The commensal lifestyle of Staphylococcus aureus and its interactions with the nasal microbiota

Nature Reviews Microbiology

Volumn 15, Issue 11, 2017, Pages 675-687

  Krismer, Bernhard ^a,b   Weidenmaier, Christopher ^a,b   Zipperer, Alexander ^a,b   Peschel, Andreas ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b German Centre for Infection Research (DZIF)   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN;

ANTIBIOSIS; CHEMICAL COMPOSITION; ENVIRONMENTAL FACTOR; EPITHELIUM; HOST RESISTANCE; INTRASPECIFIC COMPETITION; MICROFLORA; NONHUMAN; NOSE; NUTRIENT; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCUS AUREUS; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HOST PATHOGEN INTERACTION; HUMAN; MICROBIOLOGY; MOLECULAR MODEL; MULTIDRUG RESISTANCE; NOSE CAVITY; PHYSIOLOGY; RISK FACTOR; STAPHYLOCOCCAL INFECTIONS;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROBIOTA; MODELS, MOLECULAR; NASAL CAVITY; NOSE; RISK FACTORS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 85031308721     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro.2017.104     Document Type: Review

References (158)

1. Tacconelli, E., Autenrieth, I. B., & Peschel, A. Fighting the enemy within. Science 355, 689-690 (2017
2. Weidenmaier, C., Goerke, C., & Wolz, C. Staphylococcus aureus determinants for nasal colonization. Trends Microbiol. 20, 243-250 (2012
3. Brugger, S. D., Bomar, L., & Lemon, K. P. Commensal- pathogen interactions along the human nasal passages. PLoS Pathog. 12, e1005633 (2016
4. Mulcahy, M. E., & McLoughlin, R. M. Host-bacterial crosstalk determines Staphylococcus aureus nasal colonization. Trends Microbiol. 24, 872-886 (2016
5. Bode, L. G., et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N. Engl. J. Med. 362, 9-17 (2010
6. von Eiff, C., Becker, K., Machka, K., Stammer, H., & Peters, G. Nasal carriage as a source of Staphylococcus aureus bacteremia. N. Engl. J. Med. 344, 11-16 (2001
7. Septimus, E. J., & Schweizer, M. L. Decolonization in prevention of health care-Associated infections. Clin. Microbiol. Rev. 29, 201-222 (2016
8. Poovelikunnel, T., Gethin, G., & Humphreys, H. Mupirocin resistance: clinical implications and potential alternatives for the eradication of MRSA. J. Antimicrob. Chemother. 70, 2681-2692 (2015
9. Antonov, N. K., et al. High prevalence of mupirocin resistance in Staphylococcus aureus isolates from a pediatric population. Antimicrob. Agents Chemother. 59, 3350-3356 (2015
10. Fischbach, M. A., & Segre, J. A. Signaling in host-Associated microbial communities. Cell 164, 1288-1300 (2016
11. Liu, C. M., et al. Staphylococcus aureus and the ecology of the nasal microbiome. Sci. Adv. 1, e1400216 (2015
12. Wos-Oxley, M. L., et al. A poke into the diversity and associations within human anterior nare microbial communities. ISME J. 4, 839-851 (2010
13. Kluytmans, J., van Belkum, A., & Verbrugh, H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10, 505-520 (1997
14. Costello, E. K., et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694-1697 (2009
15. Frank, D. N., et al. The human nasal microbiota and Staphylococcus aureus carriage. PLoS ONE 5, e10598 (2010
16. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012
17. Yan, M., et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 14, 631-640 (2013
18. Grice, E. A., et al. Topographical and temporal diversity of the human skin microbiome. Science 324, 1190-1192 (2009
19. Ravel, J., et al. Vaginal microbiome of reproductive-Age women. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4680-4687 (2011
20. Segata, N., et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 13, R42 (2012
21. Bokulich, N. A., et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57-59 (2013
22. Warnecke, F., et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565 (2007
23. Kaspar, U., et al. The culturome of the human nose habitats reveals individual bacterial fingerprint patterns. Environ. Microbiol. 18, 2130-2142 (2016
24. Misic, A. M., et al. The shared microbiota of humans and companion animals as evaluated from Staphylococcus carriage sites. Microbiome 3, 2 (2015
25. Weese, J. S., Slifierz, M., Jalali, M., & Friendship, R. Evaluation of the nasal microbiota in slaughter-Age pigs and the impact on nasal methicillin-resistant Staphylococcus aureus (MRSA) carriage. BMC Vet. Res. 10, 69 (2014
26. Chaves-Moreno, D., et al. The microbial community structure of the cotton rat nose. Environ. Microbiol. Rep. 7, 929-935 (2015
27. Bal, A. M., et al. Genomic insights into the emergence and spread of international clones of healthcare-, community- And livestock-Associated meticillin-resistant Staphylococcus aureus: blurring of the traditional definitions. J. Glob. Antimicrob. Resist. 6, 95-101 (2016
28. Peterson, S. W., et al. A study of the infant nasal microbiome development over the first year of life and in relation to their primary adult caregivers using cpn60 universal target (UT) as a phylogenetic marker. PLoS ONE 11, e0152493 (2016
29. Man, W. H., de Steenhuijsen Piters, W. A., & Bogaert, D. The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat. Rev. Microbiol. 15, 259-270 (2017
30. Biesbroek, G., et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am. J. Respir. Crit. Care Med. 190, 1283-1292 (2014
31. Faust, K., et al. Microbial co occurrence relationships in the human microbiome. PLoS Comput. Biol. 8, e1002606 (2012
32. Lemon, K. P., et al. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. mBio 1, e00129 10 (2010
33. Becker, K., Heilmann, C., & Peters, G. Coagulase-negative staphylococci. Clin. Microbiol. Rev. 27, 870-926 (2014
34. Camarinha-Silva, A., Jauregui, R., Pieper, D. H., & Wos-Oxley, M. L. The temporal dynamics of bacterial communities across human anterior nares. Environ. Microbiol. Rep. 4, 126-132 (2012
35. Olsen, K., et al. Staphylococcus aureus nasal carriage is associated with serum 25 hydroxyvitamin D levels, gender and smoking status. The Tromso Staph and Skin Study. Eur. J. Clin. Microbiol. Infect. Dis. 31, 465-473 (2012
36. Shukla, S. K., Rose, W., & Schrodi, S. J. Complex host genetic susceptibility to Staphylococcus aureus infections. Trends Microbiol. 23, 529-536 (2015
37. Andersen, P. S., et al. Influence of host genetics and environment on nasal carriage of Staphylococcus aureus in Danish middle-Aged and elderly twins. J. Infect. Dis. 206, 1178-1184 (2012
38. Camarinha-Silva, A., et al. Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ. Microbiol. 16, 2939-2952 (2014
39. Mirzaei, M. K., & Maurice, C. F. Menage a trois in the human gut: interactions between host, bacteria and phages. Nat. Rev. Microbiol. 15, 397-408 (2017
40. Oh, J., et al. Biogeography and individuality shape function in the human skin metagenome. Nature 514, 59-64 (2014
41. McCarthy, A. J., et al. Extensive horizontal gene transfer during Staphylococcus aureus co colonization in vivo. Genome Biol. Evol. 6, 2697-2708 (2014
42. Winstel, V., et al. Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat. Commun. 4, 2345 (2013
43. Schade, J., & Weidenmaier, C. Cell wall glycopolymers of Firmicutes and their role as nonprotein adhesins. FEBS Lett. 590, 3758-3771 (2016
44. Geoghegan, J. A., & Foster, T. J. Cell wall-Anchored surface proteins of Staphylococcus aureus: many proteins, multiple functions. Curr. Top. Microbiol. Immunol. http://dx.doi.org/10.1007/82-2015-5002 (2015
45. Corrigan, R. M., Miajlovic, H., & Foster, T. J. Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol. 9, 22 (2009
46. Baur, S., et al. A nasal epithelial receptor for Staphylococcus aureus WTA governs adhesion to epithelial cells and modulates nasal colonization. PLoS Pathog. 10, e1004089 (2014
47. Weidenmaier, C., et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10, 243-245 (2004
48. Mulcahy, M. E., et al. Nasal colonisation by Staphylococcus aureus depends upon clumping factor B binding to the squamous epithelial cell envelope protein loricrin. PLoS Pathog. 8, e1003092 (2012
49. Krismer, B., & Peschel, A. Does Staphylococcus aureus nasal colonization involve biofilm formation?. Future Microbiol. 6, 489-493 (2011
50. Wollenberg, M. S., et al. Propionibacterium-produced coproporphyrin III induces Staphylococcus aureus aggregation and biofilm formation. mBio 5, e01286 14 (2014
51. Burian, M., et al. Temporal expression of adhesion factors and activity of global regulators during establishment of Staphylococcus aureus nasal colonization. J. Infect. Dis. 201, 1414-1421 (2010
52. Foster, T. J., Geoghegan, J. A., Ganesh, V. K., & Hook, M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12, 49-62 (2014
53. Weidenmaier, C., & Peschel, A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6, 276-287 (2008
54. Neuhaus, F. C., & Baddiley, J. A continuum of anionic charge: structures and functions of d alanyl-Teichoic acids in Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 686-723 (2003
55. Winstel, V., et al. Wall teichoic acid glycosylation governs Staphylococcus aureus nasal colonization. mBio 6, e00632 15 (2015
56. Weidenmaier, C., & Lee, J. C. Structure and function of surface polysaccharides of Staphylococcus aureus. Curr. Top. Microbiol. Immunol. http://dx.doi.org/.10.1007/82-2015-5018 (2016
57. Cole, A. M., et al. Determinants of Staphylococcus aureus nasal carriage. Clin. Diagn. Lab Immunol. 8, 1064-1069 (2001
58. Ten Broeke-Smits, N. J., Kummer, J. A., Bleys, R. L., Fluit, A. C., & Boel, C. H. Hair follicles as a niche of Staphylococcus aureus in the nose; is a more effective decolonisation strategy needed?. J. Hosp. Infect. 76, 211-214 (2010
59. O?Brien, L. M., Walsh, E. J., Massey, R. C., Peacock, S. J., & Foster, T. J. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell. Microbiol. 4, 759-770 (2002
60. Clarke, S. R., et al. Iron-regulated surface determinant protein A mediates adhesion of Staphylococcus aureus to human corneocyte envelope proteins. Infect. Immun. 77, 2408-2416 (2009
61. Askarian, F., et al. The interaction between Staphylococcus aureus SdrD and desmoglein 1 is important for adhesion to host cells. Sci. Rep. 6, 22134 (2016
62. Shuter, J., Hatcher, V. B., & Lowy, F. D. Staphylococcus aureus binding to human nasal mucin. Infect. Immun. 64, 310-318 (1996
63. Le, K. Y., & Otto, M. Quorum-sensing regulation in staphylococci - An overview. Front. Microbiol. 6, 1174 (2015
64. Pynnonen, M., Stephenson, R. E., Schwartz, K., Hernandez, M., & Boles, B. R. Hemoglobin promotes Staphylococcus aureus nasal colonization. PLoS Pathog. 7, e1002104 (2011
65. Ramsey, M. M., Freire, M. O., Gabrilska, R. A., Rumbaugh, K. P., & Lemon, K. P. Staphylococcus aureus shifts toward commensalism in response to Corynebacterium species. Front. Microbiol. 7, 1230 (2016
66. Iwase, T., et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465, 346-349 (2010
67. Sugimoto, S., et al. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host- pathogen interaction. J. Bacteriol. 195, 1645-1655 (2013
68. Roche, F. M., Meehan, M., & Foster, T. J. The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149, 2759-2767 (2003
69. Zapotoczna, M., Heilbronner, S., Speziale, P., & Foster, T. J. Iron-regulated surface determinant (Isd) proteins of Staphylococcus lugdunensis. J. Bacteriol. 194, 6453-6467 (2012
70. Krismer, B., et al. Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog. 10, e1003862 (2014
71. Vanthanouvong, V., & Roomans, G. M. Methods for determining the composition of nasal fluid by X ray microanalysis. Microsc. Res. Tech. 63, 122-128 (2004
72. Chaves-Moreno, D., et al. Exploring the transcriptome of Staphylococcus aureus in its natural niche. Sci. Rep. 6, 33174 (2016
73. Ahluwalia, A., et al. Nasal colonization with Staphylococcus aureus in patients with diabetes mellitus. Diabet Med. 17, 487-488 (2000
74. Olson, M. E., King, J. M., Yahr, T. L., & Horswill, A. R. Sialic acid catabolism in Staphylococcus aureus. J. Bacteriol. 195, 1779-1788 (2013
75. Bruggemann, H., et al. The complete genome sequence of Propionibacterium acnes, a commensal of human skin. Science 305, 671-673 (2004
76. King, S. J., et al. Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol. Microbiol. 54, 159-171 (2004
77. Vimr, E., & Lichtensteiger, C. To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10, 254-257 (2002
78. Vimr, E. R., Kalivoda, K. A., Deszo, E. L., & Steenbergen, S. M. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68, 132-153 (2004
79. Jorge, A. M., et al. Utilization of glycerophosphodiesters by Staphylococcus aureus. Mol. Microbiol. 103, 229-241 (2017
80. Casado, B., Pannell, L. K., Iadarola, P., & Baraniuk, J. N. Identification of human nasal mucous proteins using proteomics. Proteomics 5, 2949-2959 (2005
81. Tomazic, P. V., et al. Nasal mucus proteomic changes reflect altered immune responses and epithelial permeability in patients with allergic rhinitis. J. Allergy Clin. Immunol. 133, 741-750 (2014
82. Koziel, J., & Potempa, J. Protease-Armed bacteria in the skin. Cell Tissue Res. 351, 325-337 (2013
83. Dubin, G., et al. Molecular cloning and biochemical characterisation of proteases from Staphylococcus epidermidis. Biol. Chem. 382, 1575-1582 (2001
84. Wysocki, A. B., et al. Proteolytic activity by multiple bacterial species isolated from chronic venous leg ulcers degrades matrix substrates. Biol. Res. Nurs. 15, 407-415 (2013
85. Lanter, B. B., & Davies, D. G. Propionibacterium acnes recovered from atherosclerotic human carotid arteries undergoes biofilm dispersion and releases lipolytic and proteolytic enzymes in response to norepinephrine challenge in vitro. Infect. Immun. 83, 3960-3971 (2015
86. Arnison, P. G., et al. Ribosomally synthesized and post-Translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat. Prod. Rep. 30, 108-160 (2013
87. Janek, D., Zipperer, A., Kulik, A., Krismer, B., & Peschel, A. High frequency and diversity of antimicrobial activities produced by nasal Staphylococcus strains against bacterial competitors. PLoS Pathog. 12, e1005812 (2016
88. Bierbaum, G., & Sahl, H. G. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr. Pharm. Biotechnol. 10, 2-18 (2009
89. Sashihara, T., et al. A novel lantibiotic, nukacin ISK 1, of Staphylococcus warneri ISK 1: cloning of the structural gene and identification of the structure. Biosci. Biotechnol. Biochem. 64, 2420-2428 (2000
90. Wilaipun, P., Zendo, T., Okuda, K., Nakayama, J., & Sonomoto, K. Identification of the nukacin KQU 131, a new type A(II) lantibiotic produced by Staphylococcus hominis KQU 131 isolated from Thai fermented fish product (Pla ra). Biosci. Biotechnol. Biochem. 72, 2232-2235 (2008
91. Navaratna, M. A., Sahl, H. G., & Tagg, J. R. Two-component anti-Staphylococcus aureus lantibiotic activity produced by Staphylococcus aureus C55. Appl. Environ. Microbiol. 64, 4803-4808 (1998
92. Navaratna, M. A., Sahl, H. G., & Tagg, J. R. Identification of genes encoding two-component lantibiotic production in Staphylococcus aureus C55 and other phage group II S. aureus strains and demonstration of an association with the exfoliative toxin B gene. Infect. Immun. 67, 4268-4271 (1999
93. Nakatsuji, T., et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci. Transl Med. 9, eaah4680 (2017
94. Bennallack, P. R., Burt, S. R., Heder, M. J., Robison, R. A., & Griffitts, J. S. Characterization of a novel plasmid-borne thiopeptide gene cluster in Staphylococcus epidermidis strain 115. J. Bacteriol. 196, 4344-4350 (2014
95. Li, Y. M., Milne, J. C., Madison, L. L., Kolter, R., & Walsh, C. T. From peptide precursors to oxazole and thiazole-containing peptide antibiotics: microcin B17 synthase. Science 274, 1188-1193 (1996
96. Netz, D. J., et al. Molecular characterisation of aureocin A70, a multi-peptide bacteriocin isolated from Staphylococcus aureus. J. Mol. Biol. 311, 939-949 (2001
97. Miescher, S., Stierli, M. P., Teuber, M., & Meile, L. Propionicin SM1, a bacteriocin from Propionibacterium jensenii DF1: isolation and characterization of the protein and its gene. Syst. Appl. Microbiol. 23, 174-184 (2000
98. Attia, A. S., et al. Identification of a bacteriocin and its cognate immunity factor expressed by Moraxella catarrhalis. BMC Microbiol. 9, 207 (2009
99. Fujimura, S., & Nakamura, T. Purification and properties of a bacteriocin-like substance (acnecin) of oral Propionibacterium acnes. Antimicrob. Agents Chemother. 14, 893-898 (1978
100. Tauch, A., et al. Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora. J. Bacteriol. 187, 4671-4682 (2005
101. Donia, M. S., et al. A systematic analysis of biosynthetic gene clusters in the human microbiome reveals a common family of antibiotics. Cell 158, 1402-1414 (2014
102. Zipperer, A., et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 535, 511-516 (2016
103. Heilbronner, S., et al. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 322, 60-67 (2011
104. Bogaert, D., et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 363, 1871-1872 (2004
105. Regev-Yochay, G., et al. Association between carriage of Streptococcus pneumoniae and Staphylococcus aureus in children. JAMA 292, 716-720 (2004
106. Selva, L., et al. Killing niche competitors by remote-control bacteriophage induction. Proc. Natl Acad. Sci. USA 106, 1234-1238 (2009
107. Uehara, Y., et al. H2O2 produced by viridans group streptococci may contribute to inhibition of methicillin-resistant Staphylococcus aureus colonization of oral cavities in newborns. Clin. Infect. Dis. 32, 1408-1413 (2001
108. Lijek, R. S., et al. Protection from the acquisition of Staphylococcus aureus nasal carriage by cross-reactive antibody to a pneumococcal dehydrogenase. Proc. Natl Acad. Sci. USA 109, 13823-13828 (2012
109. Hanzelmann, D., et al. Toll-like receptor 2 activation depends on lipopeptide shedding by bacterial surfactants. Nat. Commun. 7, 12304 (2016
110. Riechelmann, H., et al. Nasal carriage of Staphylococcus aureus in house dust mite allergic patients and healthy controls. Allergy 60, 1418-1423 (2005
111. Cole, A. M., et al. Cationic polypeptides are required for antibacterial activity of human airway fluid. J. Immunol. 169, 6985-6991 (2002
112. Herbert, S., et al. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3, e102 (2007
113. Bera, A., et al. Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J. Bacteriol. 189, 280-283 (2007
114. Hoq, M. I., & Ibrahim, H. R. Potent antimicrobial action of triclosan-lysozyme complex against skin pathogens mediated through drug-Targeted delivery mechanism. Eur. J. Pharm. Sci. 42, 130-137 (2011
115. Peschel, A., & Sahl, H. G. The co evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4, 529-536 (2006
116. Harder, J., & Schroder, J. M. RNase 7, a novel innate immune defense antimicrobial protein of healthy human skin. J. Biol. Chem. 277, 46779-46784 (2002
117. Lee, D. Y., et al. Sebocytes express functional cathelicidin antimicrobial peptides and can act to kill Propionibacterium acnes. J. Invest. Dermatol. 128, 1863-1866 (2008
118. Cole, A. L., et al. Host innate inflammatory factors and staphylococcal protein A influence the duration of human Staphylococcus aureus nasal carriage. Mucosal Immunol. 9, 1537-1548 (2016
119. Kiser, K. B., Cantey-Kiser, J. M., & Lee, J. C. Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect. Immun. 67, 5001-5006 (1999
120. Boris, M., et al. Bacterial interference; protection of adults against nasal Staphylococcus aureus infection after colonization with a heterologous S. aureus strain. Am. J. Dis. Child 108, 252-261 (1964
121. Houck, P. W., Nelson, J. D., & Kay, J. L. Fatal septicemia due to Staphylococcus aureus 502A. Report of a case and review of the infectious complications of bacterial interference programs. Am. J. Dis. Child 123, 45-48 (1972
122. Uehara, Y., et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J. Hosp. Infect. 44, 127-133 (2000
123. Kommineni, S., et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526, 719-722 (2015
124. Schaffer, A. C., et al. Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect. Immun. 74, 2145-2153 (2006
125. Dorrestein, P. C., Mazmanian, S. K., & Knight, R. Finding the missing links among metabolites, microbes, and the host. Immunity 40, 824-832 (2014
126. Belkaid, Y., & Segre, J. A. Dialogue between skin microbiota and immunity. Science 346, 954-959 (2014
127. Davis, M. F., Peng, R. D., McCormack, M. C., & Matsui, E. C. Staphylococcus aureus colonization is associated with wheeze and asthma among US children and young adults. J. Allergy Clin. Immunol. 135, 811-813.5 (2015
128. Nakamura, Y., et al. Staphylococcus delta-Toxin induces allergic skin disease by activating mast cells. Nature 503, 397-401 (2013
129. Stentzel, S., et al. Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J. Allergy Clin. Immunol. 139, 492-500.e8 (2017
130. Biswas, K., Hoggard, M., Jain, R., Taylor, M. W., & Douglas, R. G. The nasal microbiota in health and disease: variation within and between subjects. Front. Microbiol. 9, 134 (2015
131. Zhang, N., Van Crombruggen, K., Gevaert, E., & Bachert, C. Barrier function of the nasal mucosa in health and type 2 biased airway diseases. Allergy 71, 295-307 (2016
132. Geurkink, N. Nasal anatomy, physiology, and function. J. Allergy Clin. Immunol. 72, 123-128 (1983
133. de Borja Callejas, F., et al. Reconstituted human upper airway epithelium as 3D in vitro model for nasal polyposis. PLoS ONE 9, e100537 (2014
134. Even-Tzur, N., et al. Air-liquid interface culture of nasal epithelial cells on denuded amniotic membranes. Cell. Mol. Bioengineer. 3, 307-318 (2010
135. Becker, S. C., et al. Triple-Acting lytic enzyme treatment of drug-resistant and intracellular Staphylococcus aureus. Sci. Rep. 6, 25063 (2016
136. Kokai-Kun, J. F. The cotton rat as a model for Staphylococcus aureus nasal colonization in humans: cotton rat S. aureus nasal colonization model. Methods Mol. Biol. 431, 241-254 (2008
137. Niewiesk, S., & Prince, G. Diversifying animal models: the use of hispid cotton rats (Sigmodon hispidus) in infectious diseases. Lab Anim. 36, 357-372 (2002
138. van den Berg, S., et al. Rhesus macaques (Macaca mulatta) are natural hosts of specific Staphylococcus aureus lineages. PLoS ONE 6, e26170 (2011
139. Wertheim, H. F., et al. Effect of mupirocin treatment on nasal, pharyngeal, and perineal carriage of Staphylococcus aureus in healthy adults. Antimicrob. Agents Chemother. 49, 1465-1467 (2005
140. Wertheim, H. F., et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 5, e17 (2008
141. Hood, M. I., & Skaar, E. P. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537 (2012
142. Latunde-Dada, G. O. Iron metabolism: microbes, mouse, and man. Bioessays 31, 1309-1317 (2009
143. Beasley, F. C., & Heinrichs, D. E. Siderophore-mediated iron acquisition in the staphylococci. J. Inorg. Biochem. 104, 282-288 (2010
144. Sebulsky, M. T., Shilton, B. H., Speziali, C. D., & Heinrichs, D. E. The role of FhuD2 in iron(iii)- hydroxamate transport in Staphylococcus aureus. Demonstration that FhuD2 binds iron(iii)- hydroxamates but with minimal conformational change and implication of mutations on transport. J. Biol. Chem. 278, 49890-49900 (2003
145. Zajdowicz, S., et al. Purification and structural characterization of siderophore (corynebactin) from Corynebacterium diphtheriae. PLoS ONE 7, e34591 (2012
146. Bachman, M. A., Miller, V. L., & Weiser, J. N. Mucosal lipocalin 2 has pro-inflammatory and iron-sequestering effects in response to bacterial enterobactin. PLoS Pathog. 5, e1000622 (2009
147. Holden, V. I., et al. Bacterial siderophores that evade or overwhelm lipocalin 2 induce hypoxia inducible factor 1α and proinflammatory cytokine secretion in cultured respiratory epithelial cells. Infect. Immun. 82, 3826-3836 (2014
148. Bachman, M. A., et al. Klebsiella pneumoniae yersiniabactin promotes respiratory tract infection through evasion of lipocalin 2. Infect. Immun. 79, 3309-3316 (2011
149. Hammer, N. D., & Skaar, E. P. The impact of metal sequestration on Staphylococcus aureus metabolism. Curr. Opin. Microbiol. 15, 10-14 (2012
150. Sheldon, J. R., & Heinrichs, D. E. Recent developments in understanding the iron acquisition strategies of gram positive pathogens. FEMS Microbiol. Rev. 39, 592-630 (2015
151. Heilbronner, S., et al. Competing for iron: duplication and amplification of the isd locus in Staphylococcus lugdunensis HKU09 01 provides a competitive advantage to overcome nutritional limitation. PLoS Genet. 12, e1006246 (2016
152. Wilks, A., & Ikeda-Saito, M. Heme utilization by pathogenic bacteria: not all pathways lead to biliverdin. Acc. Chem. Res. 47, 2291-2298 (2014
153. Karalus, R., & Campagnari, A. Moraxella catarrhalis: a review of an important human mucosal pathogen. Microbes Infect. 2, 547-559 (2000
154. Tieu, D. D., et al. Evidence for diminished levels of epithelial psoriasin and calprotectin in chronic rhinosinusitis. J. Allergy Clin. Immunol. 125, 667-675 (2010
155. Garcia, Y. M., et al. A superoxide dismutase capable of functioning with iron or manganese promotes the resistance of Staphylococcus aureus to calprotectin and nutritional immunity. PLoS Pathog. 13, e1006125 (2017
156. Kato, T., Kouzaki, H., Matsumoto, K., Hosoi, J., & Shimizu, T. The effect of calprotectin on TSLP and IL 25 production from airway epithelial cells. Allergol Int. 66, 281-289 (2017
157. Kehl-Fie, T. E., et al. MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect. Immun. 81, 3395-3405 (2013
158. Ghssein, G., et al. Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science 352, 1105-1109 (2016