1887

Abstract

is a skin and mucous commensal bacterium of warm-blooded animals. In humans, the nose is the main ecological niche of , and nasal carriage is a risk factor for developing an endogenous infection. nasal colonization is a multifactorial process, involving inter-species interactions among the nasal microbiota.

The objectives of this study were to characterize the microbiota of carriers and non-carriers of and to demonstrate the importance of inter-species relationships in the adhesion of , a key step in nasal colonization.

First, we characterized the nasal microbiota from 30 carriers and non-carriers by a culturomic approach. We then evaluated the adhesion of , first alone and then along with other bacteria of the nasal microbiota. To do that, we used an model to measure the interactions among bacteria in the presence of epithelial cells.

Analysis of the nasal microbiota of the carriers and non-carriers of made it possible to observe that each microbiota has specific features in terms of composition. However, this composition differs significantly between carriers and non-carriers mainly through two bacterial groups: coagulase-negative staphylococci and corynebacteria. In a second part, adhesion of to epithelial cells showed competition between and these bacteria, suggesting a limitation of nasal colonization by .

These findings demonstrate the existence of a negative correlation between and other species which inhibits adhesion and could limit nasal colonization.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001248
2020-09-10
2020-09-18
Loading full text...

Full text loading...

References

  1. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005; 5:751–762 [CrossRef][PubMed]
    [Google Scholar]
  2. Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus?. Trends Microbiol 2001; 9:605–610 [CrossRef][PubMed]
    [Google Scholar]
  3. von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 2001; 344:11–16 [CrossRef][PubMed]
    [Google Scholar]
  4. Kluytmans JAJW, Wertheim HFL. Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections. Infection 2005; 33:3–8 [CrossRef][PubMed]
    [Google Scholar]
  5. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S et al. Systematic literature analysis and review of targeted preventive measures to limit healthcare-associated infections by meticillin-resistant Staphylococcus aureus. Euro Surveill 2014; 19: [CrossRef]
    [Google Scholar]
  6. Biswas K, Hoggard M, Jain R, Taylor MW, Douglas RG. The nasal microbiota in health and disease: variation within and between subjects. Front Microbiol 2015; 9:134 [CrossRef][PubMed]
    [Google Scholar]
  7. Kaspar U, Kriegeskorte A, Schubert T, Peters G, Rudack C et al. The culturome of the human nose habitats reveals individual bacterial fingerprint patterns. Environ Microbiol 2016; 18:2130–2142 [CrossRef][PubMed]
    [Google Scholar]
  8. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI et al. Bacterial community variation in human body habitats across space and time. Science 2009; 326:1694–1697 [CrossRef][PubMed]
    [Google Scholar]
  9. Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN et al. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One 2010; 5:e10598 [CrossRef][PubMed]
    [Google Scholar]
  10. Yan M, Pamp SJ, Fukuyama J, Hwang PH, Cho D-Y et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 2013; 14:631–640 [CrossRef][PubMed]
    [Google Scholar]
  11. Oh J, Conlan S, Polley EC, Segre JA, Kong HH. Shifts in human skin and nares microbiota of healthy children and adults. Genome Med 2012; 4:77 [CrossRef][PubMed]
    [Google Scholar]
  12. Camarinha-Silva A, Jáuregui R, Chaves-Moreno D, Oxley APA, Schaumburg F et al. Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol 2014; 16:2939–2952 [CrossRef][PubMed]
    [Google Scholar]
  13. Liu CM, Price LB, Hungate BA, Abraham AG, Larsen LA et al. Staphylococcus aureus and the ecology of the nasal microbiome. Sci Adv 2015; 1:e1400216 [CrossRef][PubMed]
    [Google Scholar]
  14. Wos-Oxley ML, Plumeier I, von Eiff C, Taudien S, Platzer M et al. A poke into the diversity and associations within human anterior nare microbial communities. ISME J 2010; 4:839–851 [CrossRef][PubMed]
    [Google Scholar]
  15. Lina G, Boutite F, Tristan A, Bes M, Etienne J et al. Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbiol 2003; 69:18–23 [CrossRef][PubMed]
    [Google Scholar]
  16. Libberton B, Coates RE, Brockhurst MA, Horsburgh MJ. Evidence that intraspecific trait variation among nasal bacteria shapes the distribution of Staphylococcus aureus. Infect Immun 2014; 82:3811–3815 [CrossRef][PubMed]
    [Google Scholar]
  17. Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 2016; 535:511–516 [CrossRef][PubMed]
    [Google Scholar]
  18. Almeida RA, Matthews KR, Cifrian E, Guidry AJ, Oliver SP. Staphylococcus aureus invasion of bovine mammary epithelial cells. J Dairy Sci 1996; 79:1021–1026 [CrossRef][PubMed]
    [Google Scholar]
  19. Lindsay JA, Riley TV. Susceptibility to desferrioxamine: a new test for the identification of Staphylococcus epidermidis. J Med Microbiol 1991; 35:45–48 [CrossRef][PubMed]
    [Google Scholar]
  20. Ranc A-G. Microbiote nasal et portage Staphylococcus aureus, Thèse d’exercice. Université Claude Bernard; 2013
    [Google Scholar]
  21. Dusko Ehrlich S. Metagenomics of the intestinal microbiota: potential applications. Gastroenterol Clin Biol 2010; 34:S23–S28 [CrossRef]
    [Google Scholar]
  22. Bogaert D, van Belkum A, Sluijter M, Luijendijk A, de Groot R et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 2004; 363:1871–1872 [CrossRef][PubMed]
    [Google Scholar]
  23. Rasmussen TT, Kirkeby LP, Poulsen K, Reinholdt J, Kilian M. Resident aerobic microbiota of the adult human nasal cavity. APMIS 2000; 108:663–675 [CrossRef][PubMed]
    [Google Scholar]
  24. Sollid JUE, Furberg AS, Hanssen AM, Johannessen M. Staphylococcus aureus: determinants of human carriage. Infect Genet Evol 2014; 21:531–541 [CrossRef][PubMed]
    [Google Scholar]
  25. Weidenmaier C, Goerke C, Wolz C. Staphylococcus aureus determinants for nasal colonization. Trends Microbiol 2012; 20:243–250 [CrossRef][PubMed]
    [Google Scholar]
  26. Wertheim HFL, van Kleef M, Vos MC, Ott A, Verbrugh HA et al. Nose picking and nasal carriage of Staphylococcus aureus. Infect Control Hosp Epidemiol 2006; 27:863–867 [CrossRef][PubMed]
    [Google Scholar]
  27. Nouwen JL, Ott A, Kluytmans-Vandenbergh MFQ, Boelens HAM, Hofman A et al. Predicting the Staphylococcus aureus nasal carrier state: derivation and validation of a "culture rule". Clin Infect Dis 2004; 39:806–811 [CrossRef][PubMed]
    [Google Scholar]
  28. van Belkum A, Verkaik NJ, de Vogel CP, Boelens HA, Verveer J et al. Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 2009; 199:1820–1826 [CrossRef][PubMed]
    [Google Scholar]
  29. Köck R, Werner P, Friedrich AW, Fegeler C, Becker K et al. Persistence of nasal colonization with human pathogenic bacteria and associated antimicrobial resistance in the German general population. New Microbes New Infect 2016; 9:24–34 [CrossRef][PubMed]
    [Google Scholar]
  30. Uehara Y, Nakama H, Agematsu K, Uchida M, Kawakami Y et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect 2000; 44:127–133 [CrossRef][PubMed]
    [Google Scholar]
  31. Donker GA, Deurenberg RH, Driessen C, Sebastian S, Nys S et al. The population structure of Staphylococcus aureus among general practice patients from the Netherlands. Clin Microbiol Infect 2009; 15:137–143 [CrossRef][PubMed]
    [Google Scholar]
  32. Muthukrishnan G, Lamers RP, Ellis A, Paramanandam V, Persaud AB et al. Longitudinal genetic analyses of Staphylococcus aureus nasal carriage dynamics in a diverse population. BMC Infect Dis 2013; 13:221 [CrossRef][PubMed]
    [Google Scholar]
  33. Askarian F, Ajayi C, Hanssen A-M, van Sorge NM, Pettersen I et al. The interaction between Staphylococcus aureus SdrD and desmoglein 1 is important for adhesion to host cells. Sci Rep 2016; 6:22134 [CrossRef][PubMed]
    [Google Scholar]
  34. Bouchard DS, Rault L, Berkova N, Le Loir Y, Even S. Inhibition of Staphylococcus aureus invasion into bovine mammary epithelial cells by contact with live Lactobacillus casei. Appl Environ Microbiol 2013; 79:877–885 [CrossRef][PubMed]
    [Google Scholar]
  35. Lin MH, Shu JC, Lin LP, Chong KY, Cheng YW et al. Elucidating the crucial role of poly N-acetylglucosamine from Staphylococcus aureus in cellular adhesion and pathogenesis. PLoS One 2015; 10:e0124216 [CrossRef][PubMed]
    [Google Scholar]
  36. Burian M, Wolz C, Goerke C. Regulatory adaptation of Staphylococcus aureus during nasal colonization of humans. PLoS One 2010; 5:e10040 [CrossRef][PubMed]
    [Google Scholar]
  37. Foster TJ, Geoghegan JA, Ganesh VK, Höök M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 2014; 12:49–62 [CrossRef][PubMed]
    [Google Scholar]
  38. Yarwood JM, Schlievert PM. Quorum sensing in Staphylococcus infections. J Clin Invest 2003; 112:1620–1625 [CrossRef][PubMed]
    [Google Scholar]
  39. Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 2003; 48:1429–1449 [CrossRef][PubMed]
    [Google Scholar]
  40. Roche FM, Massey R, Peacock SJ, Day NPJ, Visai L et al. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 2003; 149:643–654 [CrossRef][PubMed]
    [Google Scholar]
  41. Chiller K, Selkin BA, Murakawa GJ. Skin microflora and bacterial infections of the skin. J Investig Dermatol Symp Proc 2001; 6:170–174 [CrossRef][PubMed]
    [Google Scholar]
  42. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010; 465:346–349 [CrossRef][PubMed]
    [Google Scholar]
  43. Sugimoto S, Iwamoto T, Takada K, Okuda K-I, Tajima A et al. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J Bacteriol 2013; 195:1645–1655 [CrossRef][PubMed]
    [Google Scholar]
  44. Wollenberg MS, Claesen J, Escapa IF, Aldridge KL, Fischbach MA et al. Propionibacterium-produced coproporphyrin III induces Staphylococcus aureus aggregation and biofilm formation. mBio 2014; 5:e01286–01214 [CrossRef][PubMed]
    [Google Scholar]
  45. Lo C-W, Lai Y-K, Liu Y-T, Gallo RL, Huang C-M. Staphylococcus aureus hijacks a skin commensal to intensify its virulence: immunization targeting β-hemolysin and CAMP factor. J Invest Dermatol 2011; 131:401–409 [CrossRef][PubMed]
    [Google Scholar]
  46. Collado MC, Meriluoto J, Salminen S. Measurement of aggregation properties between probiotics and pathogens: in vitro evaluation of different methods. J Microbiol Methods 2007; 71:71–74 [CrossRef][PubMed]
    [Google Scholar]
  47. Vesterlund S, Karp M, Salminen S, Ouwehand AC. Staphylococcus aureus adheres to human intestinal mucus but can be displaced by certain lactic acid bacteria. Microbiology 2006; 152:1819–1826 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001248
Loading
/content/journal/jmm/10.1099/jmm.0.001248
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error