Abundant dnase I-sensitive bacterial DNA in healthy porcine lungs and its implications for the lung microbiome

Applied and Environmental Microbiology

Volumn 79, Issue 19, 2013, Pages 5936-5941

  Pezzulo, Alejandro A ^a   Kelly, Patrick H ^a   Nassar, Boulos S ^a   Rutland, Cedric J ^a   Gansemer, Nicholas D ^a   Dohrn, Cassie L ^a   Costello, Andrew J ^a   Stoltz, David A ^a   Zabnera, Joseph ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCING; BACTERIAL ABUNDANCE; BACTERIAL DIVERSITY; CONCEPTUAL FRAMEWORKS; HOST DEFENSE; IMMUNE MECHANISM; LUNG TISSUE; MICROBIAL ANALYSIS;

BACTERIA; BIOLOGICAL ORGANS; DNA; DNA SEQUENCES; RNA;

GENE ENCODING;

ABUNDANCE; BIOME; DISEASE PREVALENCE; DNA; DOMINANCE; ENZYME ACTIVITY; IMMUNE RESPONSE; MICROBIAL COMMUNITY; PIG;

BACTERIAL DNA; DEOXYRIBONUCLEASE I;

ANIMAL; ARTICLE; BACTERIAL LOAD; BIODIVERSITY; GENETICS; LUNG; LUNG LAVAGE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MICROFLORA; SWINE;

ANIMALS; BACTERIAL LOAD; BIODIVERSITY; BRONCHOALVEOLAR LAVAGE FLUID; DEOXYRIBONUCLEASE I; DNA, BACTERIAL; LUNG; MICROBIAL VIABILITY; MICROBIOTA; SWINE;

EID: 84884178416     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01752-13     Document Type: Article

References (46)

1. Jager E, Ruden H, Zeschmar-Lahl B. 1994. Composting facilities. 2. Aerogenic microorganism content at different working areas of composting facilities. Zentralbl. Hyg. Umweltmed. 196:367-379.
2. Tsai FC, Macher JM. 2005. Concentrations of airborne culturable bacteria in 100 large US office buildings from the BASE study. Indoor Air 15:71-81.
3. Johanson WG, Pierce AK, Sanford JP. 1969. Changing pharyngeal bacterial flora of hospitalized patients. Emergence of gram-negative bacilli. N. Engl. J. Med. 281:1137-1140.
4. Jones FS. 1922. The source of the microorganisms in the lungs of normal animals. J. Exp. Med. 36:317-328.
5. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, Bushman FD, Collman RG. 2011. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am. J. Respir. Crit. Care Med. 184:957-963.
6. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, Young VB, Toews GB, Curtis JL, Sundaram B, Martinez FJ, Huffnagle GB. 2011. Analysis of the lung microbiome in the "healthy" smoker and in COPD. PLoS One 6:e16384. doi:10.1371/journal.pone.0016384.
7. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, Moffatt MF, Cookson WO. 2010. Disordered microbial communities in asthmatic airways. PLoS One 5:e8578. doi:10.1371/journal.pone.0008578.
8. Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Karaoz U, Andersen GL, Brown R, Fujimura KE, Wu B, Tran D, KoffJ, Kleinhenz ME, Nielson D, Brodie EL, Lynch SV. 2010. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 5:e11044. doi:10.1371/journal.pone.0011044.
9. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, Cavalcoli JD, Vandevanter DR, Murray S, Li JZ, Young VB, Lipuma JJ. 2012. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc. Natl. Acad. Sci. U. S. A. 109:5809-5814.
10. Huang YJ, Kim E, Cox MJ, Brodie EL, Brown R, Wiener-Kronish JP, Lynch SV. 2010. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS 14:9-59.
11. Huang YJ, Nelson CE, Brodie EL, Desantis TZ, Baek MS, Liu J, Woyke T, Allgaier M, Bristow J, Wiener-Kronish JP, Sutherland ER, King TS, Icitovic N, Martin RJ, Calhoun WJ, Castro M, Denlinger LC, Dimango E, Kraft M, Peters SP, Wasserman SI, Wechsler ME, Boushey HA, Lynch SV. 2011. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J. Allergy Clin. Immunol. 127:372-381.
12. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, Knapp AA, Lory S, Brodie EL, Lynch SV, Bohannan BJ, Green JL, Maurer BA, Kolter R. 2010. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ. Microbiol. 12:1293-1303.
13. Willner D, Haynes MR, Furlan M, Schmieder R, Lim YW, Rainey PB, Rohwer F, Conrad D. 2012. Spatial distribution of microbial communities in the cystic fibrosis lung. ISME J. 6:471-474.
14. Klein DA. 2011. Bulk extraction-based microbial ecology: three critical questions. Microbe 6:377.
15. Chastre J, Fagon JY, Domart Y, Gibert C. 1989. Diagnosis of nosocomial pneumonia in intensive care unit patients. Eur. J. Clin. Microbiol. Infect. Dis. 8:35-39.
16. Torres A, el-Ebiary M, Padro L, Gonzalez J, de la Bellacasa JP, Ramirez J, Xaubet A, Ferrer M, Rodriguez-Roisin R. 1994. Validation of different techniques for the diagnosis of ventilator-associated pneumonia. Comparison with immediate postmortem pulmonary biopsy. Am. J. Respir. Crit. Care Med. 149:324-331.
17. Heyland D, Ewig S, Torres A. 2002. Pro/con clinical debate: the use of a protected specimen brush in the diagnosis of ventilator associated pneumonia. Crit. Care 6:117-120.
18. Torres A, Puig de la Bellacasa J, Xaubet A, Gonzalez J, Rodriguez-Roisin R, Jimenez de Anta MT, Agusti Vidal A. 1989. Diagnostic value of quantitative cultures of bronchoalveolar lavage and telescoping plugged catheters in mechanically ventilated patients with bacterial pneumonia. Am. Rev. Respir. Dis. 140:306-310.
19. Chastre J, Fagon JY, Soler P, Bornet M, Domart Y, Trouillet JL, Gibert C, Hance AJ. 1988. Diagnosis of nosocomial bacterial pneumonia in intubated patients undergoing ventilation: comparison of the usefulness of bronchoalveolar lavage and the protected specimen brush. Am. J. Med. 85:499-506.
20. Chastre J, Viau F, Brun P, Pierre J, Dauge MC, Bouchama A, Akesbi A, Gibert C. 1984. Prospective evaluation of the protected specimen brush for the diagnosis of pulmonary infections in ventilated patients. Am. Rev. Respir. Dis. 130:924-929.
21. Busse WW, Wanner A, Adams K, Reynolds HY, Castro M, Chowdhury B, Kraft M, Levine RJ, Peters SP, Sullivan EJ. 2005. Investigative bronchoprovocation and bronchoscopy in airway diseases. Am. J. Respir. Crit. Care Med. 172:807-816.
22. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919-1925.
23. Murray PR, Baron EK, Jorgensen JH, Landry ML, Pfaller MA (ed). 2007. Manual of clinical microbiology, 9th ed. American Society for Microbiology, Washington, DC.
24. Fierer N, Hamady M, Lauber CL, Knight R. 2008. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc. Natl. Acad. Sci. U. S. A. 105:17994-17999.
25. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336.
26. Motulsky H. 1995. Intuitive biostatistics. Oxford University Press, New York, NY.
27. Rice KC, Bayles KW. 2008. Molecular control of bacterial death and lysis. Microbiol. Mol. Biol. Rev. 72:85-109.
28. Mulcahy H, Charron-Mazenod L, Lewenza S. 2010. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ. Microbiol. 12:1621-1629.
29. Nijland R, Hall MJ, Burgess JG. 2010. Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS One 5:e15668. doi:10.1371/journal.pone.0015668.
30. Tetz VV, Tetz GV. 2010. Effect of extracellular DNA destruction by DNase I on characteristics of forming biofilms. DNA Cell Biol. 29:399-405.
31. Allander T, Emerson SU, Engle RE, Purcell RH, Bukh J. 2001. A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. Proc. Natl. Acad. Sci. U. S. A. 98:11609-11614.
32. Mahesha L, Sigera NN, Rakshit SK. 2007. The effect of DNaseI enzyme on food pathogens subjected to different food processing treatments. J. Natl. Sci. Found. Sri Lanka 35:167-173.
33. Mukhopadhyay UK, Mukhopadhyay A. 2002. A low-cost, rapid, sensitive and reliable PCR-based alternative method for predicting the presence of possible live microbial contaminants in food. Curr. Sci. 83:53-56.
34. Dickson RP, Erb-Downward JR, Huffnagle GB. 2013. The role of the bacterial microbiome in lung disease. Expert Rev. Respir. Med. 7:245-257.
35. Huang YJ, Charlson ES, Collman RG, Colombini-Hatch S, Martinez FD, Senior RM. 2013. The role of the lung microbiome in health and disease. A National Heart, Lung, and Blood Institute workshop report. Am. J. Respir. Crit. Care Med. 187:1382-1387.
36. Goddard AF, Staudinger BJ, Dowd SE, Joshi-Datar A, Wolcott RD, Aitken ML, Fligner CL, Singh PK. 2012. Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota. Proc. Natl. Acad. Sci. U. S. A. 109:13769-13774.
37. Borewicz K, Pragman AA, Kim HB, Hertz M, Wendt C, Isaacson RE. 2013. Longitudinal analysis of the lung microbiome in lung transplantation. FEMS Microbiol. Lett. 339:57-65.
38. Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, Cooper J, Sin DD, Mohn WW, Hogg JC. 2012. The lung tissue microbiome in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 185:1073-1080.
39. Larsen JM, Steen-Jensen DB, Laursen JM, Sondergaard JN, Musavian HS, Butt TM, Brix S. 2012. Divergent pro-inflammatory profile of human dendritic cells in response to commensal and pathogenic bacteria associated with the airway microbiota. PLoS One 7:e31976. doi:10.1371/journal.pone.0031976.
40. Segal LN, Alekseyenko AV, Clemente JC, Kulkarni R, Wu B, Chen H, Berger KI, Goldring RM, Rom WN, Blaser MJ, Weiden MD. 2013. Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation. Microbiome 1:19. doi:10.1186/2049-2618-1-19.
41. Rosenecker J, Naundorf S, Rudolph C. 2009. Airway surface liquid contains endogenous DNase activity which can be activated by exogenous magnesium. Eur. J. Med. Res. 14:304-308.
42. Lethem MI, James SL, Marriott C, Burke JF. 1990. The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur. Respir. J. 3:19-23.
43. Jones AP, Wallis C. 2010. Dornase alfa for cystic fibrosis. Cochrane Database Syst. Rev. 17:CD001127. doi:10.1002/14651858.CD001127.pub2.
44. Konstan MW, Wagener JS, Pasta DJ, Millar SJ, Jacobs JR, Yegin A, Morgan WJ. 2011. Clinical use of dornase alpha is associated with a slower rate of FEV1 decline in cystic fibrosis. Pediatr. Pulmonol. 46:545-553.
45. Shak S, Capon DJ, Hellmiss R, Marsters SA, Baker CL. 1990. Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc. Natl. Acad. Sci. U. S. A. 87:9188-9192.
46. Knuefermann P, Baumgarten G, Koch A, Schwederski M, Velten M, Ehrentraut H, Mersmann J, Meyer R, Hoeft A, Zacharowski K, Grohe C. 2007. CpG oligonucleotide activates Toll-like receptor 9 and causes lung inflammation in vivo. Respir. Res. 8:72. doi:10.1186/1465-9921-8-72.