial genome sequence signatures Genome Biol. 10 2009 R85
33. P. Puigbò, Y.I. Wolf, and E.V. Koonin Search for a 'Tree of Life' in the thicket of the phylogenetic forest J. Biol. 8 2009 59
34. C. Breton, L. Snajdrová, C. Jeanneau, J. Koca, and A. Imberty Structures and mechanisms of glycosyltransferases Glycobiology 16 2006 29R 37R
35. M.F. Giraud, and J.H. Naismith The rhamnose pathway Curr. Opin. Struct. Biol. 10 2000 687 696
36. G.D. Sprott, K.M. Shaw, and K.F. Jarrell Isolation and chemical composition of the cytoplasmic membrane of the archaebacterium Methanospirillum hungatei J. Biol. Chem. 258 1983 4026 4031
37. E.E. Gill, and F.S. Brinkman The proportional lack of archaeal pathogens: Do viruses/phages hold the key? BioEssays 33 2011 248 254
38. R.F. Shand, and K.J. Leyva Peptide and protein antibiotics from the domain Archaea: Halocins and sulfolobicins M.A. Riley, M.A. Chavan, Bacteriocins: Ecology and Evolution 2007 Springer 93 109
39. C. Artola-Recolons, C. Carrasco-López, L.I. Llarrull, M. Kumarasiri, E. Lastochkin, I. Martínez de Ilarduya, K. Meindl, I. Usón, S. Mobashery, and J.A. Hermoso High-resolution crystal structure of MltE, an outer membrane-anchored endolytic peptidoglycan lytic transglycosylase from Escherichia coli Biochemistry 50 2011 2384 2386
40. L. Schöcke, and B. Schink Membrane-bound proton-translocating pyrophosphatase of Syntrophus gentianae, a syntrophically benzoate-degrading fermenting bacterium Eur. J. Biochem. 256 1998 589 594
41. I.A. Berg, D. Kockelkorn, W.H. Ramos-Vera, R.F. Say, J. Zarzycki, M. Hügler, B.E. Alber, and G. Fuchs Autotrophic carbon fixation in archaea Nat. Rev. Microbiol. 8 2010 447 460
42. N.H. Youssef, C. Rinke, R. Stepanauskas, I. Farag, T. Woyke, and M.S. Elshahed Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum "Diapherotrites" ISME J. 9 2015 447 460
43. P.M. Vignais Hydrogenases and H(+)-reduction in primary energy conservation Results Probl. Cell Differ. 45 2008 223 252
44. P.J. Silva, E.C. van den Ban, H. Wassink, H. Haaker, B. de Castro, F.T. Robb, and W.R. Hagen Enzymes of hydrogen metabolism in Pyrococcus furiosus Eur. J. Biochem. 267 2000 6541 6551
45. C.H. Verhees, S.W. Kengen, J.E. Tuininga, G.J. Schut, M.W. Adams, W.M. De Vos, and J. Van Der Oost The unique features of glycolytic pathways in Archaea Biochem. J. 375 2003 231 246
46. J. Glasemacher, A.K. Bock, R. Schmid, and P. Schønheit Purification and properties of acetyl-CoA synthetase (ADP-forming), an archaeal enzyme of acetate formation and ATP synthesis, from the hyperthermophile Pyrococcus furiosus Eur. J. Biochem. 244 1997 561 567
47. C. Ingram-Smith, and K.S. Smith AMP-forming acetyl-CoA synthetases in Archaea show unexpected diversity in substrate utilization Archaea 2 2007 95 107
48. T. Sato, H. Atomi, and T. Imanaka Archaeal type III RuBisCOs function in a pathway for AMP metabolism Science 315 2007 1003 1006
49. F.R. Tabita, T.E. Hanson, S. Satagopan, B.H. Witte, and N.E. Kreel Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms Philos. Trans. R. Soc. Lond. B Biol. Sci. 363 2008 2629 2640
50. R. Aono, T. Sato, A. Yano, S. Yoshida, Y. Nishitani, K. Miki, T. Imanaka, and H. Atomi Enzymatic characterization of AMP phosphorylase and ribose-1,5-bisphosphate isomerase functioning in an archaeal AMP metabolic pathway J. Bacteriol. 194 2012 6847 6855
51. R.S. Kantor, K.C. Wrighton, K.M. Handley, I. Sharon, L.A. Hug, C.J. Castelle, B.C. Thomas, and J.F. Banfield Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla MBio 4 2013 e00708 e00713
52. G.C. Atkinson, T. Tenson, and V. Hauryliuk The RelA/SpoT homolog (RSH) superfamily: distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life PLoS ONE 6 2011 e23479
53. R.D. Finn, A. Bateman, J. Clements, P. Coggill, R.Y. Eberhardt, S.R. Eddy, A. Heger, K. Hetherington, L. Holm, and J. Mistry Pfam: the protein families database Nucleic Acids Res. 42 2014 D222 D230
54. Z.D. Dalebroux, and M.S. Swanson ppGpp: magic beyond RNA polymerase Nat. Rev. Microbiol. 10 2012 203 212
55. A. Cellini, G.L. Scoarughi, P. Poggiali, I. Santino, R. Sessa, P. Donini, and C. Cimmino Stringent control in the archaeal genus Sulfolobus Res. Microbiol. 155 2004 98 104
56. K.C. Wrighton, C.J. Castelle, M.J. Wilkins, L.A. Hug, I. Sharon, B.C. Thomas, K.M. Handley, S.W. Mullin, C.D. Nicora, and A. Singh Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer ISME J. 8 2014 1452 1463
57. E.F. DeLong Archaea in coastal marine environments Proc. Natl. Acad. Sci. USA 89 1992 5685 5689
58. C. Vetriani, H.W. Jannasch, B.J. MacGregor, D.A. Stahl, and A.L. Reysenbach Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments Appl. Environ. Microbiol. 65 1999 4375 4384
59. K. Takai, and K. Horikoshi Genetic diversity of archaea in deep-sea hydrothermal vent environments Genetics 152 1999 1285 1297