Culture enriched molecular profiling of the cystic fibrosis airway microbiome

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Sibley, Christopher D ^a   Grinwis, Margot E ^a   Field, Tyler R ^a   Eshaghurshan, Christina S ^a   Faria, Monica M ^a   Dowd, Scot E ^c,d   Parkins, Michael D ^a,b   Rabin, Harvey R ^a,b   Surette, Michael G ^a,e  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c Medical Biofilm Research Institute Lubbock   (United States)

^d Research and Testing Laboratory of the South Plains   (United States)

^e MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ACIDAMINOCOCCACEAE; ACTINOBACTERIA; ACTINOMYCETACEAE; ANAEROBIC CELL CULTURE; ANAEROBIC GROWTH; ARTICLE; BACILLALES; BACTERIUM CULTURE; BACTERIUM ISOLATE; BACTEROIDETES; BURKHOLDERIA; CARNOBACTERIACEAE; CLINICAL ARTICLE; CLOSTRIDIACEAE; CLOSTRIDIALES; COLONY FORMATION; CORIOBACTERIACEAE; CULTURE MEDIUM; ENTEROBACTERIACEAE; EUBACTERIACEAE; FIRMICUTES; FUSOBACTERIA; GENE SEQUENCE; HAEMOPHILUS; HUMAN; INCUBATION TIME; LACTOBACILLACEAE; LUNG FIBROSIS; MICROBIAL COMMUNITY; MICROBIOME; MICROCOCCACEAE; MYCOBACTERIUM; NOCARDIACEAE; PLANOCOCCACEAE; PREVOTELLACEAE; PROPIONIBACTERIACEAE; PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA; PYROSEQUENCING; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RHIZOBIACEAE; SENSITIVITY ANALYSIS; SPUTUM ANALYSIS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS; BACTERIUM; CLASSIFICATION; CYSTIC FIBROSIS; DNA BARCODING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METAGENOME; MICROBIOLOGY; RESPIRATORY SYSTEM; SPUTUM;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

BACTERIA; CYSTIC FIBROSIS; DNA BARCODING, TAXONOMIC; HUMANS; METAGENOME; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RESPIRATORY SYSTEM; RNA, RIBOSOMAL, 16S; SPUTUM;

EID: 79960886859     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022702     Document Type: Article

References (86)

1. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, et al. (1998) Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
2. Accurso FJ, (1997) Early pulmonary disease in cystic fibrosis. Curr Opin Pulm Med 3: 400-403.
3. Miller MB, Gilligan PH, (2003) Laboratory aspects of management of chronic pulmonary infections in patients with cystic fibrosis. J Clin Microbiol 41: 4009-4015.
4. Lipuma JJ, (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23: 299-323.
5. Rogers GB, Carroll MP, Bruce KD, (2009) Studying bacterial infections through culture-independent approaches. J Med Microbiol 58: 1401-1418.
6. Harris JK, De Groote MA, Sagel SD, Zemanick ET, Kapsner R, et al. (2007) Molecular identification of bacteria in bronchoalveolar lavage fluid from children with cystic fibrosis. Proc Natl Acad Sci U S A 104: 20529-20533.
7. Bittar F, Richet H, Dubus JC, Reynaud-Gaubert M, Stremler N, et al. (2008) Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS ONE 3: e2908.
8. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, et al. (2004) Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16S ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 42: 5176-5183.
9. Rogers GB, Hart CA, Mason JR, Hughes M, Walshaw MJ, et al. (2003) Bacterial diversity in cases of lung infection in cystic fibrosis patients: 16S ribosomal DNA (rDNA) length heterogeneity PCR and 16S rDNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 41: 3548-3558.
10. Sibley CD, Parkins MD, Rabin HR, Duan K, Norgaard JC, et al. (2008) A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A 105: 15070-15075.
11. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, et al. (2010) Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol.
12. Kolak M, Karpati F, Monstein HJ, Jonasson J, (2003) Molecular typing of the bacterial flora in sputum of cystic fibrosis patients. Int J Med Microbiol 293: 309-317.
13. Ecker DJ, Sampath R, Massire C, Blyn LB, Hall TA, et al. (2008) Ibis T5000: a universal biosensor approach for microbiology. Nat Rev Microbiol 6: 553-558.
14. Rogers GB, Daniels TW, Tuck A, Carroll MP, Connett GJ, et al. (2009) Studying bacteria in respiratory specimens by using conventional and molecular microbiological approaches. BMC Pulm Med 9: 14.
15. Sibley CD, Rabin H, Surette MG, (2006) Cystic fibrosis: a polymicrobial infectious disease. Future Microbiol 1: 53-61.
16. Parkins MD, Sibley CD, Surette MG, Rabin HR, (2008) The Streptococcus milleri group-an unrecognized cause of disease in cystic fibrosis: a case series and literature review. Pediatr Pulmonol 43: 490-497.
17. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, et al. (2008) Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med 177: 995-1001.
18. Raoult D, Fournier PE, Drancourt M, (2004) What does the future hold for clinical microbiology? Nat Rev Microbiol 2: 151-159.
19. Woese CR, Fox GE, (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci of the U S A 74: 5088-5090.
20. Pace NR, Stahl DA, Lane DJ, Olsen GJ, (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv in Microb Ecol 9: 1-55.
21. Ward DM, Weller R, Bateson MM, (1990) 16S ribosomal RNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345: 63-65.
22. Amann RI, Ludwig W, Schleifer KH, (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
23. Rappe MS, Giovannoni SJ, (2003) The uncultured microbial majority. Ann Rev Microbiol 57: 369-394.
24. Keller M, Zengler K, (2004) Tapping into microbial diversity. Nat Rev Microbiol 2: 141-150.
25. Hugenholtz P, Tyson GW, (2008) Microbiology- Metagenomics. Nature 455: 481-483.
26. Alain K, Querellou J, (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13: 583-594.
27. Staley JT, Konopka A, (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Ann Rev Microbiol 39: 321-346.
28. Socransky SS, Gibbons RJ, Dale AC, Bortnick L, Rosenthal E, et al. (1963) The microbiota of the gingival crevice area of man - I: Total microscopic and viable counts and counts of specific organisms. Arch Oral Biol 8: 275-280.
29. Gordon DF, Stutman M, Loesche WJ, (1971) Improved isolation of anaerobic bacteria from gingival crevice area of man. Appl Microbiol 21: 1046-1050.
30. Moore WEC, Holdeman LV, (1974) Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl Microbiol 27: 961-979.
31. Wilson KH, Blitchington RB, (1996) Human colonic biota studied by ribosomal DNA sequence analysis. Appl Environ Microbiol 62: 2273-2278.
32. Gilligan PH, Kiska DL, Appleman MD, (2006) Cumitech: cystic fibrosis microbiology Washington, D.C.
33. Kopke B, Wilms R, Engelen B, Cypionka H, Sass H, (2005) Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol 71: 7819-7830.
34. Finegold SM, Sutter VL, Mathison GE, (1983) Normal indigenous flora. In: Hentges DJ, editors. Human intestinal microflora in health and disease New York Academic Press pp. 3-31.
35. Moore WE, Moore LV, (1994) The bacteria of periodontal diseases. Periodontol 2000 5: 66-77.
36. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, et al. (2007) The human microbiome project. Nature 449: 804-810.
37. Achtman M, Wagner M, (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6: 431-440.
38. Stackebrandt E, Goebel BM, (1994) A place for DNA-DNA reassociation and 16S ribosomal RNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846-849.
39. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, et al. (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37-43.
40. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
41. Facklam R, (2002) What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev 15: 613-630.
42. Kawamura Y, Hou XG, Sultana F, Miura H, Ezaki T, (1995) Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Bacteriol 45: 406-408.
43. Kaeberlein T, Lewis K, Epstein SS, (2002) Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment. Science 296: 1127-1129.
44. D'Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, et al. (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17: 254-264.
45. Liu WT, Marsh TL, Cheng H, Forney LJ, (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516-4522.
46. Flint HJ, Duncan SH, Scott KP, Louis P, (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol 9: 1101-1111.
47. Watve M, Shejval V, Sonawane C, Rahalkar M, Matapurkar A, et al. (2000) The 'K' selected oligophilic bacteria: A key to uncultured diversity? Current Science 78: 1535-1542.
48. Leadbetter JR, (2003) Cultivation of recalcitrant microbes: cells are alive, well and revealing their secrets in the 21st century laboratory. Curr Opin Microbiol 6: 274-281.
49. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, et al. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
50. Sait M, Hugenholtz P, Janssen PH, (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4: 654-666.
51. Tu O, Knott T, Marsh M, Bechtol K, Harris D, et al. (1998) The influence of fluorescent dye structure on the electrophoretic mobility of end-labeled DNA. Nucleic Acids Research 26: 2797-2802.
52. Kaplan CW, Kitts CL, (2003) Variation between observed and true Terminal Restriction Fragment length is dependent on true TRF length and purine content. J Microbiol Methods 54: 121-125.
53. Schutte UME, Abdo Z, Bent SJ, Shyu C, Williams CJ, et al. (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 80: 365-380.
54. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
55. Dethlefsen L, Huse S, Sogin ML, Relman DA, (2008) The Pervasive Effects of an Antibiotic on the Human Gut Microbiota, as Revealed by Deep 16S rRNA Sequencing. PLoS Biology 6: 2383-2400.
56. Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, et al. (2010) Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J.
57. Manganiello AD, Socransky SS, Smith C, Propas D, Oram V, et al. (1977) Attempts to increase viable count recovery of human supragingival dental plaque. J Periodontal Res 12: 107-119.
58. Qin JJ, Li RQ, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-U70.
59. Ingham CJ, Sprenkels A, Bomer J, Molenaar D, van den Berg A, et al. (2007) The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc Natl Acad Sci U S A 104: 18217-18222.
60. Zengler K, Toledo G, Rappe M, Elkins J, Mathur EJ, et al. (2002) Cultivating the uncultured. Proc Natl Acad Sci U S A 99: 15681-15686.
61. Zengler K, (2009) Central role of the cell in microbial ecology. Microbiol Mol Biol Rev 73: 712-729.
62. Sibley CD, Grinwis M, Field TR, Parkins MD, Noorgard JC, et al. (2010) McKay Agar Enables Routine Quantification of the Streptococcus milleri Group in Cystic Fibrosis Patients. J Med Microbiol 48: 2592-2594.
63. Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, et al. (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6: 639-641.
64. Reeder J, Knight R, (2009) The 'rare biosphere': a reality check. Nat Methods 6: 636-637.
65. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P, (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118-123.
66. Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, et al. (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci U S A.
67. Muyzer G, Teske A, Wirsen CO, Jannasch HW, (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165-172.
68. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261-5267.
69. Huang Y, Niu B, Gao Y, Fu L, Li W, (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680-682.
70. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
71. DeSantis TZ Jr, Hugenholtz P, Keller K, Brodie EL, Larsen N, et al. (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34: W394-399.
72. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
73. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
74. Callaway TR, Dowd SE, Wolcott RD, Sun Y, McReynolds JL, et al. (2009) Evaluation of the bacterial diversity in cecal contents of laying hens fed various molting diets by using bacterial tag-encoded FLX amplicon pyrosequencing. Poult Sci 88: 298-302.
75. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, et al. (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 125.
76. Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, et al. (2008) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8: 43.
77. Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA, (2008) Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis 5: 459-472.
78. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, et al. (2008) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3: e3326.
79. Leake JL, Dowd SE, Wolcott RD, Zischkau AM, (2009) Identification of yeast in chronic wounds using new pathogen-detection technologies. J Wound Care 18: 103-104, 106, 108.
80. Suchodolski JS, Dowd SE, Westermarck E, Steiner JM, Wolcott RD, et al. (2009) The effect of the macrolide antibiotic tylosin on microbial diversity in the canine small intestine as demonstrated by massive parallel 16S rRNA gene sequencing. BMC Microbiol 9: 210.
81. Wolcott RD, Gontcharova V, Sun Y, Zischakau A, Dowd SE, (2009) Bacterial diversity in surgical site infections: not just aerobic cocci any more. J Wound Care 18: 317-323.
82. Wolcott RD, Gontcharova V, Sun Y, Dowd SE, (2009) Evaluation of the bacterial diversity among and within individual venous leg ulcers using bacterial tag-encoded FLX and titanium amplicon pyrosequencing and metagenomic approaches. BMC Microbiol 9: 226.
83. Dowd SE, Zaragoza J, Rodriguez JR, Oliver MJ, Payton PR, (2005) Windows. NET Network Distributed Basic Local Alignment Search Toolkit (W.ND-BLAST). BMC Bioinformatics 6: 93.
84. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-145.
85. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
86. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, et al. (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33: D294-296.