Diverse uncultivated ultra-small bacterial cells in groundwater

Nature Communications

Volumn 6, Issue , 2015, Pages

  Luef, Birgit ^a,e   Frischkorn, Kyle R ^a,f   Wrighton, Kelly C ^a,g   Holman, Hoi Ying N ^b   Birarda, Giovanni ^b   Thomas, Brian C ^a   Singh, Andrea ^a   Williams, Kenneth H ^b   Siegerist, Cristina E ^a   Tringe, Susannah G ^c   Downing, Kenneth H ^b   Comolli, Luis R ^b   Banfield, Jillian F ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^f Och Spine at New York Presbyterian Hospitals   (United States)

^g OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; GROUND WATER; RNA 16S;

BACTERIUM; CELL ORGANELLE; DATA SET; FILTRATION; GENOME; GENOMICS; GROUNDWATER; MORPHOLOGY;

ARCHAEON; ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIUM PILUS; CELL SIZE; CELL ULTRASTRUCTURE; CELL VOLUME; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CYTOPLASM; FILTER; GENOME SIZE; METAGENOMICS; NONHUMAN; PHYLOGENY; RIBOSOME; SPIROCHETE; TRANSMISSION ELECTRON MICROSCOPY; BACTERIUM; DNA SEQUENCE; FILTRATION; GENETICS; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SPECIES DIFFERENCE; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS);

BACTERIA; BASE SEQUENCE; CRYOELECTRON MICROSCOPY; FILTRATION; GENOME SIZE; GROUNDWATER; MICROBIOTA; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; WATER MICROBIOLOGY;

EID: 84924085084     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7372     Document Type: Article

References (54)

1. McKay, D. S. et al. Search for past life on Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science 273, 924-930 (1996).
2. Uwins, P. J. R., Webb, R. I. & Taylor, A. P. Novel nano-organisms from Australian sandstones. Am. Mineral. 83, 1541-1550 (1998).
3. Kajander, E. O. & Çiftçioglu, N. Nanobacteria: an alternative mechanism for pathogenic intra- and extracellular calcification and stone formation. Proc. Natl Acad. Sci. USA 95, 8274-8279 (1998).
4. Young, J. D. & Martel, J. The rise and fall of nanobacteria. Sci. Am. 302, 52-59 (2009).
5. Duda, V. I. in: eLS (John Wiley & Sons, 2001).
6. Velimirov, B. Nanobacteria, ultramicrobacteria and starvation forms: A search for the smallest metabolizing bacterium. Microbes Environ. 16, 67-77 (2001).
7. Bae, H. C., Cota-Robles, E. H. & Casida, Jr L. E. Microflora of soil as viewed by transmission electron microscopy. Appl. Microbiol. 23, 637-648 (1972).
8. Watson, S. W., Novitsky, T. J., Quinby, H. L. & Valois, F. W. Determination of bacterial number and biomass in the marine environment. Appl. Environ. Microbiol. 33, 940-946 (1977).
9. Kjelleberg, S. et al. in Trends in Microbial Ecology (eds Guerrero, R. & Pedros-Alio, C.) (Spanish Society for Microbiology, 1993).
10. Steering Group for the Workshop on size limits of very small Microorganisms NRC. Size Limits of Very Small Microorgansisms: Proceedings of a Workshop (National Academy Press, 1999).
11. Ghai, R., Mizuno, C. M., Picazo, A., Camacho, A. & Rodriguez-Valera, F. Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci. Rep. 3, 2471 (2013).
12. Comolli, L. R., Baker, B. J., Downing, K. H., Siegerist, C. E. & Banfield, J. F. Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J. 3, 159-167 (2009).
13. Miyoshi, T., Iwatsuki, T. & Naganuma, T. Phylogenetic characterization of 16S rRNA gene clones from deep-groundwater microorganisms that pass through 0.2-micrometer-pore-size filters. Appl. Environ. Microbiol. 71, 1084-1088 (2005).
14. Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661-1665 (2012).
15. Rappé, M. S. & Giovannoni, S. J. The uncultured microbial majority. Annu. Rev. Microbiol. 57, 369-394 (2003).
16. Kantor, R. S. et al. Small genomes and sparse metabolisms of sedimentassociated bacteria from four candidate phyla. mBio 4, e708-e713 (2013).
17. Comolli, L. R. et al. A portable cryo-plunger for on-site intact cryogenic microscopy sample preparation in natural environments. Microsc. Res. Tech. 75, 829-836 (2012).
18. Milne, J. L. S. & Subramaniam, S. Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat. Rev. Microbiol. 7, 666-675 (2009).
19. Comolli, L. R., Luef, B. & Chan, C. S. High-resolution 2D and 3D cryo-TEM reveals structural adaptions of two stalk-forming bacteria to an Fe-oxidizing lifestyle. Environ. Microbiol. 13, 2915-2929 (2011).
20. Miller, C. S., Baker, B. J., Thomas, B. C., Singer, S. W. & Banfield, J. F. EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol. 12, R44 (2011).
21. Matsumi, R., Atomi, H., Driessen, A. J. M. & van der Oost, J. Isoprenoid biosynthesis in Archaea-biochemical and evolutionary implications. Res. Microbiol. 162, 39-52 (2011).
22. Probst, A. J. et al. Tackling the minority: sulfate-reducing bacteria in an archaea-dominated subsurface biofilm. ISME J. 7, 635-651 (2013).
23. Eltsov, M. & Dubochet, J. Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol. 187, 8047-8054 (2005).
24. Gilbert, R. J. C. et al. Three-dimensional structures of translating ribosomes by cryo-EM. Mol. Cell 14, 57-66 (2004).
25. Warner, J. R., Knopf, P. M. & Rich, A. A multiple ribosomal structure in protein synthesis. Proc. Natl Acad. Sci. USA 49, 122-129 (1963).
26. Schramm, A., Fuchs, B. M., Nielsen, J. L., Tonolla, M. & Stahl, D. A. Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ. Microbiol. 4, 713-720 (2002).
27. Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-538 (2013).
28. Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated archaea. Proc. Natl Acad. Sci. USA 107, 8806-8811 (2010).
29. Andersson, S. G. & Kurland, C. G. Reductive evolution of resident genomes. Trends Microbiol. 6, 263-268 (1998).
30. Moran, N. A. & Wernegreen, J. J. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15, 321-326 (2000).
31. McLean, J. S. et al. Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proc. Natl Acad. Sci. USA 110, E2390-E2399 (2013).
32. 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).
33. Chen, I. & Dubnau, D. DNA uptake during bacterial transformation. Nat. Rev. Microbiol. 2, 241-249 (2004).
34. Proft, T. & Baker, E. N. Pili in Gram-negative and Gram-positive bacteria- structure, assembly and their role in disease. Cell. Mol. Life Sci. 66, 613-635 (2009).
35. Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl Acad. Sci. USA 103, 11358-11363 (2006).
36. Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63-67 (2002).
37. Pavkov-Keller, T., Howorka, S. & Keller, W. The structure of bacterial S-layer proteins. Prog. Mol. Biol. Transl. Sci. 103, 73-130 (2011).
38. Sleytr, U. B. et al. Nanobiotechnology with S-layer proteins as building blocks. Prog. Mol. Biol. Transl. Sci. 103, 277-352 (2011).
39. Hugenholtz, P., Goebel, B. M. & Pace, N. R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765-4774 (1998).
40. Harris, J. K., Kelley, S. T. & Pace, N. R. New perspective on uncultured bacterial phylogenetic division OP11. Appl. Environ. Microbiol. 70, 845-849 (2004).
41. Baker, B. J. & Dick, G. J. Omic approaches in microbial ecology: charting the unknown. Microbe 8, 353-360 (2013).
42. Williams, K. H. et al. Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol. J. 28, 519-539 (2011).
43. Lane, D. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) (John Wiley and Sons, 1991).
44. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
45. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
46. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690 (2006).
47. Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128 (2006).
48. Peng, Y., Leung, H. C. M., Yiu, S. M. & Chin, F. Y. L. IDBA-UD: A de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420-1428 (2012).
49. Hyatt, D., LoCascio, P. F., Hauser, L. J. & Uberbacher, E. C. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28, 2223-2230 (2012).
50. Knierim, B. et al. Correlative microscopy for phylogenetic and ultrastructural characterization of microbial communities. Environ. Microbiol. Rep. 4, 36-41 (2011).
51. Downing, K. H. & Mooney, P. E. A charge coupled device camera with electron decelerator for intermediate voltage electron microscopy. Rev. Sci. Instrum. 79, 043702 (2008).
52. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
53. Collins, T. J. ImageJ for microscopy. BioTechniques 43, 25-30 (2007).
54. Birarda, G. et al. Synchrotron infrared imaging of advanced glycation endproducts (AGEs) in cardiac tissue from mice fed high glycemic diets. Biomed. Spectrosc. Imaging 2, 301-315 (2013).