The bright side of microbial dark matter: Lessons learned from the uncultivated majority

Current Opinion in Microbiology

Volumn 31, Issue , 2016, Pages 217-226

  Solden, Lindsey ^a   Lloyd, Karen ^b   Wrighton, Kelly ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN; METAGENOMICS; TREE OF LIFE; ARCHAEAL GENOME; ARCHAEON; BACTERIAL GENOME; BACTERIUM; GENETICS; METABOLISM; SINGLE CELL ANALYSIS;

RNA 16S;

ARCHAEA; BACTERIA; GENOME, ARCHAEAL; GENOME, BACTERIAL; METAGENOMICS; RNA, RIBOSOMAL, 16S; SINGLE-CELL ANALYSIS;

EID: 84966781466     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2016.04.020     Document Type: Review

References (68)

1. Castelle C.J., Wrighton K.C., Thomas B.C., Hug L.A., Brown C.T., Wilkins M.J., Frischkorn K.R., Tringe S.G., Singh A., Markillie L.M., et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol 2015, 25.
2. Rinke C., Schwientek P., Sczyrba A., Ivanova N.N., Anderson I.J., Cheng J.-F., Darling A., Malfatti S., Swan B.K., Gies E.A., et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 2013, 499(7459):431-437.
3. 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. Unusual biology across a group comprising more than 15% of domain bacteria. Nature 2015, 523(7559):208-211.
4. Baker B.J., Lazar C.S., Teske A.P., Dick G.J. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome 2015, 3:14.
5. Hug L.A., Baker B.J., Anantharaman K., Brown C.T., Probst A.J., Castelle C.J., Butterfield C.N., Hernsdorf A.W., Amano Y., Ise K., Suzuki Y., Dudek N., Relman D.A., Finstad K.M., Amundson R., Thomas B.C., Banfield J.F. A new view of the tree of life. Nat Microbiol 2016, 16048.
6. Yarza P., Yilmaz P., Pruesse E., Glockner F.O., Ludwig W., Schleifer K.H., Whitman W.B., Euzeby J., Amann R., Rossello-Mora R. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014, 12(9):635-645.
7. Baker B.J. Omic approaches in microbial ecology: charting the unknown. Microbe 2013, 8(9):353-359.
8. Hedlund B.P., Dodsworth J.A., Murugapiran S.K., Rinke C., Woyke T. Impact of single-cell genomics and metagenomics on the emerging view of extremophile "microbial dark matter". Extremophiles 2014, 18(5):865-875.
9. Sharon I., Banfield J.F. Genomes from metagenomics. Science 2013, 342:1057-1058.
10. Wrighton K.C., Thomas B.C., Sharon I., Miller C.S., Castelle C.J., VerBerkmoes N.C., Wilkins M.J., Hettich R.L., Lipton M.S., Williams K.H., Long P.E., Banfield J.F. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 2012, 337(6102):1661-1665.
11. Kantor R.S., Wrighton K.C., Handley K.M., Sharon I., Hug L.A., Castelle C.J., Thomas B.C., Banfield J.F. Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. MBio 2013, 4(5):e00708-e00713.
12. Albertsen M., Hugenholtz P., Skarshewski A., Nielsen K.L., Tyson G.W., Nielsen P.H. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 2013, 31(6):533-538.
13. Seitz K.W., Lazar C.S., Hinrichs K.U., Teske A.P., Baker B.J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J 2016, 10.1038/ismej.2015.233.
14. Spang A., Saw J.H., Jorgensen S.L., Zaremba-Niedzwiedzka K., Martijn J., Lind A.E., van Eijk R., Schleper C., Guy L., Ettema T.J. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 2015, 521(7551):173-179.
15. Evans P.N., Parks D.H., Chadwick G.L., Robbins S.J., Orphan V.J., Golding S.D., Tyson G.W. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 2015, 350(6259):434-438.
16. Baker B.J., Saw J.H., Lind A.E., Lazar C.S., Hinrichs K.U., Teske A.P., Ettema J.G. Genomic inference of the metabolism of a cosmopolitan subsurface Archaea, Hadesarchaea. Nat Microbiol 2016, 1.
17. Lloyd K.G., Schreiber L., Petersen D.G., Kjeldsen K.U., Lever M.A., Steen A.D., Stepanauskas R., Richter M., Kleindienst S., Lenk S., Schramm A., Jorgensen B.B. Predominant archaea in marine sediments degrade detrital proteins. Nature 2013, 496(7444):215-218.
18. Lazar C.S., Baker B.J., Seitz K., Hyde A.S., Dick G.J., Hinrichs K., Teske A.P. Genomic evidence for distinct carbon substrate preferences and ecolofical niches of Bathyarchaeota in estuarine sediments. Environ Microbiol 2016, 18.
19. Campbell J.H., O'Donoghue P., Campbell A.G., Schwientek P., Sczyrba A., Woyke T., Soll D., Podar M. UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc Natl Acad Sci U S A 2013, 110(14):5540-5545.
20. McLean J.S., Lombardo M.J., Badger J.H., Edlund A., Novotny M., Yee-Greenbaum J., Vyahhi N., Hall A.P., Yang Y., Dupont C.L., Ziegler M.G., Chitsaz H., Allen A.E., Yooseph S., Tesler G., Pevzner P.A., Friedman R.M., Nealson K.H., Venter J.C., Lasken R.S. Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proc Natl Acad Sci U S A 2013, 110(26):E2390-E2399.
21. Yeoh Y.K., Sekiguchi Y., Parks D.H., Hugenholtz P. Comparative genomics of candidate phylum TM6 suggests that parasitism is widespread and ancestral in this lineage. Mol Biol Evol 2015, 33.
22. Reddy T.B., Thomas A.D., Stamatis D., Bertsch J., Isbandi M., Jansson J., Mallajosyula J., Pagani I., Lobos E.A., Kyrpides N.C. The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res 2015, 43(Database issue):D1099-D1106.
23. Woese C.R., Fox G.E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 1977, 74(11):5088-5090.
24. Woese C.R., Kandler O., Wheelis M.L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 1990, 87(12):4576-4579.
25. Williams T.A., Foster P.G., Nye T.M., Cox C.J., Embley T.M. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci 2012, 279(1749):4870-4879.
26. Williams T.A., Embley T.M. Archaeal "dark matter" and the origin of eukaryotes. Genome Biol Evol 2014, 6(3):474-481.
27. Lake J.A., Henderson E., Oakes M., Clark M.W. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci U S A 1984, 81(12):3786-3790.
28. Villanueva L., Schouten S., Sinninghe Damste J.S. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the 'lipid divide'. Env Micro 2016, 10.1111/1462-2920.13361.
29. Pedersen R.B., Rapp H.T., Thorseth I.H., Lilley M.D., Barriga F.J., Baumberger T., Flesland K., Fonseca R., Fruh-Green G.L., Jorgensen S.L. Discovery of a black smoker vent field and vent fauna at the Arctic Mid-Ocean Ridge. Nat Commun 2010, 1:126.
30. Kubatko L.S., Degnan J.H. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 2007, 56(1):17-24.
31. Takai K., Moser D.P., DeFlaun M., Onstott T.C., Fredrickson J.K. Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 2001, 67(12):5750-5760.
32. Jurgens G., Glockner F., Amann R., Saano A., Montonen L., Likolammi M., Munster U. Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization(1). FEMS Microbiol Ecol 2000, 34(1):45-56.
33. Meng J., Xu J., Qin D., He Y., Xiao X., Wang F. Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 2014, 8(3):650-659.
34. Kubo K., Lloyd K.G., Biddle F.J., Amann R., Reske A., Knittel K. Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J 2012, 6(10):1949-1965.
35. He Y., Li M., Perumal V., Feng X., Fang J., Xie J., Sievert S.M., Wang F. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 2016, 16035.
36. Scheller S., Goenrich M., Boecher R., Thauer R.K., Jaun B. The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 2010, 465(7298):606-608.
37. Elshahed M.S., Najar F.Z., Aycock M., Qu C., Roe B.A., Krumholz L.R. Metagenomic analysis of the microbial community at Zodletone Spring (Oklahoma): insights into the genome of a member of the novel candidate division OD1. Appl Environ Microbiol 2005, 71(11):7598-7602.
38. Harris J.K., Kelley S.T., Pace N.R. New perspective on uncultured bacterial phylogenetic division OP11. Appl Environ Microbiol 2004, 70(2):845-849.
39. Raghavan R., Hicks L.D., Minnick M.F. Toxic introns and parasitic intein in Coxiella burnetii: legacies of a promiscuous past. J Bacteriol 2008, 190(17):5934-5943.
40. Dueholm M.S., Albertsen M., Stokholm-Bjerregaard M., McIlroy S.J., Karst S.M., Nielsen P.H. Complete genome sequence of the bacterium Aalborg_AAW-1, representing a novel family within the candidate phylum SR1. Genome Announc 2015, 3(3).
41. Hanke A., Hamann E., Sharma R., Geelhoed J.S., Hargesheimer T., Kraft B., Meyer V., Lenk S., Osmers H., Wu R., et al. Recoding of the stop codon UGA to glycine by a BD1-5/SN-2 bacterium and niche partitioning between Alpha- and Gammaproteobacteria in a tidal sediment microbial community naturally selected in a laboratory chemostat. Front Microbiol 2014, 5:231.
42. Ivanova N.N., Schwientek P., Tripp H.J., Rinke C., Pati A., Huntemann M., Visel A., Woyke T., Kyrpides N.C., Rubin E.M. Stop codon reassignments in the wild. Science 2014, 344(6186):909-913.
43. Nelson W.C., Stegen J.C. The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle. Front Microbiol 2015, 6:713.
44. Lombard V., Golaconda R.H., Drula E., Coutinho P.M., Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2013, 42:D490-D495.
45. Anantharaman K., Brown C.T., Burstein D., Castelle C.J., Probst A.J., Thomas B.C., Williams K.H., Banfield J.F. Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum. PeerJ 2016, 4:e1607.
46. Wrighton K.C., Castelle C.J., Wilkins M.J., Hug L.A., Sharon I., Thomas B.C., Handley K.M., Mullin S.W., Nicora C.D., Singh A., et al. Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. ISME J 2014, 8(7):1452-1463.
47. Luef B., Frischkorn K.R., Wrighton K.C., Holman H.Y.N., Birarda G., Thomas B.C., Singh A., Williams K.H., Siegerist C.E., Tringe S.G., Downing K.H., Comolli L.R., Banfield J.F. Diverse uncultivated ultra-small bacterial cells in groundwater. Nat Commun 2015, 6.
48. Giovannoni S.J., Cameron Thrash J., Temperton B. Implications of streamlining theory for microbial ecology. ISME J 2014, 8(8):1553-1565.
49. He X., McLean J.S., Edlund A., Yooseph S., Hall A.P., Liu S.Y., Dorrestein P.C., Esquenazi E., Hunter R.C., Cheng G., Nelson K.E., Lux R., Shi W. Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle. Proc Natl Acad Sci U S A 2015, 112(1):244-249.
50. 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 2014, 37(1):35-41.
51. Wrighton K.C., Castelle C.J., Varaljay C.A., Satagopan S., Brown C.T., Wilkins M.J., Thomas B.C., Sharon I., Williams K.H., Tabita F.R., Banfield J.F. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. ISME J 2016, 8:1452-1463.
52. Michalska K., Steen A.D., Chhor G., Endres M., Webber A.T., Bird J., Lloyd K.G., Joachimiak A. New aminopeptidase from "microbial dark matter" archaeon. FASEB J 2015, 29(9):4071-4079.
53. Stott M.B., Crowe M.A., Mountain B.W., Smirnova A.V., Hou S., Alam M., Dunfield P.F. Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ Microbiol 2008, 10(8):2030-2041.
54. Konneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437(7058):543-546.
55. Hugenholtz P., Pitulle C., Hershberger K.L., Pace N.R. Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 1998, 180(2):366-376.
56. Tanaka Y., Tamaki H., Matsuzawa H., Nigaya M., Mori K., Kamagata Y. Microbial community analysis in the roots of aquatic plants and isolation of novel microbes including an organism of the candidate phylum OP10. Microbes Environ 2012, 27(2):149-157.
57. Marcy Y., Ouverney C., Bik E.M., Losekann T., Ivanova N., Martin H.G., Szeto E., Platt D., Hugenholtz P., Relman D.A., Quake S.R. Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci U S A 2007, 104(29):11889-11894.
58. Tian Y., He X., Torralba M., Yooseph S., Nelson K.E., Lux R., McLean J.S., Yu G., Shi W. Using DGGE profiling to develop a novel culture medium suitable for oral microbial communities. Mol Oral Microbiol 2010, 25(5):357-367.
59. McInerney M.J., Struchtemeyer C.G., Sieber J., Mouttaki H., Stams A.J., Schink B., Rohlin L., Gunsalus R.P. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 2008, 1125:58-72.
60. Henson M.W., Pitre D.M., Weckhorst J.L., Lanclos V.C., Webber A.T., Thrash J.C. Artificial seawater media facilitates cultivating members of the microbial majority from the Gulf of Mexico. mSphere 2016, 1(2):e00028-16.
61. Kaeberlein T., Lewis K., Epstein S.S. Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment. Science 2002, 296(5570):1127-1129.
62. Stewart E.J. Growing unculturable bacteria. J Bacteriol 2012, 194(16):4151-4160.
63. Konstantinidis K.T., Rossello-Mora R. Classifying the uncultivated microbial majority: a place for metagenomic data in the Candidatus proposal. Syst Appl Microbiol 2015, 38(4):223-230.
64. Martinez-Lavanchy P.M., Dohrmann A.B., Imfeld G., Trescher K., Tebbe C.C., Richnow H.H., Nijenhuis I. Detection of monochlorobenzene metabolizing bacteria under anoxic conditions by DNA-stable isotope probing. Biodegradation 2011, 22(5):973-982.
65. Peura S., Eiler A., Bertilsson S., Nykanen H., Tiirola M., Jones R.I. Distinct and diverse anaerobic bacterial communities in boreal lakes dominated by candidate division OD1. ISME J 2012, 6(9):1640-1652.
66. Baker B.J., Comolli L.R., Dick G.J., Hauser L.J., Hyatt D., Dill B.D., Land M.L., Verberkmoes N.C., Hettich R.L., Banfield J.F. Enigmatic, ultrasmall, uncultivated Archaea. Proc Natl Acad Sci U S A 2010, 107(19):8806-8811.
67. Orphan V.J., House C.H., Hinrichs K.U., McKeegan K.D., DeLong E.F. Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci U S A 2002, 99(11):7663-7668.
68. Garcia P.A., Ge Z., Moran J.L., Buie C.R. Microfluidic screening of electric fields for electroporation. Sci Rep 2016, 6.