Linking microbiota and respiratory disease

FEBS Letters

Volumn 590, Issue 21, 2016, Pages 3721-3738

  Hauptmann, Matthias ^a   Schaible, Ulrich E ^a,b  

^a Research Center Borstel   (Germany)

^b German Centre for Infection Research TTU TB   (Germany)

Author keywords

commensal bacteria; epithelial barrier function; gut lung axis; microbiome; microbiota; pulmonary immunology

Indexed keywords

RNA 16S;

ADAPTIVE IMMUNITY; ALLERGY; ASTHMA; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMMENSAL MICROECOLOGY; COMMENSALISM; COMORBIDITY; CYSTIC FIBROSIS; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT; GENE SEQUENCE; HEALTH; HOST PATHOGEN INTERACTION; HUMAN; IMMUNITY; IMMUNOREGULATION; INNATE IMMUNITY; INTESTINE FLORA; LUNG MICROBIOTA; MICROBIAL COMMUNITY; MICROFLORA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOPHYSIOLOGY; POPULATION ABUNDANCE; PRIORITY JOURNAL; PULMONARY HEALTH; PULMONARY IMMUNITY; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT INFECTION; REVIEW; RNA GENE; SPECIES COMPOSITION; BACTERIUM IDENTIFICATION; IMMUNOLOGY; INTESTINE; LUNG; MICROBIOLOGY; PROCEDURES;

BACTERIAL TYPING TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; LUNG; MICROBIOTA; RESPIRATORY TRACT INFECTIONS;

EID: 84995520600     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12421     Document Type: Review

References (167)

1. Brown RL and Clarke TB (2016) The regulation of host defences to infection by the microbiota. Immunology doi: 10.1111/imm.12634.
2. Barfod KK, Roggenbuck M, Hansen LH, Schjorring S, Larsen ST, Sorensen SJ and Krogfelt KA (2013) The murine lung microbiome in relation to the intestinal and vaginal bacterial communities. BMC Microbiol 13, 303.
3. Glendinning L, Wright S, Pollock J, Tennant P, Collie D and McLachlan G (2016) Variability of the sheep lung microbiota. Appl Environ Microbiol 82, 3225–3238.
4. Yun Y, Srinivas G, Kuenzel S, Linnenbrink M, Alnahas S, Bruce KD, Steinhoff U, Baines JF and Schaible UE (2014) Environmentally determined differences in the murine lung microbiota and their relation to alveolar architecture. PLoS One 9, e113466.
5. Ericsson AC, Personett AR, Grobman ME, Rindt H and Reinero CR (2016) Composition and predicted metabolic capacity of upper and lower airway microbiota of healthy dogs in relation to the fecal microbiota. PLoS One 11, e0154646.
6. Morris A, Paulson JN, Talukder H, Tipton L, Kling H, Cui L, Fitch A, Pop M, Norris KA and Ghedin E (2016) Longitudinal analysis of the lung microbiota of cynomolgous macaques during long-term SHIV infection. Microbiome 4, 38.
7. Madan J, Koestler D, Stanton B, Davidson L, Moulton L, Housman M, Moore J, Guill MF, Morrison H and Sogin M (2012) Serial analysis of the gut and respiratory microbiome in cystic fibrosis in infancy: interaction between intestinal and respiratory tracts and impact of nutritional exposures. mBio 3, e00251–e00212.
8. Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM, Young VB, Beck JM, Curtis JL and Huffnagle GB (2015) Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. mbio 6, e00037–e00015.
9. Sin D, Sze M and Hogg J (2014) Bacterial microbiome of lungs in COPD. Int J Chron Obstruct Pulmon Dis 9, 229–238.
10. Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, Cooper J, Sin DD, Mohn WW and Hogg JC (2012) The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 185, 1073–1080.
11. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, Bushman FD and Collman RG (2011) Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184, 957–963.
12. Gollwitzer ES, Saglani S, Trompette A, Yadava K, Sherburn R, McCoy KD, Nicod LP, Lloyd CM and Marsland BJ (2014) Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat Med 20, 642–647.
13. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM et al. (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO rep 13, 440–447.
14. Russell SL, Gold MJ, Willing BP, Thorson L, McNagny KM and Finlay BB (2013) Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes 4, 158–164.
15. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL et al. (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20, 159–166.
16. Clarke TB (2014) Early innate immunity to bacterial infection in the lung is regulated systemically by the commensal microbiota via Nod-like receptor ligands. Infect Immun 82, 4596–4606.
17. Vieira AT, Rocha VM, Tavares L, Garcia CC, Teixeira MM, Oliveira SC, Cassali GD, Gamba C, Martins FS and Nicoli JR (2016) Control of Klebsiella pneumoniae pulmonary infection and immunomodulation by oral treatment with the commensal probiotic Bifidobacterium longum 51A. Microbes Infect 18, 180–189.
18. Schuijt TJ, Lankelma JM, Scicluna BP, de Sousa e Melo F, Roelofs JJTH, de Boer JD, Hoogendijk AJ, de Beer R, de Vos A, Belzer C et al. (2016) The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut 65, 575–583.
19. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WOCM, Braun-Fahrländer C, Heederik D, Piarroux R and von Mutius E (2011) Exposure to environmental microorganisms and childhood asthma. N Engl J Med 364, 701–709.
20. Bach JF and Chatenoud L (2012) The hygiene hypothesis: an explanation for the increased frequency of insulin-dependent diabetes. Cold Spring Harb Perspect Med 2, a007799.
21. Spor A, Koren O and Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9, 279–290.
22. Thorpe JE, Baughman RP, Frame PT, Wesseler TA and Staneck JL (1987) Bronchoalveolar lavage for diagnosing acute bacterial pneumonia. J Infect Dis 155, 855–861.
23. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, Muhlebach MS, Wolfgang MC, Boucher R, Gilpin DF, McDowell A 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.
24. Goddard AF, Staudinger BJ, Dowd SE, Joshi-Datar A, Wolcott RD, Aitken ML, Fligner CL and 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 USA 109, 13769–13774.
25. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Kehagia V, Connett GJ and Bruce KD (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.
26. Baselski VS and Wunderink RG (1994) Bronchoscopic diagnosis of pneumonia. Clin Microbiol Rev 7, 533–558.
27. Charlson ES, Bittinger K, Chen J, Diamond JM, Li H, Collman RG and Bushman FD (2012) Assessing bacterial populations in the lung by replicate analysis of samples from the upper and lower respiratory tracts. PLoS One 7, e42786.
28. Rose AS and Knox KS (2007) Bronchoalveolar Lavage as a Research Tool. Semin Respir Crit Care Med 28, 561–574.
29. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB and Curtis JL (2015) Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc 12, 821–830.
30. McNally L and Brown SP (2015) Building the microbiome in health and disease: niche construction and social conflict in bacteria. Philos Trans R Soc Lond B Biol Sci 370, 20140298.
31. Jorth P, Staudinger BJ, Wu X, Hisert KB, Hayden H, Garudathri J, Harding CL, Radey MC, Rezayat A and Bautista G (2015) Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 18, 307–319.
32. Einarsson GG, Comer DM, McIlreavey L, Parkhill J, Ennis M, Tunney MM and Elborn JS (2016) Community dynamics and the lower airway microbiota in stable chronic obstructive pulmonary disease, smokers and healthy non-smokers. Thorax 71, 795–803.
33. Tunney M, Klem E, Fodor A, Gilpin D, Moriarty T, McGrath S, Muhlebach M, Boucher RC, Cardwell C and Doering G (2011) Use of culture and molecular analysis to determine the effect of antibiotic treatment on microbial community diversity and abundance during exacerbation in patients with cystic fibrosis. Thorax 66, 579–584.
34. Yu G, Gail MH, Consonni D, Carugno M, Humphrys M, Pesatori AC, Caporaso NE, Goedert JJ, Ravel J and Landi MT (2016) Characterizing human lung tissue microbiota and its relationship to epidemiological and clinical features. Genome Biol 17, 163.
35. Pezzulo AA, Kelly PH, Nassar BS, Rutland CJ, Gansemer ND, Dohrn CL, Costello AJ, Stoltz DA and Zabner J (2013) Abundant DNase I-sensitive bacterial DNA in healthy porcine lungs and its implications for the lung microbiome. Appl Environ Microbiol 79, 5936–5941.
36. Nocker A, Cheung CY and Camper AK (2006) Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods 67, 310–320.
37. Nocker A and Camper AK (2006) Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Appl Environ Microbiol 72, 1997–2004.
38. Rogers GB, Stressmann FA, Koller G, Daniels T, Carroll MP and Bruce KD (2008) Assessing the diagnostic importance of nonviable bacterial cells in respiratory infections. Diagn Microbiol Infect Dis 62, 133–141.
39. Rogers GB, Cuthbertson L, Hoffman LR, Wing PA, Pope C, Hooftman DA, Lilley AK, Oliver A, Carroll MP, Bruce KD et al. (2013) Reducing bias in bacterial community analysis of lower respiratory infections. ISME J 7, 697–706.
40. Molaee N, Abtahi H, Ghannadzadeh MJ, Karimi M and Ghaznavi-Rad E (2015) Application of reverse transcriptase-PCR (RT-PCR) for rapid detection of viable Escherichia coli in drinking water samples. J Environ Health Sci Eng 13, 1–6.
41. Klouche M and Schröder U (2008) Rapid methods for diagnosis of bloodstream infections. Clin Chem Lab Med 46, 888–908.
42. Blazewicz SJ, Barnard RL, Daly RA and Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7, 2061–2068.
43. Venkataraman A, Bassis CM, Beck JM, Young VB, Curtis JL, Huffnagle GB and Schmidt TM (2015) Application of a neutral community model to assess structuring of the human lung microbiome. mBio 6, e02284–e02214.
44. Huang YJ, Sethi S, Murphy T, Nariya S, Boushey HA and Lynch SV (2014) Airway microbiome dynamics in exacerbations of chronic obstructive pulmonary disease. J Clin Microbiol 52, 2813–2823.
45. Cheung MK, Lam WY, Fung WYW, Law PTW, Au CH, Nong W, Kam KM, Kwan HS and Tsui SKW (2013) Sputum microbiota in tuberculosis as revealed by 16S rRNA pyrosequencing. PLoS One 8, e54574.
46. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L et al. (2010) Disordered microbial communities in asthmatic airways. PLoS One 5, e8578.
47. Dickson RP, Erb-Downward JR and Huffnagle GB (2014) Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis. Lancet Respir Med 2, 238–246.
48. Lozupone C, Cota-Gomez A, Palmer B, Linderman D, Charlson E, Sodergren E, Mitreva M, Abubucker S, Martin J and Yao G (2013) Widespread colonization of the lung by Tropheryma whipplei in HIV infection. Am J Respir Crit Care Med 187, 1110–1117.
49. Morris A, Beck J, Schloss P, Campbell T, Crothers K, Curtis J, Flores S, Fontenot A, Ghedin E and Huang L (2013) Comparison of the respiratory microbiome in healthy non-smokers and smokers. Am J Respir Crit Care Med 187, 1067–1075.
50. Tap J, Mondot S, Levenez F, Pelletier E, Caron C, Furet JP, Ugarte E, Muñoz-Tamayo R, Paslier DL and Nalin R (2009) Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 11, 2574–2584.
51. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E, Teggatz P, Barman M, Hayward M, Eastwood D et al. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11, 76–82.
52. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CCGM, Troost FJ, Bork P, Wels M, de Vos WM and Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6, 1415–1426.
53. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W and Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336, 1262–1267.
54. Guarner F and Malagelada J-R (2003) Gut flora in health and disease. Lancet 361, 512–519.
55. Roberfroid M, Bornet F, Bouley CE and Cummings J (1995) Colonic microflora: nutrition and health. Summary and conclusions of an International Life Sciences Institute (ILSI) [Europe] workshop held in Barcelona, Spain. Nutr Rev 53, 127–130.
56. Sekirov I, Russell SL, Antunes LCM and Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90, 859–904.
57. Marteau P, Pochart P, Doré J, Béra-Maillet C, Bernalier A and Corthier G (2001) Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl Environ Microbiol 67, 4939–4942.
58. Hayashi H, Takahashi R, Nishi T, Sakamoto M and Benno Y (2005) Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol 54, 1093–1101.
59. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K et al. (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci 107, 18933–18938.
60. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N and Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107, 11971–11975.
61. Kozyrskyj AL, Bahreinian S and Azad MB (2011) Early life exposures: impact on asthma and allergic disease. Curr Opin Allergy Clin Immunol 11, 400–406.
62. Manichanh C, Reeder J, Gibert P, Varela E, Llopis M, Antolin M, Guigo R, Knight R and Guarner F (2010) Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res 20, 1411–1419.
63. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT and Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci 108 (Suppl 1), 4578–4585.
64. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN and Anokhin AP (2012) Human gut microbiome viewed across age and geography. Nature 486, 222–227.
65. Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA and Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915–1920.
66. Jeffery IB and O'Toole PW (2013) Diet-microbiota interactions and their implications for healthy living. Nutrients 5, 234–252.
67. Scott KP, Gratz SW, Sheridan PO, Flint HJ and Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69, 52–60.
68. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, Moulton L, Glawe A, Wang Y, Leone V et al. (2014) Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One 9, e92193.
69. Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, Matsubara N and Hara H (2008) Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem 72, 572–576.
70. Keeney KM, Yurist-Doutsch S, Arrieta MC and Finlay BB (2014) Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol 68, 217–235.
71. Jernberg C, Lofmark S, Edlund C and Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1, 56–66.
72. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK and Engstrand L (2010) Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 5, e9836.
73. Sanders ME, Guarner F, Guerrant R, Holt PR, Quigley EM, Sartor RB, Sherman PM and Mayer EA (2013) An update on the use and investigation of probiotics in health and disease. Gut 62, 787–796.
74. Borody TJ and Khoruts A (2012) Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9, 88–96.
75. Mäkivuokko H, Tiihonen K, Tynkkynen S, Paulin L and Rautonen N (2010) The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr 103, 227–234.
76. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK and Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230.
77. Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M and Brigidi P (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125, 286–292.
78. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL and Suzuki T (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547.
79. van der Waaij D, Berghuis JM and Lekkerkerk JE (1972) Colonization resistance of the digestive tract of mice during systemic antibiotic treatment. J Hyg (Lond) 70, 605–610.
80. Hooper LV, Littman DR and Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336, 1268–1273.
81. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K and Mazmanian SK (2013) Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426–429.
82. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA and Mazmanian SK (2011) The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974–977.
83. Kubinak JL and Round JL (2012) Toll-like receptors promote mutually beneficial commensal-host interactions. PLoS Pathog 8, e1002785.
84. Peterson DA, McNulty NP, Guruge JL and Gordon JI (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2, 328–339.
85. Mantis NJ, Rol N and Corthesy B (2011) Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol 4, 603–611.
86. Pédron T, Mulet C, Dauga C, Frangeul L, Chervaux C, Grompone G and Sansonetti PJ (2012) A crypt-specific core microbiota resides in the mouse colon. mBio 3, e00116–e00112.
87. Richmond BW, Brucker RM, Han W, Du RH, Zhang Y, Cheng DS, Gleaves L, Abdolrasulnia R, Polosukhina D, Clark PE et al. (2016) Airway bacteria drive a progressive COPD-like phenotype in mice with polymeric immunoglobulin receptor deficiency. Nat Commun 7, 11240.
88. Richmond BW, Brucker RM, Du RH, Gleaves L, Bordenstein S, Blackwell TS and Polosukhin VV (2016) A21. Chronic airway inflammation: microbial influence. In The Lung Microbiota Drives a COPD-like Phenotype in Secretory IgA-deficient Mice. ajrccm-conference; 193, A1074.
89. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM and Wolfgang MC (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.
90. Stressmann FA, Rogers GB, van der Gast CJ, Marsh P, Vermeer LS, Carroll MP, Hoffman L, Daniels TWV, Patel N, Forbes B 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.
91. Coburn B, Wang PW, Caballero JD, Clark ST, Brahma V, Donaldson S, Zhang Y, Surendra A, Gong Y, Tullis DE et al. (2015) Lung microbiota across age and disease stage in cystic fibrosis. Sci Rep 5, 10241.
92. Flight WG, Smith A, Paisey C, Marchesi JR, Bull MJ, Norville PJ, Mutton KJ, Webb AK, Bright-Thomas RJ, Jones AM et al. (2015) Rapid detection of emerging pathogens and loss of microbial diversity associated with severe lung disease in cystic fibrosis. J Clin Microbiol 53, 2022–2029.
93. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, Cavalcoli JD, VanDevanter DR, Murray S, Li JZ et al. (2012) Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci 109, 5809–5814.
94. Stokell JR, Gharaibeh RZ, Hamp TJ, Zapata MJ, Fodor AA and Steck TR (2015) Analysis of changes in diversity and abundance of the microbial community in a cystic fibrosis patient over a multiyear period. J Clin Microbiol 53, 237–247.
95. Paganin P, Fiscarelli EV, Tuccio V, Chiancianesi M, Bacci G, Morelli P, Dolce D, Dalmastri C, De Alessandri A, Lucidi V et al. (2015) Changes in cystic fibrosis airway microbial community associated with a severe decline in lung function. PLoS One 10, e0124348.
96. Palmer KL, Mashburn LM, Singh PK and Whiteley M (2005) Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187, 5267–5277.
97. Brooks C, Pearce N and Douwes J (2013) The hygiene hypothesis in allergy and asthma: an update. Curr Opin Allergy Clin Immunol 13, 70–77.
98. Maizels RM, McSorley HJ and Smyth DJ (2014) Helminths in the hygiene hypothesis: sooner or later? Clin Exp Immunol 177, 38–46.
99. Daley D (2014) The evolution of the hygiene hypothesis: the role of early-life exposures to viruses and microbes and their relationship to asthma and allergic diseases. Curr Opin Allergy Clin Immunol 14, 390–396.
100. Guarner F, Bourdet-Sicard R, Brandtzaeg P, Gill HS, McGuirk P, van Eden W, Versalovic J, Weinstock JV and Rook GAW (2006) Mechanisms of disease: the hygiene hypothesis revisited. Nat Clin Pract Gastroenterol Hepatol 3, 275–284.
101. Hansen CHF, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, Tlaskalova-Hogenova H and Hansen AK (2012) Patterns of early gut colonization shape future immune responses of the host. PLoS One 7, e34043.
102. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, Becker AB, Scott JA and Kozyrskyj AL (2013) Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol 9, 1.
103. Loss G, Apprich S, Waser M, Kneifel W, Genuneit J, Büchele G, Weber J, Sozanska B, Danielewicz H, Horak E et al. (2011) The protective effect of farm milk consumption on childhood asthma and atopy: the GABRIELA study. J Allergy Clin Immunol 128, 766–773. e764.
104. Debarry J, Garn H, Hanuszkiewicz A, Dickgreber N, Blümer N, von Mutius E, Bufe A, Gatermann S, Renz H, Holst O et al. (2007) Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. J Allergy Clin Immunol 119, 1514–1521.
105. Inghammar M, Ekbom A, Engström G, Ljungberg B, Romanus V, Löfdahl CG and Egesten A (2010) COPD and the risk of tuberculosis – a population-based cohort study. PLoS One 5, e10138.
106. Parameswaran GI and Murphy TF (2007) Infections in chronic lung diseases. Infect Dis Clin North Am 21, 673–695.
107. Mirković B, Murray MA, Lavelle GM, Molloy K, Azim AA, Gunaratnam C, Healy F, Slattery D, McNally P, Hatch J et al. (2015) The role of short-chain fatty acids, produced by anaerobic bacteria, in the cystic fibrosis airway. Am J Respir Crit Care Med 192, 1314–1324.
108. Cohen-Cymberknoh M, Kerem E, Ferkol T and Elizur A (2013) Airway inflammation in cystic fibrosis: molecular mechanisms and clinical implications. Thorax 68, 1157–1162.
109. Larsen N, Vogensen FK, van den Berg FWJ, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH and Jakobsen M (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5, e9085.
110. Musso G, Gambino R and Cassader M (2010) Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes Care 33, 2277–2284.
111. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER and Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1131.
112. Suputtamongkol Y, Chaowagul W, Chetchotisakd P, Lertpatanasuwun N, Intaranongpai S, Ruchutrakool T, Budhsarawong D, Mootsikapun P, Wuthiekanun V and Teerawatasook N (1999) Risk factors for melioidosis and bacteremic melioidosis. Clin Infect Dis 29, 408–413.
113. Kornum JB, Thomsen RW, Riis A, Lervang H-H, Schønheyder HC and Sørensen HT (2007) Type 2 diabetes and pneumonia outcomes a population-based cohort study. Diabetes Care 30, 2251–2257.
114. Jeon CY and Murray MB (2008) Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med 5, e152.
115. Dooley KE and Chaisson RE (2009) Tuberculosis and diabetes mellitus: convergence of two epidemics. Lancet Infect Dis 9, 737–746.
116. Martens GW, Arikan MC, Lee J, Ren F, Greiner D and Kornfeld H (2007) Tuberculosis susceptibility of diabetic mice. Am J Respir Cell Mol Biol 37, 518–524.
117. Herbst T, Sichelstiel A, Schär C, Yadava K, Bürki K, Cahenzli J, McCoy K, Marsland BJ and Harris NL (2011) Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am J Respir Crit Care Med 184, 198–205.
118. Bisgaard H, Li N, Bonnelykke K, Chawes BLK, Skov T, Paludan-Müller G, Stokholm J, Smith B and Krogfelt KA (2011) Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol 128, 646–652. e645.
119. Corrêa-Oliveira R, Fachi JL, Vieira A, Sato FT and Vinolo MAR (2016) Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunology 5, e73.
120. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, Korecka A, Bakocevic N, Ng LG and Kundu P (2014) The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med 6, 263ra158.
121. Trompette A, Yadava K, Gollwitzer E, Sichelstiel A, Nicod L and Marsland B (2012) Short-chain fatty acids are potent modulators of allergic airway inflammation. Eur Respir J 40 (Suppl 56), P2362.
122. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL et al. (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489–493.
123. Perry S, de Jong BC, Solnick JV, Sanchez MdlL, Yang S, Lin PL, Hansen LM, Talat N, Hill PC, Hussain R et al. (2010) Infection with Helicobacter pylori is associated with protection against tuberculosis. PLoS One 5, e8804.
124. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, Paley MA, Antenus M, Williams KL, Erikson J et al. (2012) Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37, 158–170.
125. Tanaka K, Sawamura S, Satoh T, Kobayashi K and Noda S (2007) Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J Immunol 178, 5209–5216.
126. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS and Iwasaki A (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci 108, 5354–5359.
127. Gauguet S, D'Ortona S, Ahnger-Pier K, Duan B, Surana NK, Lu R, Cywes-Bentley C, Gadjeva M, Shan Q, Priebe GP et al. (2015) Intestinal microbiota of mice influences resistance to Staphylococcus aureus pneumonia. Infect Immun 83, 4003–4014.
128. Huempfner HR and Deuschle KW (1966) Experimental tuberculosis in germ-free and conventional mice. Am Rev Respir Dis 93, 465–467.
129. Arnold IC, Hutchings C, Kondova I, Hey A, Powrie F, Beverley P and Tchilian E (2015) Helicobacter hepaticus infection in BALB/c mice abolishes subunit-vaccine-induced protection against M. tuberculosis. Vaccine 33, 1808–1814.
130. Kamada N, Chen GY, Inohara N and Nunez G (2013) Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 14, 685–690.
131. Belkaid Y and Hand Timothy W (2014) Role of the microbiota in immunity and inflammation. Cell 157, 121–141.
132. Macpherson AJ and Uhr T (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303, 1662–1665.
133. Sonnenberg GF and Artis D (2012) Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 37, 601–610.
134. Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y and Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288.
135. Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, Mention J-J, Thiam K, Cerf-Bensussan N and Mandelboim O (2008) Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29, 958–970.
136. Ganal SC, Sanos SL, Kallfass C, Oberle K, Johner C, Kirschning C, Lienenklaus S, Weiss S, Staeheli P and Aichele P (2012) Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 37, 171–186.
137. Samuelson DR, Welsh DA and Shellito JE (2015) Regulation of lung immunity and host defense by the intestinal microbiota. Front Microbiol 6, 1085.
138. McAleer JP, Nguyen NLH, Chen K, Kumar P, Ricks DM, Binnie M, Armentrout RA, Pociask DA, Hein A, Yu A et al. (2016) Pulmonary Th17 antifungal immunity is regulated by the gut microbiome. J Immunol 197, 97–107.
139. Marsland BJ, Trompette A and Gollwitzer ES (2015) The gut-lung axis in respiratory disease. Ann Am Thorac Soc 12 (Suppl 2), S150–S156.
140. Rooks MG and Garrett WS (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16, 341–352.
141. Lachmandas E, van den Heuvel CNAM, Damen MSMA, Cleophas MCP, Netea MG and van Crevel R (2016) Diabetes mellitus and increased tuberculosis susceptibility: the role of short-chain fatty acids. J Diabetes Res 2016, 6014631.
142. Dickson RP and Cox MJ (2016) The premature invocation of a ‘gut-lung axis’ may obscure the direct effects of respiratory microbiota on pneumonia susceptibility. Gut doi: 10.1136/gutjnl-2016-311823.
143. Bellinghausen C, Gulraiz F, Heinzmann ACA, Dentener MA, Savelkoul PHM, Wouters EF, Rohde GG and Stassen FR (2016) Exposure to common respiratory bacteria alters the airway epithelial response to subsequent viral infection. Respir Res 17, 68.
144. Hart AL, Ng SC, Mann E, Al-Hassi HO, Bernardo D and Knight SC (2010) Homing of immune cells: role in homeostasis and intestinal inflammation. Inflamm Bowel Dis 16, 1969–1977.
145. Sigmundsdottir H and Butcher EC (2008) Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol 9, 981–987.
146. Valdez J, Peral M, Rachid M, Santana M and Perdigon G (2005) Interference of Lactobacillus plantarum with Pseudomonas aeruginosa in vitro and in infected burns: the potential use of probiotics in wound treatment. Clin Microbiol Infect 11, 472–479.
147. Mu C, Yang Y and Zhu W (2015) Crosstalk between the immune receptors and gut microbiota. Curr Protein Pept Sci 16, 622–631.
148. Bremel RD and Homan EJ (2015) Extensive T-cell epitope repertoire sharing among human proteome, gastrointestinal microbiome, and pathogenic bacteria: implications for the definition of self. Front Immunol 6, 538.
149. Price DN, Kusewitt DF, Lino CA, McBride AA and Muttil P (2016) Oral tolerance to environmental mycobacteria interferes with intradermal, but not pulmonary, immunization against tuberculosis. PLoS Pathog 12, e1005614.
150. Fine PE (1995) Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346, 1339–1345.
151. Brandt L, Cunha JF, Olsen AW, Chilima B, Hirsch P, Appelberg R and Andersen P (2002) Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infect Immun 70, 672–678.
152. Kelly CR, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T and Wu G (2015) Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology 149, 223–237.
153. Antonopoulos DA and Chang EB (2016) Transplanting a microbial organ: the good, the bad, and the unknown. mBio 7, e00572–e00516.
154. Carr TF and Kraft M (2016) Chronic infection and severe asthma. Immunol Allergy Clin North Am 36, 483–502.
155. Iramain R, De Jesús R, Spitters C, Jara A, Jimenez J, Bogado N and Cardozo L (2016) Chlamydia pneumoniae, and mycoplasma pneumoniae: are they related to severe asthma in childhood? J Asthma 53, 618–621.
156. Lenoir-Wijnkoop I, Sanders ME, Cabana MD, Caglar E, Corthier G, Rayes N, Sherman PM, Timmerman HM, Vaneechoutte M, Van Loo J et al. (2007) Probiotic and prebiotic influence beyond the intestinal tract. Nutr Rev 65, 469–489.
157. Mortaz E, Adcock IM, Ricciardolo FL, Varahram M, Jamaati H, Velayati AA, Folkerts G and Garssen J (2015) Anti-inflammatory effects of Lactobacillus rahmnosus and Bifidobacterium breve on cigarette smoke activated human macrophages. PLoS One 10, e0136455.
158. Zhang Q, Cox M, Liang Z, Brinkmann F, Cardenas PA, Duff R, Bhavsar P, Cookson W, Moffatt M and Chung KF (2016) Airway microbiota in severe asthma and relationship to asthma severity and phenotypes. PLoS One 11, e0152724.
159. Krishna P, Jain A and Bisen PS (2016) Microbiome diversity in the sputum of patients with pulmonary tuberculosis. Eur J Clin Microbiol Infect Dis 35, 1205–1210.
160. Wu S, Jiang ZY, Sun YF, Yu B, Chen J, Dai CQ, Wu XL, Tang XL and Chen XY (2013) Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza a virus infection. Curr Microbiol 67, 414–422.
161. Adam E, Delbrassinne L, Bouillot C, Reynders V, Mailleux AC, Muraille E and Jacquet A (2010) Probiotic Escherichia coli Nissle 1917 activates DC and prevents house dust mite allergy through a TLR4-dependent pathway. Eur J Immunol 40, 1995–2005.
162. Blümer N, Sel S, Virna S, Patrascan C, Zimmermann S, Herz U, Renz H and Garn H (2007) Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring. Clin Exp Allergy 37, 348–357.
163. Bernasconi E, Pattaroni C, Koutsokera A, Pison C, Kessler R, Benden C, Soccal PM, Magnan A, Aubert JD, Marsland BJ et al. (2016) Airway microbiota determines innate cell inflammatory or tissue remodeling profiles in lung transplantation. Am J Respir Crit Care Med doi: 10.1164/rccm.201512-2424OC.
164. Forsythe P, Inman MD and Bienenstock J (2007) Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med 175, 561–569.
165. Stentzel S, Teufelberger A, Nordengrün M, Kolata J, Schmidt F, van Crombruggen K, Michalik S, Kumpfmüller J, Tischer S and Schweder T (2016) Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J Allergy Clin Immunol doi: 10.1016/j.jaci.2016.03.045.
166. Karimi K, Inman MD, Bienenstock J and Forsythe P (2009) Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med 179, 186–193.
167. Schabussova I, Hufnagl K, Tang ML, Hoflehner E, Wagner A, Loupal G, Nutten S, Zuercher A, Mercenier A and Wiedermann U (2012) Perinatal maternal administration of Lactobacillus paracasei NCC 2461 prevents allergic inflammation in a mouse model of birch pollen allergy. PLoS One 7, e40271.