Respiratory microbiota resistance and resilience to pulmonary exacerbation and subsequent antimicrobial intervention

ISME Journal

Volumn 10, Issue 5, 2016, Pages 1081-1091

  Cuthbertson, Leah ^a,b   Rogers, Geraint B ^c   Walker, Alan W ^d,e   Oliver, Anna ^a   Green, Laura E ^f   Daniels, Thomas W V ^g   Carroll, Mary P ^g   Parkhill, Julian ^d   Bruce, Kenneth D ^b   Van Der Gast, Christopher J ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c FLINDERS UNIVERSITY   (Australia)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e ROWETT RESEARCH INSTITUTE   (United Kingdom)

^f UNIVERSITY OF WARWICK   (United Kingdom)

^g UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIAL DISEASE; BACTERIUM; DISEASE TREATMENT; DRUG RESISTANCE; MICROBIAL COMMUNITY; RELATIVE ABUNDANCE; RESPIRATORY DISEASE; SYMPTOM;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ANTIINFECTIVE AGENT; BACTERIAL DNA; RNA 16S;

ADOLESCENT; ADULT; CHRONIC DISEASE; COMPLICATION; CYSTIC FIBROSIS; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LUNG; MALE; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; PATHOPHYSIOLOGY; PSEUDOMONAS AERUGINOSA; RESPIRATORY TRACT INFECTION; SPUTUM; YOUNG ADULT;

ADOLESCENT; ADULT; ANTI-BACTERIAL AGENTS; CHRONIC DISEASE; CYSTIC FIBROSIS; DNA, BACTERIAL; FEMALE; HUMANS; LUNG; MALE; MICROBIOTA; MIDDLE AGED; PSEUDOMONAS AERUGINOSA; RESPIRATORY TRACT INFECTIONS; RNA, RIBOSOMAL, 16S; SPUTUM; YOUNG ADULT;

EID: 84946771265     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.198     Document Type: Article

References (42)

1. Allison SD, Martiny JBH. (2008). Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105: 11512-11519.
2. Brown JH, Kodric-Brown A. (1977). Turnover rates in insular biogeography: effect of immigration and extinction. Ecology 58: 445-449.
3. Carmody LA, Zhao J, Schloss PD, Petrosino JF, Murray S, Young VB et al. (2013). Changes in cystic fibrosis airway microbiota at pulmonary exacerbation. Ann Am Thorac Soc 10: 179-187.
4. Chen AI, Dolben EF, Okegbe C, Harty CE, Golub Y, Thao S et al. (2014). Candida albicans ethanol stimulates Pseudomonas aeruginosa WspR-controlled biofilm formation as part of a cyclic relationship involving phenazines. PLoS Pathog 10: e1004480.
5. Cooper P, Walker AW, Reyes J, Chico M, Salter SJ, Vaca M et al. (2013). Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE 8: e76573.
6. Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA et al. (2010). Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS ONE 5: e11044.
7. Cuthbertson L, Rogers GB, Walker AW, Oliver A, Hafiz T, Hoffman LR et al. (2014). Time between collection and storage significantly influences bacterial sequence composition in sputum samples from cystic fibrosis respiratory infections. J Clin Microbiol 52: 3011-3016.
8. Daniels TWV, Rogers GB, Stressmann FA, van der Gast CJ, Bruce KD, Jones GR et al. (2013). Impact of antibiotic treatment for pulmonary exacerbations on bacterial diversity in cystic fibrosis. J Cyst Fibros 12: 22-28.
9. Davies JC, Ebdon A-M, Orchard C. (2014). Recent advances in the management of cystic fibrosis. Arch Dis Child 11: 1033-1036.
10. Flume PA, Mogayzel PJ, Robinson KA, Goss CH, Rosenblatt RL, Kuhn RJ et al. (2009). Cystic fibrosis pulmonary guidelines. Am J Respir Crit Care Med 180: 802-808.
11. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM et al. (2012). The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS ONE 7: e45001.
12. Foweraker J. (2009). Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. Br Med Bull 89: 93-110.
13. Fuchs HJ, Borowitz DS, Christiansen DH, Morris EM, Nash ML, Ramsey BW et al. (1994). Effect of aerosolized recombinant human DNase on exacerbations of respiratory symptoms and on pulmonary function in patients with cystic fibrosis. New Engl J Med 331: 637-642.
14. Hedin C, van der Gast CJ, Rogers GB, Cuthbertson L, McCartney S, Stagg AJ et al. (2015). Siblings of patients with Crohn's disease exhibit a biologically relevant dysbiosis in mucosal microbial meta-communities. Gut; e-pub ahead of print 8 April 2015; doi:10.1136/gutjnl-2014-308896.
15. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, Knapp AA et al. (2010). Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol 12: 1293-1303.
16. Korgaonkar A, Trivedi U, Rumbaugh KP, Whiteley M. (2013). Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc Natl Acad Sci USA 110: 1059-1064.
17. LiPuma JJ. (2014). Expanding our understanding of respiratory microbiota in cystic fibrosis. Ann Am Thorac Soc 11: 1084-1085.
18. Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. (2013). Package Vegan: Community Ecology Package. R package version 2.0-7. R Foundation for Statistical Computing: Vienna, Austria.
19. Pattison SH, Rogers GB, Crockard M, Elborn JS, Tunney MM. (2013). Molecular detection of CF lung pathogens: current status and future potential. J Cyst Fibros 12: 194-205.
20. Price K, Hampton T, Gifford A, Dolben E, Hogan D, Morrison H et al. (2013). Unique microbial communities persist in individual cystic fibrosis patients throughout a clinical exacerbation. Microbiome 1: 27.
21. Quince C, Lanzen A, Davenport R, Turnbaugh P. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
22. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Kehagia V et al. (2006). Use of 16S rRNA gene profiling by terminal restriction fragment length polymorphism analysis to compare bacterial communities in sputum and mouthwash samples from patients with cystic fibrosis. J Clin Microbiol 44: 2601-2604.
23. Rogers GB, Cuthbertson L, Hoffman LR, Wing PAC, Pope C, Hooftman DAP et al. (2013). Reducing bias in bacterial community analysis of lower respiratory infections. ISME J 7: 697-706.
24. Rosenfeld M, Emerson J, Williams-Warren J, Pepe M, Smith A, Montgomery AB et al. (2001). Defining a pulmonary exacerbation in cystic fibrosis. J Pediatr 139: 359-365.
25. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF et al. (2014). Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12: 87.
26. Sanders DB, Bittner RCL, Rosenfeld M, Hoffman LR, Redding GJ, Goss CH. (2010). Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med 182: 627-632.
27. Schloss PD, Handelsman J. (2006). Toward a census of bacteria in soil. PLoS Comput Biol 2: e92.
28. Schloss PD, Gevers D, Westcott SL. (2011). Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6: e27310.
29. Sherrard LJ, Tunney MM, Elborn JS. (2014). Antimicrobial resistance in the respiratory microbiota of people with cystic fibrosis. Lancet 384: 703-713.
30. Sibley CD, Parkins MD, Rabin HR, Duan K, Norgaard JC, Surette MG. (2008). A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci USA 105: 15070-15075.
31. Smith DJ, Badrick AC, Zakrzewski M, Krause L, Bell SC, Anderson GJ et al. (2014). Pyrosequencing reveals transient cystic fibrosis lung microbiome changes with intravenous antibiotics. Eur Respir J 44: 922-930.
32. Smyth A, Elborn JS. (2008). Exacerbations in cystic fibrosis: 3. Management. Thorax 63: 180-184.
33. Stressmann FA, Rogers GB, van der Gast CJ, Marsh P, Vermeer LS, Carroll MP et al. (2012). Long-term cultivation-independent microbial diversity analysis demonstrates that bacterial communities infecting the adult cystic fibrosis lung show stability and resilience. Thorax 67: 867-873.
34. Stressmann FA, Rogers GB, Marsh P, Lilley AK, Daniels TWV, Carroll MP et al. (2011). Does bacterial density in cystic fibrosis sputum increase prior to pulmonary exacerbation? J Cyst Fibros 10: 357-365.
35. The R Development Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.
36. van der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW et al. (2011). Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J 5: 780-791.
37. van der Gast CJ, Cuthbertson L, Rogers GB, Pope C, Marsh RL, Redding GJ et al. (2014). Three clinically distinct chronic pediatric airway infections share a common core microbiota. Ann Am Thorac Soc 11: 1039-1048.
38. VanDevanter DR, Elkin EP, Pasta DJ, Morgan WJ, Konstan MW. (2013). Changing thresholds and incidence of antibiotic treatment of cystic fibrosis pulmonary exacerbations, 1995-2005. J Cyst Fibros 12: 332-337.
39. Venkataraman A, Rosenbaum MA, Werner JJ, Winans SC, Angenent LT. (2014). Metabolite transfer with the fermentation product 2, 3-butanediol enhances virulence by Pseudomonas aeruginosa. ISME J 8: 1210-1220.
40. Whiteson KL, Meinardi S, Lim YW, Schmieder R, Maughan H, Quinn R et al. (2014). Breath gas metabolites and bacterial metagenomes from cystic fibrosis airways indicate active pH neutral 2, 3-butane-dione fermentation. ISME J 8: 1247-1258.
41. Zemanick ET, Harris JK, Wagner BD, Robertson CE, Sagel SD, Stevens MJ et al. (2013). Inflammation and airway microbiota during cystic fibrosis pulmonary exacerbations. PLoS ONE 8: e62917.
42. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF et al. (2012). Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA 109: 5809-5814.