Preview

PULMONOLOGIYA

Advanced search

The upper respiratory tract microbiome and its role in human health: barrier function

https://doi.org/10.18093/0869-0189-2022-32-6-876-884

Abstract

The human respiratory tract is a complex system characterized by a series of niches colonized with specific microbial communities. Until recently, researchers were mostly interested in lung microbiomes associated with acute and chronic infections. The upper respiratory tract microbiota has gained attention during COVID-19 (COronaVIrus Disease 2019) pandemic because it was suspected to influence the course and the outcome of viral infections. Aim. In this two-part review (see part 1, Pul’monolog;iya. 2022; 32 (5): 745-754), we summarize current knowledge of the microbial communities at each upper respiratory tract location, considering the proposed barrier function of the respiratory microbiome. Conclusion. Based on the evidence presented in this review, we can see how the respiratory microbiome is involved in the pathogenesis of viral respiratory infections, including SARS-CoV-2 (Severe Acute Respiratory Syndrome CoronaVirus 2).

About the Authors

E. V. Starikova
Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation

Elizaveta V. Starikova - Researcher, Laboratory of Genomic Research and Computational Biology, Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency.

Malaya Pirogovskaya ul. 1A, Moscow, 119435

tel.: (499) 245-04-71


Competing Interests:

The authors declare no conflict of interests



Yu. S. Galeeva
Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation

Yuliya S. Galeeva - Research Assistant at Laboratory of Genomic Research and Computational Biology, Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency.

Malaya Pirogovskaya ul. 1A, Moscow, 119435

tel.: (499) 245-04-71


Competing Interests:

The authors declare no conflict of interests



E. N. Il’ina
Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency
Russian Federation

Elena N. Il’ina - Doctor of Biology, Professor, Corresponding Member of Russian Academy of Sciences, Head of Laboratory of Genomic Studies and Computational Biology, Deputy Director for Science, Federal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological Agency.

Malaya Pirogovskaya ul. 1A, Moscow, 119435

tel.: (499) 245-04-71


Competing Interests:

The authors declare no conflict of interests



References

1. Selva L., Viana D., Regev-Yochay G. et al. Killing niche competitors by remote-control bacteriophage induction. Proc. Natl. Acad. 5ci. USA. 2009; 106 (4): 1234-1238. DOI: 10.1073/pnas.0809600106.

2. Clauditz A., Resch A., Wieland K.P. et al. Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect. Immun. 2006; 74 (8): 4950-4953. DOI: 10.1128/iai.00204-06.

3. Margolis E., Yates A., Levin B.R. The ecology of nasal colonization of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus: the role of competition and interactions with host's immune response. BMC Microbiol. 2010; 10: 59. DOI: 10.1186/14712180-10-59.

4. Bogaert D., van Belkum A., Sluijter M. et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet. 2004; 363 (9424): 1871-1872. DOI: 10.1016/s0140-6736(04)16357-5.

5. Shiri T., Nunes M.C., Adrian P.V. et al. Interrelationship of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus colonization within and between pneumococcal-vaccine naive mother-child dyads. BMCInfect. Dis. 2013;13: 483. DOI: 10.1186/1471-2334-13-483.

6. Pericone C.D., Overweg K., Hermans P.W.M., Weiser J.N. Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect. Immun. 2000; 68 (7): 3990-3997. DOI: 10.1128/iai.68.7.3990-3997.2000.

7. Shakhnovich E.A., King S.J., Weiser J.N. Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of neisseria meningitidis and haemophilus influenzae : a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect. Immun. 2002; 70 (12): 7161-7164. DOI: 10.1128/iai.70.12.7161-7164.2002.

8. Tong H.H., James M., Grants I. et al. Comparison of structural changes of cell surface carbohydrates in the eustachian tube epithelium of chinchillas infected with a Streptococcus pneumoniae neuraminidase-deficient mutant or its isogenic parent strain. Microb. Pathog. 2001; 31 (6): 309-317. DOI: 10.1006/mpat.2001.0473.

9. Miller E.L., Abrudan M.I., Roberts I.S., Rozen D.E. Diverse ecological strategies are encoded by Streptococcus pneumoniae bacterio-cin-like peptides. Genome Biol. Evol. 2016; 8 (4): 1072-1090. DOI: 10.1093/gbe/evw055.

10. Lux T., Nuhn M., Hakenbeck R., Reichmann P. Diversity of bacte-riocins and activity spectrum in Streptococcus pneumoniae. J. Bac-teriol. 2007; 189 (21): 7741-7751. DOI: 10.1128/jb.00474-07.

11. Ikryannikova L.N., Malakhova M.V., Lominadze G.G. et al. Inhibitory effect of streptococci on the growth of M. catarrhalis strains and the diversity of putative bacteriocin-like gene loci in the genomes of S. pneumoniae and its relatives. AMB Express. 2017; 7 (1): 218. DOI: 10.1186/s13568-017-0521-z.

12. Hathaway L.J., Battig P., Reber S. et al. Streptococcus pneumoniae detects and responds to foreign bacterial peptide fragments in its environment. Open Biology. 2014; 4 (4): 130224. DOI: 10.1098/rsob.130224.

13. Iwase T., Uehara Y., Shinji H. et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010; 465 (7296): 346-349. DOI: 10.1038/nature09074.

14. Janek D., Zipperer A., Kulik A. et al. High frequency and diversity of antimicrobial activities produced by nasal Staphylococcus strains against bacterial competitors. PLo5 Pathog. 2016; 12 (8): e1005812. DOI: 10.1371/journal.ppat.1005812.

15. Yan M., Pamp S.J., Fukuyama J. et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe. 2013; 14 (6): 631-640. DOI: 10.1016/j.chom.2013.11.005.

16. Menberu M.A., Liu S., Cooksley C. et al. Corynebacterium accolens has antimicrobial activity against Staphylococcus aureus and Methicillin-resistant S. aureus pathogens isolated from the sinonasal niche of chronic rhinosinusitis patients. Pathogens. 2021; 10 (2): 207. DOI: 10.3390/pathogens10020207.

17. Abreu N.A., Nagalingam N.A., Song Y. et al. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci. Transl. Med. 2012; 4 (151): 151ra124. DOI: 10.1126/scitranslmed.3003783.

18. Hardy B.L., Dickey S.W., Plaut R.D. et al. Corynebacterium pseu-dodiphtheriticum exploits Staphylococcus aureus virulence components in a novel polymicrobial defense strategy. mBio. 2019; 10 (1): e02491-18. DOI: 10.1128/mbio.02491-18.

19. Kiryukhina N.V., Melnikov V.G., Suvorov A.V. et al. Use of Coryne-bacterium pseudodiphtheriticum for elimination of Staphylococcus aureus from the nasal cavity in volunteers exposed to abnormal microclimate and altered gaseous environment. Probiotics Antimicrob. Proteins. 2013; 5 (4): 233-238. DOI: 10.1007/s12602-013-9147-x.

20. Ramsey M.M., Freire M.O., Gabrilska R.A. et al. Staphylococcus aureus shifts toward commensalism in response to corynebacterium species. Front. Microbiol. 2016; 7: 1230. DOI: 10.3389/fmicb.2016.01230.

21. Stubbendieck R.M., May D.S., Chevrette M.G. et al. Competition among nasal bacteria suggests a role for Siderophore-mediated interactions in shaping the human nasal microbiota. Appl. Environ. Microbiol. 2019; 85 (10): e02406-18. DOI: 10.1128/AEM.02406-18.

22. Bomar L., Brugger S.D., Yost B.H. et al. Corynebacterium acco-lens releases antipneumococcal free fatty acids from human nostril and skin surface triacylglycerols. MBio. 2016; 7 (1): e01725-15. DOI: 10.1128/mbio.01725-15.

23. Wollenberg M.S., Claesen J., Escapa I.F. et al. Propionibacteri-um-produced coproporphyrin III induces Staphylococcus aureus aggregation and biofilm formation. MBio. 2014; 5 (4): e01286-14. DOI: 10.1128/mbio.01286-14.

24. Lo C.W., Lai Y.K., Liu Y.T. et al. Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting в-hemolysin and CAMP factor. J. Invest. Dermatol. 2011; 131 (2): 401-409. DOI: 10.1038/jid.2010.319.

25. Scholz C.F.P., Kilian M. The natural history of cutaneous propioni-bacteria, and reclassification of selected species within the genus Pro-pionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov. Int. J. Syst. Evol. Microbiol. 2016; 66 (11): 4422-4432. DOI: 10.1099/ijsem.0.001367.

26. Shu M., Wang Y., Yu J. et al. Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillin-resistant Staphylococcus aureus. PLoS One. 2013; 8 (2): e55380. DOI: 10.1371/journal.pone.0055380.

27. Wang Y., Kuo S., Shu M. et al. Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Appl. Microbiol. Biotechnol. 2014; 98 (1): 411-424. DOI: 10.1007/s00253-013-5394-8.

28. Christensen G.J.M., Scholz C.F.P., Enghild J. et al. Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis. BMC Genomics. 2016; 17: 152. DOI: 10.1186/s12864-016-2489-5.

29. Escapa I.F., Chen T., Huang Y. et al. New insights into human nostril microbiome from the expanded human oral microbiome database (eHOMD): a resource for the microbiome of the human aerodigestive tract. 2018; 3 (6): e00187-18. DOI: 10.1101/347013.

30. Laufer A.S., Metlay J.P., Gent J.F. et al. Microbial communities of the upper respiratory tract and otitis media in children. MBio. 2011; 2 (1): e00245-10. DOI: 10.1128/mbio.00245-10.

31. Brugger S.D., Eslami S.M., Pettigrew M.M. et al. Dolosigranulum pigrum cooperation and competition in human nasal microbiota. mSphere. 2020; 5 (5): е00852-20. DOI: 10.1128/mSphere.00852-20.

32. Tashiro M., Ciborowski P., Klenk H.D. et al. Role of Staphylococcus protease in the development of influenza pneumonia. Nature. 1987; 325 (6104): 536-537. DOI: 10.1038/325536a0.

33. Tashiro M., Ciborowski P., Reinacher M. et al. Synergistic role of staphylococcal proteases in the induction of influenza virus pathogenicity. Virology. 1987; 157 (2): 421-430. DOI: 10.1016/0042-6822(87)90284-4.

34. Ayala V.I., Teijaro J.R., Farber D.L. et al. Bordetella pertussis infection exacerbates influenza virus infection through pertussis toxin-mediated suppression of innate immunity. PLoS One. 2011; 6 (4): e19016. DOI: 10.1371/journal.pone.0019016.

35. van den Bergh M.R., Biesbroek G., Rossen J.W.A. et al. Associations between pathogens in the upper respiratory tract of young children: interplay between viruses and bacteria. PLoS One. 2012; 7 (10): e47711. DOI: 10.1371/journal.pone.0047711.

36. de Steenhuijsen Piters W.A.A., Heinonen S., Hasrat R. et al. Nasopharyngeal microbiota, host transcriptome, and disease severity in children with respiratory syncytial virus infection. Am. J. Re-spir. Crit. Care Med. 2016; 194 (9):1104-1115. DOI: 10.1164/rccm.201602-0220oc.

37. Short K.R., Vissers M., de Kleijn S. et al. Bacterial lipopolysaccharide inhibits influenza virus infection of human macrophages and the consequent induction of CD8+ T-cell immunity. J. Innate Immun. 2014; 6 (2): 129-139. DOI: 10.1159/000353905.

38. Abt M.C., Osborne L.C., Monticelli L.A. et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity. 2012; 37 (1): 158-170. DOI: 10.1016/j.immuni.2012.04.011.

39. Wang J., Li F., Sun R. et al. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat. Commun. 2013; 4: 2106. DOI: 10.1038/ncomms3106.

40. Kanmani P., Clua P., Vizoso-Pinto M.G. et al. Respiratory commensal bacteria Corynebacterium pseudodiphtheriticum Improves resistance of infant mice to respiratory syncytial virus and Streptococcus pneumoniae superinfection. Front. Microbiol. 2017; 8: 1613. DOI: 10.3389/fmicb.2017.01613.

41. McCullers J.A., Rehg J.E. Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J. Infect. Dis. 2002; 186 (3): 341-350. DOI: 10.1086/341462.

42. Nardelli C., Gentile I., Setaro M. et al. Nasopharyngeal microbiome signature in COVID-19 positive patients: can we definitively get a role to Fusobacterium periodonticum? Front. Cell. Infect. Microbiol. 2021; 11: 625581. DOI: 10.3389/fcimb.2021.625581.

43. Yoneda S., Loeser B., Feng J. et al. Ubiquitous sialometabolism present among oral fusobacteria. PLoS One. 2014; 9 (6): e99263. DOI: 10.1371/journal.pone.0099263.

44. Morniroli D., Gianni M.L., Consales A. et al. Human Sialome and Coronavirus disease-2019 (COVID-19) pandemic: an understated correlation? Front. Immunol. 2020; 11: 1480. DOI: 10.3389/fim-mu.2020.01480.

45. Honarmand Ebrahimi K. SARS-CoV-2 spike glycoprotein-binding proteins expressed by upper respiratory tract bacteria may prevent severe viral infection. FEBS Lett. 2020; 594 (11): 1651-1660. DOI: 10.1002/1873-3468.13845.

46. Harvey H.A., Swords W.E., Apicella M.A. The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J. Autoimmun. 2001: 16 (3): 257-262. DOI: 10.1006/jaut.2000.0477.

47. Rosas-Salazar C., Kimura K.S., Shilts M.H. et al. SARS-CoV-2 infection and viral load are associated with the upper respiratory tract microbiome. J. Allergy Clin. Immunol. 2021; 147 (4): 1226-1233.e2. DOI: 10.1016/j.jaci.2021.02.001.

48. Feehan A.K., Rose R., Nolan D.J. et al. Nasopharyngeal microbiome community composition and structure is associated with severity of COVID-19 disease and breathing treatment. Appl. Microbiol. 2021; 1 (2): 177-188. DOI: 10.3390/applmicrobiol1020014.

49. De Maio F., Posteraro B., Ponziani F.R. et al. Nasopharyngeal microbiota profiling of SARS-CoV-2 infected patients. Biol. Proced. Online. 2020; 22: 18. DOI: 10.1186/s12575-020-00131-7.

50. Zhang H., Ai J.W., Yang W. et al. Metatranscriptomic characterization of coronavirus disease 2019 identified a host transcriptional classifier associated with immune signaling. Clin. Infect. Dis. 2021; 73 (3): 376-385. DOI: 10.1093/cid/ciaa663.

51. Engen P.A., Naqib A., Jennings C. et al. Nasopharyngeal microbiota in SARS-CoV-2 positive and negative patients. Biol. Proced. Online. 2021; 23 (1): 10. DOI: 10.1186/s12575-021-00148-6.

52. Liu J., Liu S., Zhang Z. et al. Association between the nasopharyngeal microbiome and metabolome in patients with COVID-19. Synth. Syst. Biotechnol. 2021; 6 (3): 135-143. DOI: 10.1016/j.synbio.2021.06.002.

53. Ma S., Zhang F., Zhou F. et al. Metagenomic analysis reveals oropharyngeal microbiota alterations in patients with COVID-19. Signal Transduct. Target. Ther. 2021; 6 (1): 191. DOI: 10.1038/s41392-021-00614-3.


Supplementary files

Review

For citations:


Starikova E.V., Galeeva Yu.S., Il’ina E.N. The upper respiratory tract microbiome and its role in human health: barrier function. PULMONOLOGIYA. 2022;32(6):876-884. (In Russ.) https://doi.org/10.18093/0869-0189-2022-32-6-876-884

Views: 529


ISSN 0869-0189 (Print)
ISSN 2541-9617 (Online)