Diversity and genomic insights into the uncultured Chloroflexi from the human microbiota

Environmental Microbiology

Volumn 16, Issue 9, 2014, Pages 2635-2643

  Campbell, Alisha G ^a,f   Schwientek, Patrick ^b   Vishnivetskaya, Tatiana ^c   Woyke, Tanja ^b   Levy, Shawn ^d   Beall, Clifford J ^e   Griffen, Ann ^e   Leys, Eugene ^e   Podar, Mircea ^a  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b DOE JOINT GENOME INSTITUTE   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

^d HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f NORTHWEST MISSOURI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROLINEAE; ANIMALIA; BACTERIA (MICROORGANISMS); CHLOROFLEXI; CHLOROFLEXI (CLASS); MAMMALIA;

BACTERIAL RNA;

CHLOROFLEXI; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOMICS; HUMAN; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUTH; PHYLOGENY; PROCEDURES; SINGLE CELL ANALYSIS;

CHLOROFLEXI; GENOMICS; HUMANS; MICROBIOTA; MOUTH; PHYLOGENY; RNA, BACTERIAL; SEQUENCE ANALYSIS, DNA; SINGLE-CELL ANALYSIS;

EID: 84906944512     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12461     Document Type: Article

References (62)

1. Abusleme, L., Dupuy, A.K., Dutzan, N., Silva, N., Burleson, J.A., Strausbaugh, L.D., etal. (2013) The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 7: 1016-1025.
2. Altschul, S.F., Gish, W., Miller, W., Meyers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Campbell, A.G., Campbell, J.H., Schwientek, P., Woyke, T., Sczyrba, A., Allman, S., etal. (2013a) Multiple single-cell genomes provide insight into functions of uncultured Deltaproteobacteria in the human oral cavity. PLoS ONE 8: e59361.
4. Campbell, J.H., O'Donoghue, P., Campbell, A.G., Schwientek, P., Sczyrba, A., Woyke, T., etal. (2013b) UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc Natl Acad Sci USA 110: 5540-5545.
5. Capestany, C.A., Tribble, G.D., Maeda, K., Demuth, D.R., and Lamont, R.J. (2008) Role of the Clp system in stress tolerance, biofilm formation, and intracellular invasion in Porphyromonas gingivalis. J Bacteriol 190: 1436-1446.
6. Caporaso, J., Kuczynski, J., Stombaugh, J., and Bittinger, K. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
7. Clemente, J.C., Ursell, L.K., Parfrey, L.W., and Knight, R. (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270.
8. Darling, A.C.E., Mau, B., Blattner, F.R., and Perna, N.T. (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
9. Derrien, M., Collado, M.C., Ben-Amor, K., Salminen, S., and de Vos, W.M. (2008) The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74: 1646-1648.
10. Dewhirst, F.E., Chen, T., Izard, J., Paster, B.J., Tanner, A.C.R., Yu, W.-H., etal. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
11. Dewhirst, F.E., Klein, E.A., Thompson, E.C., Blanton, J.M., Chen, T., Milella, L., etal. (2012) The canine oral microbiome. PLoS ONE 7: e36067.
12. Di Rienzi, S.C., Sharon, I., Wrighton, K.C., Koren, O., Hug, L.A., Thomas, B.C., etal. (2013) The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife 2: e01102.
13. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., etal. (2011) Geneious Pro (v5.6.3). URL http://www.geneious.com.
14. Frosch, M., and Muller, A. (1993) Phospholipid substitution of capsular polysaccharides and mechanisms of capsule formation in Neisseria meningitidis. Mol Microbiol 8: 483-493.
15. Garrity, G., and Holt, J. (2001) Phylum BVI, Chloroflexi phy. nov. In Bergey's Manual of Systematic Bacteriology: The Archasea and the Deeply Branching and Phototrophic Bacteria. Boone, D., and Castenholz, R. (eds). New York, USA: Springer, pp. 447-450.
16. Graentzdoerffer, A., Rauh, D., Pich, A., and Andreesen, J.R. (2003) Molecular and biochemical characterization of two tungsten- and selenium-containing formate dehydrogenases from Eubacterium acidaminophilum that are associated with components of an iron-only hydrogenase. Arch Microbiol 179: 116-130.
17. Griffen, A.L., Beall, C.J., Campbell, J.H., Firestone, N.D., Kumar, P.S., Yang, Z.K., etal. (2011) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6: 1176-1185.
18. Gupta, R.S., Chander, P., and George, S. (2013) Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexia class. nov. [corrected] into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov. Antonie Van Leeuwenhoek 103: 99-119.
19. Hug, L.A., Castelle, C.J., Wrighton, K.C., Thomas, B.C., Sharon, I., Frischkorn, K.R., etal. (2013) Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1: 22.
20. Hugenholtz, P., and Stackebrandt, E. (2004) Reclassification of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description). Int J Syst Evol Microbiol 54: 2049-2051.
21. Hugenholtz, P., Goebel, B.M., and Pace, N.R. (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180: 4765-4774.
22. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214.
23. Kindaichi, T., Ito, T., and Okabe, S. (2004) Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiography-fluorescence in situ hybridization. Appl Environ Microbiol 70: 1641-1650.
24. Klatt, C.G., Wood, J.M., Rusch, D.B., Bateson, M.M., Hamamura, N., Heidelberg, J.F., etal. (2011) Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J 5: 1262-1278.
25. Kong, Y.H., Teather, R., and Forster, R. (2010) Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiol Ecol 74: 612-622.
26. Lasken, R.S. (2012) Genomic sequencing of uncultured microorganisms from single cells. Nat Rev Microbiol 10: 631-640.
27. Ley, R.E., Backhed, F., Turnbaugh, P., Lozupone, C.A., Knight, R.D., and Gordon, J.I. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070-11075.
28. Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R., and Gordon, J.I. (2008a) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776-788.
29. Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., etal. (2008b) Evolution of mammals and their gut microbes. Science 320: 1647-1651.
30. de Lillo, A., Ashley, F.P., Palmer, R.M., Munson, M.A., Kyriacou, L., Weightman, A.J., and Wade, W.G. (2006) Novel subgingival bacterial phylotypes detected using multiple universal polymerase chain reaction primer sets. Oral Microbiol Immunol 21: 61-68.
31. Lin, W.S., Cunneen, T., and Lee, C.Y. (1994) Sequences, analysis and molecular characterization of genes required for the biosynthesis of type-1 capsular polysaccharide in Staphylococcus aureus. J Bacteriol 176: 7005-7016.
32. Loughlin, M.F., Arandhara, V., Okolie, C., Aldsworth, T.G., and Jenks, P.J. (2009) Helicobacter pylori mutants defective in the clpP ATP-dependant protease and the chaperone clpA display reduced macrophage and murine survival. Microb Pathog 46: 53-57.
33. Lourdault, K., Cerqueira, G.M., Wunder, E.A., and Picardeau, M. (2011) Inactivation of clpB in the pathogen Leptospira interrogans reduces virulence and resistance to stress conditions. Infect Immun 79: 3711-3717.
34. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
35. Marcy, Y., Ouverney, C., Bik, E.M., Losekann, T., Ivanova, N., Martin, H.G., etal. (2007) Dissecting biological 'dark matter' with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA 104: 11889-11894.
36. Markowitz, V.M., Chen, I.M.A., Palaniappan, K., Chu, K., Szeto, E., Grechkin, Y., etal. (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40: D115-D122.
37. Miura, Y., and Okabe, S. (2008) Quantification of cell specific uptake activity of microbial products by uncultured Chloroflexi by microautoradiography combined with fluorescence in situ hybridization. Environ Sci Technol 42: 7380-7386.
38. Miura, Y., Watanabe, Y., and Okabe, S. (2007) Significance of Chloroflexi in performance of submerged membrane bioreactors (MBR) treating municipal wastewater. Environ Sci Technol 41: 7787-7794.
39. Morgan, X.C., Segata, N., and Huttenhower, C. (2013) Biodiversity and functional genomics in the human microbiome. Trends Genet 29: 51-58.
40. 14C-labeled microbial products derived from nitrifying bacteria in autotrophic nitrifying biofilms. Appl Environ Microbiol 71: 3987-3994.
41. Pamp, S.J., Harrington, E.D., Quake, S.R., Relman, D.A., and Blainey, P.C. (2012) Single-cell sequencing provides clues about the host interactions of segmented filamentous bacteria (SFB). Genome Res 22: 1107-1119.
42. Paster, B.J., Boches, S.K., Galvin, J.L., Ericson, R.E., Lau, C.N., Levanos, V.A., etal. (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183: 3770-3783.
43. Plumbridge, J., and Vimr, E. (1999) Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli. J Bacteriol 181: 47-54.
44. Podar, M., Makarova, K.S., Graham, D.E., Wolf, Y.I., Koonin, E.V., and Reysenbach, A.L. (2013) 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.
45. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., etal. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
46. Richter, M., and Rossello-Mora, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106: 19126-19131.
47. Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N.N., Anderson, I.J., Cheng, J.F., etal. (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499: 431-437.
48. Roberts, I.S. (1996) The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu Rev Microbiol 50: 285-315.
49. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., etal. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
50. Smillie, C.S., Smith, M.B., Friedman, J., Cordero, O.X., David, L.A., and Alm, E.J. (2011) Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480: 241-244.
51. Stafford, G., Roy, S., Honma, K., and Sharma, A. (2012) Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast! Mol Oral Microbiol 27: 11-22.
52. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
53. Swan, B.K., Martinez-Garcia, M., Preston, C.M., Sczyrba, A., Woyke, T., Lamy, D., etal. (2011) Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333: 1296-1300.
54. Wade, W.G. (2013) The oral microbiome in health and disease. Pharmacol Res 69: 137-143.
55. Wang, R.K., Kaplan, A., Guo, L.H., Shi, W.Y., Zhou, X.D., Lux, R., and He, X.S. (2012) The influence of iron availability on human salivary microbial community composition. Microb Ecol 64: 152-161.
56. Woyke, T., Xie, G., Copeland, A., Gonzalez, J.M., Han, C., Kiss, H., etal. (2009) Assembling the marine metagenome, one cell at a time. PLoS ONE 4: e5299.
57. Yabe, S., Aiba, Y., Sakai, Y., Hazaka, M., and Yokota, A. (2010) Thermosporothrix hazakensis gen. nov., sp. nov., isolated from compost, description of Thermosporotrichaceae fam. nov. within the class Ktedonobacteria Cavaletti et al. 2007 and emended description of the class Ktedonobacteria. Int J Syst Evol Microbiol 60: 1794-1801.
58. Yamada, T., and Sekiguchi, Y. (2009) Cultivation of uncultured chloroflexi subphyla: significance and ecophysiology of formerly uncultured chloroflexi 'subphylum i' with natural and biotechnological relevance. Microbes Environ 24: 205-216.
59. Yamada, T., Sekiguchi, Y., Hanada, S., Imachi, H., Ohashi, A., Harada, H., and Kamagata, Y. (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56: 1331-1340.
60. Yoon, H.S., Price, D.C., Stepanauskas, R., Rajah, V.D., Sieracki, M.E., Wilson, W.H., etal. (2011) Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332: 714-717.
61. Zang, K., Kurisu, F., Kasuga, I., Furumai, H., and Yagi, O. (2008) Analysis of the phylogenetic diversity of estrone-degrading bacteria in activated sewage sludge using microautoradiography-fluorescence in situ hybridization. Syst Appl Microbiol 31: 206-214.
62. Zhou, Y., Gao, H., Mihindukulasuriya, K.A., Rosa, P.S., Wylie, K.M., Vishnivetskaya, T., etal. (2013) Biogeography of the ecosystems of the healthy human body. Genome Biol 14: R1.