Skip to main content
SpringerLink
Log in

Development of a Stable Lung Microbiome in Healthy Neonatal Mice

  • Human Microbiome
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The lower respiratory tract has been previously considered sterile in a healthy state, but advances in culture-independent techniques for microbial identification and characterization have revealed that the lung harbors a diverse microbiome. Although research on the lung microbiome is increasing and important questions were already addressed, longitudinal studies aiming to describe developmental stages of the microbial communities from the early neonatal period to adulthood are lacking. Thus, little is known about the early-life development of the lung microbiome and the impact of external factors during these stages. In this study, we applied a barcoding approach based on high-throughput sequencing of 16S ribosomal RNA gene amplicon libraries to determine age-dependent differences in the bacterial fraction of the murine lung microbiome and to assess potential influences of differing “environmental microbiomes” (simulated by the application of used litter material to the cages). We could clearly show that the diversity of the bacterial community harbored in the murine lung increases with age. Interestingly, bacteria belonging to the genera Delftia and Rhodococcus formed an age-independent core microbiome. The addition of the used litter material influenced the lung microbiota of young mice but did not significantly alter the community composition of adult animals. Our findings elucidate the dynamic nature of the early-life lung microbiota and its stabilization with age. Further, this study indicates that even slight environmental changes modulate the bacterial community composition of the lung microbiome in early life, whereas the lung microbes of adults demonstrate higher resilience towards environmental variations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Cho I, Blaser MJ (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13(4):260–270. https://doi.org/10.1038/nrg3182

    CAS  PubMed  PubMed Central  Google Scholar 

  2. van Rensburg JJ, Lin H, Gao X, Toh E, Fortney KR, Ellinger S, Zwickl B, Janowicz DM, Katz BP, Nelson DE, Dong Q, Spinola SM (2015) The human skin microbiome associates with the outcome of and is influenced by bacterial infection. mBio 6(5):e01315-15. https://doi.org/10.1128/mBio.01315-15

  3. Igartua C, Davenport ER, Gilad Y, Nicolae DL, Pinto J, Ober C (2017) Host genetic variation in mucosal immunity pathways influences the upper airway microbiome. Microbiome 5(1):16. https://doi.org/10.1186/s40168-016-0227-5

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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(1):e8578. https://doi.org/10.1371/journal.pone.0008578

    Article  PubMed  PubMed Central  Google Scholar 

  5. 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(2):e16384. https://doi.org/10.1371/journal.pone.0016384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. van der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P, Daniels TW, Carroll MP, Parkhill J, Bruce KD (2011) Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J 5(5):780–791. https://doi.org/10.1038/ismej.2010.175

    Article  PubMed  Google Scholar 

  7. Dickson RP, Erb-Downward JR, Huffnagle GB (2014) Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis. Lancet Respir. Med. 2(3):238–246. https://doi.org/10.1016/s2213-2600(14)70028-1

    Article  PubMed  PubMed Central  Google Scholar 

  8. Beck JM, Schloss PD, Venkataraman A, Twigg 3rd H, Jablonski KA, Bushman FD, Campbell TB, Charlson ES, Collman RG, Crothers K, Curtis JL, Drews KL, Flores SC, Fontenot AP, Foulkes MA, Frank I, Ghedin E, Huang L, Lynch SV, Morris A, Palmer BE, Schmidt TM, Sodergren E, Weinstock GM, Young VB, Lung HIVMP (2015) Multicenter comparison of lung and oral microbiomes of HIV-infected and HIV-uninfected individuals. Am. J. Respir. Crit. Care Med. 192(11):1335–1344. https://doi.org/10.1164/rccm.201501-0128OC

    Article  PubMed  PubMed Central  Google Scholar 

  9. Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, Bushman FD, Collman RG (2012) Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am. J. Respir. Crit. Care Med. 186(6):536–545. https://doi.org/10.1164/rccm.201204-0693OC

    Article  PubMed  PubMed Central  Google Scholar 

  10. Marsland BJ, Gollwitzer ES (2014) Host-microorganism interactions in lung diseases. Nat Rev Immunol 14(12):827–835. https://doi.org/10.1038/nri3769

    Article  CAS  PubMed  Google Scholar 

  11. 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(8):957–963. https://doi.org/10.1164/rccm.201104-0655OC

    Article  PubMed  PubMed Central  Google Scholar 

  12. Gensollen T, Iyer SS, Kasper DL, Blumberg RS (2016) How colonization by microbiota in early life shapes the immune system. Science 352(6285):539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. de Steenhuijsen Piters WA, Huijskens EG, Wyllie AL, Biesbroek G, van den Bergh MR, Veenhoven RH, Wang X, Trzcinski K, Bonten MJ, Rossen JW, Sanders EA, Bogaert D (2016) Dysbiosis of upper respiratory tract microbiota in elderly pneumonia patients. ISME J 10(1):97–108. https://doi.org/10.1038/ismej.2015.99

    Article  PubMed  Google Scholar 

  14. Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM, Young VB, Beck JM, Curtis JL, Huffnagle GB (2015) Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. mBio 6(2):e00037-15. https://doi.org/10.1128/mBio.00037-15

  15. Dickson RP, Erb-Downward JR, Martinez FJ, Huffnagle GB (2015) The microbiome and the respiratory tract. Annu Rev Physiol 78:481–504. https://doi.org/10.1146/annurev-physiol-021115-105238

  16. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB, Curtis JL (2015) Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc 12(6):821–830. https://doi.org/10.1513/AnnalsATS.201501-029OC

    Article  PubMed  PubMed Central  Google Scholar 

  17. Biesbroek G, Tsivtsivadze E, Sanders EA, Montijn R, Veenhoven RH, Keijser BJ, Bogaert D (2014) Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am. J. Respir. Crit. Care Med. 190(11):1283–1292. https://doi.org/10.1164/rccm.201407-1240OC

    Article  PubMed  Google Scholar 

  18. Vital M, Harkema JR, Rizzo M, Tiedje J, Brandenberger C (2015) Alterations of the murine gut microbiome with age and allergic airway disease. J Immunol Res 2015:892568. https://doi.org/10.1155/2015/892568

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yu G, Fadrosh D, Goedert JJ, Ravel J, Goldstein AM (2015) Nested PCR biases in interpreting microbial community structure in 16S rRNA gene sequence datasets. PLoS One 10(7):e0132253. https://doi.org/10.1371/journal.pone.0132253

    Article  PubMed  PubMed Central  Google Scholar 

  20. Field KG, Gordon D, Wright T, Rappé M, Urback E, Vergin K, Giovannoni SJ (1997) Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl. Environ. Microbiol. 63(1):63–70

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J. Bacteriol. 178(19):5636–5643

    Article  PubMed  PubMed Central  Google Scholar 

  22. McKenna P, Hoffmann C, Minkah N, Aye PP, Lackner A, Liu Z, Lozupone CA, Hamady M, Knight R, Bushman FD (2008) The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog. 4(2):e20. https://doi.org/10.1371/journal.ppat.0040020

    Article  PubMed  PubMed Central  Google Scholar 

  23. Muyzer G, Teske A, Wirsen C, Jannasch H (1995) Phylogenetic relationships ofThiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch. Microbiol. 164(3):165–172. https://doi.org/10.1007/BF02529967

    Article  CAS  PubMed  Google Scholar 

  24. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41(1):e1. https://doi.org/10.1093/nar/gks808

    Article  CAS  PubMed  Google Scholar 

  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(5):335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhou J, Wu L, Deng Y, Zhi X, Jiang YH, Tu Q, Xie J, Van Nostrand JD, He Z, Yang Y (2011) Reproducibility and quantitation of amplicon sequencing-based detection. ISME J 5(8):1303–1313. https://doi.org/10.1038/ismej.2011.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12:87. https://doi.org/10.1186/s12915-014-0087-z

    Article  PubMed  PubMed Central  Google Scholar 

  28. Newman ME (2006) Modularity and community structure in networks. Proc. Natl. Acad. Sci. U. S. A. 103(23):8577–8582. https://doi.org/10.1073/pnas.0601602103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Aho VT, Pereira PA, Haahtela T, Pawankar R, Auvinen P, Koskinen K (2015) The microbiome of the human lower airways: a next generation sequencing perspective. World Allergy Organ J 8(1):23. https://doi.org/10.1186/s40413-015-0074-z

    Article  PubMed  Google Scholar 

  30. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, Stanton C, van Sinderen D, O'Connor M, Harnedy N, O'Connor K, Henry C, O'Mahony D, Fitzgerald AP, Shanahan F, Twomey C, Hill C, Ross RP, O'Toole PW (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl 1):4586–4591. https://doi.org/10.1073/pnas.1000097107

    Article  CAS  PubMed  Google Scholar 

  31. Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17(5):690–703. https://doi.org/10.1016/j.chom.2015.04.004

    Article  PubMed  Google Scholar 

  32. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gollwitzer ES, Saglani S, Trompette A, Yadava K, Sherburn R, McCoy KD, Nicod LP, Lloyd CM, Marsland BJ (2014) Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat. Med. 20(6):642–647. https://doi.org/10.1038/nm.3568

    Article  CAS  PubMed  Google Scholar 

  34. Yun Y, Srinivas G, Kuenzel S, Linnenbrink M, Alnahas S, Bruce KD, Steinhoff U, Baines JF, Schaible UE (2014) Environmentally determined differences in the murine lung microbiota and their relation to alveolar architecture. PLoS One 9(12):e113466. https://doi.org/10.1371/journal.pone.0113466

    Article  PubMed  PubMed Central  Google Scholar 

  35. Barfod KK, Roggenbuck M, Hansen LH, Schjorring S, Larsen ST, Sorensen SJ, Krogfelt KA (2013) The murine lung microbiome in relation to the intestinal and vaginal bacterial communities. BMC Microbiol. 13:303. https://doi.org/10.1186/1471-2180-13-303

    Article  PubMed  PubMed Central  Google Scholar 

  36. Merrifield CA, Lewis MC, Berger B, Cloarec O, Heinzmann SS, Charton F, Krause L, Levin NS, Duncker S, Mercenier A, Holmes E, Bailey M, Nicholson JK (2016) Neonatal environment exerts a sustained influence on the development of the intestinal microbiota and metabolic phenotype. ISME J 10(1):145–157. https://doi.org/10.1038/ismej.2015.90

    Article  CAS  PubMed  Google Scholar 

  37. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563. https://doi.org/10.1038/nature12820

    Article  CAS  PubMed  Google Scholar 

  38. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, Blanchard C, Junt T, Nicod LP, Harris NL, Marsland BJ (2014) Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20(2):159–166. https://doi.org/10.1038/nm.3444

    Article  CAS  PubMed  Google Scholar 

  39. Kepert I, Fonseca J, Muller C, Milger K, Hochwind K, Kostric M, Fedoseeva M, Ohnmacht C, Dehmel S, Nathan P, Bartel S, Eickelberg O, Schloter M, Hartmann A, Schmitt-Kopplin P, Krauss-Etschmann S (2016) D-tryptophan from probiotic bacteria influences the gut microbiome and allergic airway disease. J Allergy Clin Immunol 139(5):1525–1535. https://doi.org/10.1016/j.jaci.2016.09.003

  40. Draijer C, Hylkema MN, Boorsma CE, Klok PA, Robbe P, Timens W, Postma DS, Greene CM, Melgert BN (2016) Sexual maturation protects against development of lung inflammation through estrogen. Am J Physiol Lung Cell Mol Physiol 310(2):L166–L174. https://doi.org/10.1152/ajplung.00119.2015

    Article  PubMed  Google Scholar 

  41. Haro C, Rangel-Zuniga OA, Alcala-Diaz JF, Gomez-Delgado F, Perez-Martinez P, Delgado-Lista J, Quintana-Navarro GM, Landa BB, Navas-Cortes JA, Tena-Sempere M, Clemente JC, Lopez-Miranda J, Perez-Jimenez F, Camargo A (2016) Intestinal microbiota is influenced by gender and body mass index. PLoS One 11(5):e0154090. https://doi.org/10.1371/journal.pone.0154090

    Article  PubMed  PubMed Central  Google Scholar 

  42. Poroyko V, Meng F, Meliton A, Afonyushkin T, Ulanov A, Semenyuk E, Latif O, Tesic V, Birukova AA, Birukov KG (2015) Alterations of lung microbiota in a mouse model of LPS-induced lung injury. Am J Physiol Lung Cell Mol Physiol 309(1):L76–L83. https://doi.org/10.1152/ajplung.00061.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Gundelly P, Suzuki Y, Ribes JA, Thornton A (2016) Differences in Rhodococcus equi infections based on immune status and antibiotic susceptibility of clinical isolates in a case series of 12 patients and cases in the literature. Biomed. Res. Int. 2016:2737295. https://doi.org/10.1155/2016/2737295

    Article  PubMed  PubMed Central  Google Scholar 

  44. Miller RA (1995) Cellular and biochemical changes in the aging mouse immune system. Nutr. Rev. 53(4):S8–S17. https://doi.org/10.1111/j.1753-4887.1995.tb01521.x

    Article  CAS  PubMed  Google Scholar 

  45. Arulazhagan P, Vasudevan N (2011) Biodegradation of polycyclic aromatic hydrocarbons by a halotolerant bacterial strain Ochrobactrum sp. VA1. Mar. Pollut. Bull. 62(2):388–394. https://doi.org/10.1016/j.marpolbul.2010.09.020

    Article  CAS  PubMed  Google Scholar 

  46. Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environment Int 35(1):162–177. https://doi.org/10.1016/j.envint.2008.07.018

    Article  Google Scholar 

  47. Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl. Microbiol. Biotechnol. 85(2):207–228. https://doi.org/10.1007/s00253-009-2192-4

    Article  CAS  PubMed  Google Scholar 

  48. Costa KC, Bergkessel M, Saunders S, Korlach J, Newman DK (2015) Enzymatic degradation of phenazines can generate energy and protect sensitive organisms from toxicity. MBio 6(6):e01520–e01515. https://doi.org/10.1128/mBio.01520-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Segal LN, Blaser MJ (2014) A brave new world: the lung microbiota in an era of change. Ann Am Thoracic Soc 11(Supplement 1):S21–S27. https://doi.org/10.1513/AnnalsATS.201306-189MG

    Article  Google Scholar 

  50. Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR (2015) Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21(10):1228–1234. https://doi.org/10.1038/nm.3950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lahti L, Salonen A, Kekkonen RA, Salojärvi J, Jalanka-Tuovinen J, Palva A, Orešič M, de Vos WM (2013) Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data. Peer J 1:e32. https://doi.org/10.7717/peerj.32

    Article  PubMed  PubMed Central  Google Scholar 

  52. Kolmeder CA, Salojarvi J, Ritari J, de Been M, Raes J, Falony G, Vieira-Silva S, Kekkonen RA, Corthals GL, Palva A, Salonen A, de Vos WM (2016) Faecal metaproteomic analysis reveals a personalized and stable functional microbiome and limited effects of a probiotic intervention in adults. PLoS One 11(4):e0153294. https://doi.org/10.1371/journal.pone.0153294

    Article  PubMed  PubMed Central  Google Scholar 

  53. Dickson RP (2016) The microbiome and critical illness. Lancet Respir. Med. 4(1):59–72. https://doi.org/10.1016/s2213-2600(15)00427-0

    Article  PubMed  Google Scholar 

  54. Marsland BJ, Salami O (2015) Microbiome influences on allergy in mice and humans. Curr. Opin. Immunol. 36:94–100. https://doi.org/10.1016/j.coi.2015.07.005

    Article  CAS  PubMed  Google Scholar 

  55. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336(6080):489–493. https://doi.org/10.1126/science.1219328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Thaiss CA, Zmora N, Levy M, Elinav E (2016) The microbiome and innate immunity. Nature 535(7610):65–74. https://doi.org/10.1038/nature18847

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully thank Rabea Imker for performing all necessary animal experiments, Susanne Kublik for excellent assistance in sequencing, and Maria de Vries for great statistical support. We further thank the reviewers for their critical feedback and insightful suggestions. This work was supported by intramural funding for Environmental Health projects of Helmholtz Zentrum München.

Author information

Authors and Affiliations

  1. Research Unit Comparative Microbiome Analysis, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85716, Neuherberg, Germany

    Matea Kostric, Gisle Vestergaard, Michael Schloter & Anne Schöler

  2. Department of Internal Medicine V, University of Munich, Comprehensive Pneumology Center, Member of the German Center for Lung Research (DZL), Munich, Germany

    Katrin Milger

  3. Institute of Lung Biology and Disease (ILBD), Helmholtz Center Munich, Comprehensive Pneumology Center (CPC-M), Munich, Germany

    Katrin Milger

  4. Division of Experimental Asthma Research, Research Center Borstel, Leibniz-Center for Medicine and Biosciences, Member of the German Center for Lung Research (DZL), Parkallee 1-40, 23845, Borstel, Germany

    Susanne Krauss-Etschmann

  5. Institute for Experimental Medicine, Christian-Albrechts-Universität zu Kiel, Niemannsweg 11, 24105, Kiel, Germany

    Susanne Krauss-Etschmann

  6. Research Unit Scientific Computing, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85716, Neuherberg, Germany

    Marion Engel

  7. ZIEL Institute for Food and Health, Technische Universität München, Weihenstephaner Berg 1, 85354, Freising, Germany

    Michael Schloter

Authors
  1. Matea Kostric
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katrin Milger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanne Krauss-Etschmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marion Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gisle Vestergaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Schloter
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anne Schöler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Schloter.

Ethics declarations

Compliance with Ethical Standards

During dissection, care was taken to minimize contamination and all animal procedures were realized in accordance with the Federal Guidelines for the Care and Use of Laboratory Animals.

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Table S1

(PDF 104 kb)

Table S2

(PDF 13 kb)

Table S3

(PDF 20 kb)

Table S4

(PDF 25 kb)

Table S5

(PDF 17 kb)

ESM 1

(DOCX 971 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kostric, M., Milger, K., Krauss-Etschmann, S. et al. Development of a Stable Lung Microbiome in Healthy Neonatal Mice. Microb Ecol 75, 529–542 (2018). https://doi.org/10.1007/s00248-017-1068-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1068-x

Keywords

Search

Navigation