Microbiome disturbance and resilience dynamics of the upper respiratory tract during influenza A virus infection.
Adolescent
Adult
Aged
Animals
Bacteria
/ classification
Biodiversity
Child
Child, Preschool
Dysbiosis
/ microbiology
Female
Ferrets
Humans
Infant
Influenza A virus
/ physiology
Influenza, Human
/ microbiology
Longitudinal Studies
Male
Microbiota
/ genetics
Middle Aged
Nasopharynx
/ microbiology
Orthomyxoviridae Infections
/ microbiology
Young Adult
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
21 05 2020
21 05 2020
Historique:
received:
03
05
2019
accepted:
28
04
2020
entrez:
23
5
2020
pubmed:
23
5
2020
medline:
18
8
2020
Statut:
epublish
Résumé
Infection with influenza can be aggravated by bacterial co-infections, which often results in disease exacerbation. The effects of influenza infection on the upper respiratory tract (URT) microbiome are largely unknown. Here, we report a longitudinal study to assess the temporal dynamics of the URT microbiomes of uninfected and influenza virus-infected humans and ferrets. Uninfected human patients and ferret URT microbiomes have stable healthy ecostate communities both within and between individuals. In contrast, infected patients and ferrets exhibit large changes in bacterial community composition over time and between individuals. The unhealthy ecostates of infected individuals progress towards the healthy ecostate, coinciding with viral clearance and recovery. Pseudomonadales associate statistically with the disturbed microbiomes of infected individuals. The dynamic and resilient microbiome during influenza virus infection in multiple hosts provides a compelling rationale for the maintenance of the microbiome homeostasis as a potential therapeutic target to prevent IAV associated bacterial co-infections.
Identifiants
pubmed: 32439901
doi: 10.1038/s41467-020-16429-9
pii: 10.1038/s41467-020-16429-9
pmc: PMC7242466
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2537Subventions
Organisme : NIAID NIH HHS
ID : HHSN272201400008C
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI135972
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN266200700010C
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI110819
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN272200900007C
Pays : United States
Commentaires et corrections
Type : ErratumIn
Références
Iuliano, A. D. et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 391, 1285–1300 (2017).
Johnson, N. P. & Mueller, J. Updating the accounts: global mortality of the 1918-1920 “Spanish” influenza pandemic. Bull. Hist. Med. 76, 105–115 (2002).
pubmed: 11875246
doi: 10.1353/bhm.2002.0022
Brundage, J. F. Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect. Dis. 6, 303–312 (2006).
pubmed: 16631551
pmcid: 7106411
doi: 10.1016/S1473-3099(06)70466-2
Brundage, J. F. & Shanks, G. D. Deaths from bacterial pneumonia during 1918-19 influenza pandemic. Emerg. Infect. Dis. 14, 1193–1199 (2008).
pubmed: 18680641
pmcid: 2600384
doi: 10.3201/eid1408.071313
Morens, D. M., Taubenberger, J. K. & Fauci, A. S. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198, 962–970 (2008).
pubmed: 18710327
pmcid: 2599911
doi: 10.1086/591708
Blyth, C. C. et al. The impact of bacterial and viral co-infection in severe influenza. Influenza Other Respir. Viruses 7, 168–176 (2013).
pubmed: 22487223
doi: 10.1111/j.1750-2659.2012.00360.x
Shah, N. S. et al. Bacterial and viral co-infections complicating severe influenza: Incidence and impact among 507 U.S. patients, 2013-14. J. Clin. Virol. 80, 12–19 (2016).
pubmed: 27130980
pmcid: 7185824
doi: 10.1016/j.jcv.2016.04.008
Charlson, E. S. et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am. J. Respir. Crit. Care Med. 184, 957–963 (2011).
pubmed: 21680950
pmcid: 3208663
doi: 10.1164/rccm.201104-0655OC
Tarabichi, Y. et al. The administration of intranasal live attenuated influenza vaccine induces changes in the nasal microbiota and nasal epithelium gene expression profiles. Microbiome 3, 74 (2015).
pubmed: 26667497
pmcid: 4678663
doi: 10.1186/s40168-015-0133-2
Langevin, S. et al. Early nasopharyngeal microbial signature associated with severe influenza in children: a retrospective pilot study. J. Gen. Virol. 98, 2425–2437 (2017).
Gao, Z., Kang, Y., Yu, J. & Ren, L. Human pharyngeal microbiome may play a protective role in respiratory tract infections. Genomics Proteom. Bioinforma. 12, 144–150 (2014).
doi: 10.1016/j.gpb.2014.06.001
Huang, Y. J. & Lynch, S. V. The emerging relationship between the airway microbiota and chronic respiratory disease: clinical implications. Expert Rev. Respir. Med. 5, 809–821 (2011).
pubmed: 22082166
pmcid: 3359942
doi: 10.1586/ers.11.76
Planet, P. J. et al. Lambda interferon restructures the nasal microbiome and increases susceptibility to Staphylococcus aureus superinfection. mBio 7, e01939–01915 (2016).
pubmed: 26861017
pmcid: 4752601
doi: 10.1128/mBio.01939-15
Whelan, F. J. et al. The loss of topography in the microbial communities of the upper respiratory tract in the elderly. Ann. Am. Thorac. Soc. 11, 513–521 (2014).
pubmed: 24601676
doi: 10.1513/AnnalsATS.201310-351OC
Chaban, B. et al. Characterization of the upper respiratory tract microbiomes of patients with pandemic H1N1 influenza. PLoS ONE 8, e69559 (2013).
pubmed: 23844261
pmcid: 3699515
doi: 10.1371/journal.pone.0069559
Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl Acad. Sci. USA 108, 5354–5359 (2011).
pubmed: 21402903
doi: 10.1073/pnas.1019378108
Wang, J. et al. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat. Commun. 4, 2106 (2013).
pubmed: 23820884
pmcid: 3715851
doi: 10.1038/ncomms3106
Wu, S. et al. Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza A virus infection. Curr. Microbiol. 67, 414–422 (2013).
pubmed: 23677145
doi: 10.1007/s00284-013-0380-z
Belser, J. A., Eckert, A. M., Tumpey, T. M. & Maines, T. R. Complexities in ferret influenza virus pathogenesis and transmission models. Microbiol. Mol. Biol. Rev. 80, 733–744 (2016).
pubmed: 27412880
pmcid: 4981671
doi: 10.1128/MMBR.00022-16
Belser, J. A., Katz, J. M. & Tumpey, T. M. The ferret as a model organism to study influenza A virus infection. Dis. Models Amp; Mechanisms 4, 575–579 (2011).
doi: 10.1242/dmm.007823
Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 17121 (2017).
pubmed: 28836573
doi: 10.1038/nmicrobiol.2017.121
O’Brien, J. D., Record, N. & Countway, P. The power and pitfalls of Dirichlet-multinomial mixture models for ecological count data. Preprint at https://www.biorxiv.org/content/10.1101/045468v2 (2016).
Holmes, I., Harris, K. & Quince, C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS ONE 7, e30126 (2012).
pubmed: 22319561
pmcid: 3272020
doi: 10.1371/journal.pone.0030126
Menuet, M. et al. First isolation of two colistin-resistant emerging pathogens, Brevundimonas diminuta and Ochrobactrum anthropi, in a woman with cystic fibrosis: a case report. J. Med. Case Rep. 2, 373 (2008).
pubmed: 19061488
pmcid: 2628933
doi: 10.1186/1752-1947-2-373
Huang, Y. J. et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS 14, 9–59 (2010).
pubmed: 20141328
pmcid: 3116451
doi: 10.1089/omi.2009.0100
Dickson, R. P., Erb-Downward, J. R. & Huffnagle, G. B. Homeostasis and its disruption in the lung microbiome. Am. J. Physiol. Lung Cell Mol. Physiol. 309, L1047–L1055 (2015).
pubmed: 26432870
pmcid: 4652146
doi: 10.1152/ajplung.00279.2015
Heirali, A. A. et al. The effects of inhaled aztreonam on the cystic fibrosis lung microbiome. Microbiome 5, 51 (2017).
pubmed: 28476135
pmcid: 5420135
doi: 10.1186/s40168-017-0265-7
Relman, D. A. The human microbiome: ecosystem resilience and health. Nutr. Rev. 70, S2–S9 (2012).
pubmed: 22861804
pmcid: 3422777
doi: 10.1111/j.1753-4887.2012.00489.x
Walker, B., Holling, C. S., Carpenter, S. R. & Kinzig, A. Resilience, adaptability, and transformability in social-ecological systems. Ecol. Soc. 9, 5 (2004).
doi: 10.5751/ES-00650-090205
Lee, K. H. et al. The respiratory microbiome and susceptibility to influenza virus infection. PLoS ONE 14, e0207898 (2019).
pubmed: 30625134
pmcid: 6326417
doi: 10.1371/journal.pone.0207898
Tsang, T. K. et al. Association between the respiratory microbiome and susceptibility to influenza virus infection. Clin. Infect. Dis. https://doi.org/10.1093/cid/ciz968 (2019).
Ding, T. et al. Microbial composition of the human nasopharynx varies according to influenza virus type and vaccination status. mBio 10, e01296-19 (2019).
Killip, M. J., Fodor, E. & Randall, R. E. Influenza virus activation of the interferon system. Virus Res. 209, 11–22 (2015).
pubmed: 25678267
pmcid: 4638190
doi: 10.1016/j.virusres.2015.02.003
Ramos-Sevillano, E. et al. The effect of influenza virus on the human oropharyngeal microbiome. Clin. Infect. Dis. 68, 1993–2002 (2019).
pubmed: 30445563
doi: 10.1093/cid/ciy821
Proctor, D. M. & Relman, D. A. The landscape ecology and microbiota of the human nose, mouth, and throat. Cell Host Microbe 21, 421–432 (2017).
pubmed: 28407480
pmcid: 5538306
doi: 10.1016/j.chom.2017.03.011
Klein, E. Y. et al. The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis. Influenza Other Respir. Viruses 10, 394–403 (2016).
pubmed: 27232677
pmcid: 4947938
doi: 10.1111/irv.12398
Leung, R. K. et al. Modulation of potential respiratory pathogens by pH1N1 viral infection. Clin. Microbiol. Infect. 19, 930–935 (2013).
pubmed: 23167452
doi: 10.1111/1469-0691.12054
Chen, H. W. et al. Nasal commensal Staphylococcus epidermidis counteracts influenza virus. Sci. Rep. 6, 27870 (2016).
pubmed: 27306590
pmcid: 4910069
doi: 10.1038/srep27870
Spinler, J. K. et al. From prediction to function using evolutionary genomics: human-specific ecotypes of Lactobacillus reuteri have diverse probiotic functions. Genome Biol. Evol. 6, 1772–1789 (2014).
pubmed: 24951561
pmcid: 4122935
doi: 10.1093/gbe/evu137
Morris, D. E., Cleary, D. W. & Clarke, S. C. Secondary bacterial infections associated with influenza pandemics. Front Microbiol. 8, 1041 (2017).
pubmed: 28690590
pmcid: 5481322
doi: 10.3389/fmicb.2017.01041
Hotterbeekx, A. et al. The endotracheal tube microbiome associated with Pseudomonas aeruginosa or Staphylococcus epidermidis. Sci. Rep. 6, 36507 (2016).
pubmed: 27812037
pmcid: 5095667
doi: 10.1038/srep36507
Rello, J. Bench-to-bedside review: therapeutic options and issues in the management of ventilator-associated bacterial pneumonia. Crit. Care 9, 259–265 (2005).
pubmed: 15987380
doi: 10.1186/cc3014
Lu, Q. et al. Pseudomonas aeruginosa serotypes in nosocomial pneumonia: prevalence and clinical outcomes. Crit. Care 18, R17 (2014).
pubmed: 24428878
pmcid: 4057348
doi: 10.1186/cc13697
Hoffken, G. & Niederman, M. S. Nosocomial pneumonia: the importance of a de-escalating strategy for antibiotic treatment of pneumonia in the ICU. Chest 122, 2183–2196 (2002).
pubmed: 12475862
doi: 10.1378/chest.122.6.2183
Sharma-Chawla, N. et al. Influenza A virus infection predisposes hosts to secondary infection with different Streptococcus pneumoniae serotypes with similar outcome but serotype-specific manifestation. Infect. Immun. 84, 3445–3457 (2016).
pubmed: 27647871
pmcid: 5116722
doi: 10.1128/IAI.00422-16
Gupta, R. K., George, R. & Nguyen-Van-Tam, J. S. Bacterial pneumonia and pandemic influenza planning. Emerg. Infect. Dis. 14, 1187–1192 (2008).
pubmed: 18680640
pmcid: 2600366
doi: 10.3201/eid1408.070751
Kash, J. C. & Taubenberger, J. K. The role of viral, host, and secondary bacterial factors in influenza pathogenesis. Am. J. Pathol. 185, 1528–1536 (2015).
pubmed: 25747532
pmcid: 4450310
doi: 10.1016/j.ajpath.2014.08.030
Manicassamy, B. et al. Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog. 6, e1000745 (2010).
pubmed: 20126449
pmcid: 2813279
doi: 10.1371/journal.ppat.1000745
Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005).
pubmed: 16056220
pmcid: 16056220
doi: 10.1038/nature03959
Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ. Microbiol. 75, 7537–7541 (2009).
pubmed: 19801464
pmcid: 2786419
doi: 10.1128/AEM.01541-09
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).
pubmed: 23193283
doi: 10.1093/nar/gks1219
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
pubmed: 23955772
pmcid: 23955772
doi: 10.1038/nmeth.2604
Paulson, J. N., Stine, O. C., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200 (2013).
pubmed: 24076764
pmcid: 4010126
doi: 10.1038/nmeth.2658
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
pubmed: 20383131
pmcid: 20383131
doi: 10.1038/nmeth.f.303
Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A. & Knight, R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2, 16 (2013).
pubmed: 24280061
pmcid: 4076506
doi: 10.1186/2047-217X-2-16
Gelman, A., Meng, X.-L. & Stern, H. Posterior predictive assessment of model fitness via realized discrepancies. Statistica Sin. 6, 733–760 (1996).
Meng, X.-L. Multiple-imputation inferences with uncongenial sources of input. Stat. Sci. 9, 538–558 (1994).
doi: 10.1214/ss/1177010269