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Colonization of the Human Nose and Interaction with Other Microbiome Members

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  • Authors: Claudia Laux1, Andreas Peschel2, Bernhard Krismer3
  • Editors: Vincent A. Fischetti4, Richard P. Novick5, Joseph J. Ferretti6, Daniel A. Portnoy7, Miriam Braunstein8, Julian I. Rood9
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: University of Tübingen, Interfaculty Institute for Microbiology and Infection Medicine Tübingen, Infection Biology Unit, 72076 Tübingen, Germany; 2: University of Tübingen, Interfaculty Institute for Microbiology and Infection Medicine Tübingen, Infection Biology Unit, 72076 Tübingen, Germany; 3: University of Tübingen, Interfaculty Institute for Microbiology and Infection Medicine Tübingen, Infection Biology Unit, 72076 Tübingen, Germany; 4: The Rockefeller University, New York, NY; 5: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 6: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 7: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 8: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 9: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
    • Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.GPP3-0029-2018
  • Received 05 April 2018 Accepted 10 April 2018 Published 19 April 2019
  • Andreas Peschel, [email protected]
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  • Abstract:

    is usually regarded as a bacterial pathogen due to its ability to cause multiple types of invasive infections. Nevertheless, colonizes about 30% of the human population asymptomatically in the nares, either transiently or persistently, and can therefore be regarded a human commensal as well, although carriage increases the risk of infection. Whereas many facets of the infection processes have been studied intensively, little is known about the commensal lifestyle of . Recent studies highlight the major role of the composition of the highly variable nasal microbiota in promoting or inhibiting colonization. Competition for limited nutrients, trace elements, and epithelial attachment sites, different susceptibilities to host defense molecules and the production of antimicrobial molecules by bacterial competitors may determine whether nasal bacteria outcompete each other. This chapter summarizes our knowledge about mechanisms that are used by for efficient nasal colonization and strategies used by other nasal bacteria to interfere with its colonization. An improved understanding of naturally evolved mechanisms might enable us to develop new strategies for pathogen eradication.

  • Citation: Laux C, Peschel A, Krismer B. 2019. Colonization of the Human Nose and Interaction with Other Microbiome Members. Microbiol Spectrum 7(2):GPP3-0029-2018. doi:10.1128/microbiolspec.GPP3-0029-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.GPP3-0029-2018
2019-04-19
2020-09-26

Abstract:

is usually regarded as a bacterial pathogen due to its ability to cause multiple types of invasive infections. Nevertheless, colonizes about 30% of the human population asymptomatically in the nares, either transiently or persistently, and can therefore be regarded a human commensal as well, although carriage increases the risk of infection. Whereas many facets of the infection processes have been studied intensively, little is known about the commensal lifestyle of . Recent studies highlight the major role of the composition of the highly variable nasal microbiota in promoting or inhibiting colonization. Competition for limited nutrients, trace elements, and epithelial attachment sites, different susceptibilities to host defense molecules and the production of antimicrobial molecules by bacterial competitors may determine whether nasal bacteria outcompete each other. This chapter summarizes our knowledge about mechanisms that are used by for efficient nasal colonization and strategies used by other nasal bacteria to interfere with its colonization. An improved understanding of naturally evolved mechanisms might enable us to develop new strategies for pathogen eradication.

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Colonization of the Human Nose and Interaction with Other Microbiome Members
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Citation: Laux C, Peschel A, Krismer B. 2019. colonization of the human nose and interaction with other microbiome members. microbiolspec 7(2): doi:10.1128/microbiolspec.GPP3-0029-2018
/content/microbiolspec/10.1128/microbiolspec.GPP3-0029-2018.fig1
FIGURE 1
Attachment mechanisms of in the human nasal cavity. The anterior and posterior parts of the human nose are lined by different types of epithelial cell, which require alternative bacterial adhesion mechanisms. For the keratinized stratified squamous epithelium in the anterior nasal cavity, predominantly uses cell wall-attached surface proteins (MSCRAMMs) ( 2 , 41 ). In contrast, the primary attachment in the posterior area, composed of a pseudostratified columnar ciliated epithelium, is mediated by specific interaction of the cell-wall linked wall teichoic acid (WTA) with the scavenger receptor class F member 1 (SREC1) ( 41 , 46 ). The corneocytes (desquamated epithelial cells) in the anterior nasal cavity contain high levels of the proteins loricrin, cytokeratin 10, and involucrin ( 55 ). can express a variety of cell wall proteins, which bind to these matrix proteins. The adhesin clumping factor B (ClfB) binds to cytokeratin 10 and loricrin ( 48 , 52 ), whereas the iron-regulated surface determinant A (IsdA) can also interact with involucrin ( 55 ). In addition, the serine-aspartate repeat-containing protein D (SdrD) mediates adhesion to human squamous epithelial cells by binding to desmoglein 1 ( 56 ). Some isolates secrete an extracellular serine protease (Esp), which inhibits colonization by degradation of the surface proteins IsdA and SdrD and host receptors ( 77 , 78 ). In addition, can prevent nasal colonization of by producing the cyclic thiazolidine-containing peptide antibiotic lugdunin ( 35 ).
microbiolspec/7/2/GPP3-0029-2018-fig1_thmb.gif
microbiolspec/7/2/GPP3-0029-2018-fig1.gif
Image of FIGURE 1
FIGURE 1

Attachment mechanisms of in the human nasal cavity. The anterior and posterior parts of the human nose are lined by different types of epithelial cell, which require alternative bacterial adhesion mechanisms. For the keratinized stratified squamous epithelium in the anterior nasal cavity, predominantly uses cell wall-attached surface proteins (MSCRAMMs) ( 2 , 41 ). In contrast, the primary attachment in the posterior area, composed of a pseudostratified columnar ciliated epithelium, is mediated by specific interaction of the cell-wall linked wall teichoic acid (WTA) with the scavenger receptor class F member 1 (SREC1) ( 41 , 46 ). The corneocytes (desquamated epithelial cells) in the anterior nasal cavity contain high levels of the proteins loricrin, cytokeratin 10, and involucrin ( 55 ). can express a variety of cell wall proteins, which bind to these matrix proteins. The adhesin clumping factor B (ClfB) binds to cytokeratin 10 and loricrin ( 48 , 52 ), whereas the iron-regulated surface determinant A (IsdA) can also interact with involucrin ( 55 ). In addition, the serine-aspartate repeat-containing protein D (SdrD) mediates adhesion to human squamous epithelial cells by binding to desmoglein 1 ( 56 ). Some isolates secrete an extracellular serine protease (Esp), which inhibits colonization by degradation of the surface proteins IsdA and SdrD and host receptors ( 77 , 78 ). In addition, can prevent nasal colonization of by producing the cyclic thiazolidine-containing peptide antibiotic lugdunin ( 35 ).

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.GPP3-0029-2018
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FIGURE 2
Established interactions between nasal bacteria. and spp. can promote the colonization by (green boxes) by modulation of its adhesive capacities ( 20 , 85 ) (blue arrows), while specific clones of , , and spp. can lead to growth inhibition (orange boxes). Some isolates secrete high levels of extracellular serine protease (Esp), which inhibits nasal colonization ( 77 ) (yellow arrow). In addition, and can impede colonization by producing antimicrobial molecules ( 35 , 64 ) (black arrows). can release hydrogen peroxide, which leads to prophage activation in along with phage-mediated lysis of cells ( 80 , 81 ) (red arrow).
microbiolspec/7/2/GPP3-0029-2018-fig2_thmb.gif
microbiolspec/7/2/GPP3-0029-2018-fig2.gif
Image of FIGURE 2
FIGURE 2

Established interactions between nasal bacteria. and spp. can promote the colonization by (green boxes) by modulation of its adhesive capacities ( 20 , 85 ) (blue arrows), while specific clones of , , and spp. can lead to growth inhibition (orange boxes). Some isolates secrete high levels of extracellular serine protease (Esp), which inhibits nasal colonization ( 77 ) (yellow arrow). In addition, and can impede colonization by producing antimicrobial molecules ( 35 , 64 ) (black arrows). can release hydrogen peroxide, which leads to prophage activation in along with phage-mediated lysis of cells ( 80 , 81 ) (red arrow).

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.GPP3-0029-2018
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Tables

Colonization of the Human Nose and Interaction with Other Microbiome Members
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Citation: Laux C, Peschel A, Krismer B. 2019. colonization of the human nose and interaction with other microbiome members. microbiolspec 7(2): doi:10.1128/microbiolspec.GPP3-0029-2018
/content/microbiolspec/10.1128/microbiolspec.GPP3-0029-2018.T1
TABLE 1
Community state types of the human nose
Generic image for table
TABLE 1

Community state types of the human nose

Source: microbiolspec April 2019 vol. 7 no. 2 doi:10.1128/microbiolspec.GPP3-0029-2018

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