Secretory IgA impacts the microbiota density in the human nose.

IgA-seq Mucosal immunology Nasal antibodies Nasal microbiota Secretory IgA

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
21 10 2023
Historique:
received: 24 01 2023
accepted: 24 09 2023
medline: 2 11 2023
pubmed: 22 10 2023
entrez: 21 10 2023
Statut: epublish

Résumé

Respiratory mucosal host defense relies on the production of secretory IgA (sIgA) antibodies, but we currently lack a fundamental understanding of how sIgA is induced by contact with microbes and how such immune responses may vary between humans. Defense of the nasal mucosal barrier through sIgA is critical to protect from infection and to maintain homeostasis of the microbiome, which influences respiratory disorders and hosts opportunistic pathogens. We applied IgA-seq analysis to nasal microbiota samples from male and female healthy volunteers, to identify which bacterial genera and species are targeted by sIgA on the level of the individual host. Furthermore, we used nasal sIgA from the same individuals in sIgA deposition experiments to validate the IgA-seq outcomes. We observed that the amount of sIgA secreted into the nasal mucosa by the host varied substantially and was negatively correlated with the bacterial density, suggesting that nasal sIgA limits the overall bacterial capacity to colonize. The interaction between mucosal sIgA antibodies and the nasal microbiota was highly individual with no obvious differences between potentially invasive and non-invasive bacterial species. Importantly, we could show that for the clinically relevant opportunistic pathogen and frequent nasal resident Staphylococcus aureus, sIgA reactivity was in part the result of epitope-independent interaction of sIgA with the antibody-binding protein SpA through binding of sIgA Fab regions. This study thereby offers a first comprehensive insight into the targeting of the nasal microbiota by sIgA antibodies. It thereby helps to better understand the shaping and homeostasis of the nasal microbiome by the host and may guide the development of effective mucosal vaccines against bacterial pathogens. Video Abstract.

Sections du résumé

BACKGROUND
Respiratory mucosal host defense relies on the production of secretory IgA (sIgA) antibodies, but we currently lack a fundamental understanding of how sIgA is induced by contact with microbes and how such immune responses may vary between humans. Defense of the nasal mucosal barrier through sIgA is critical to protect from infection and to maintain homeostasis of the microbiome, which influences respiratory disorders and hosts opportunistic pathogens.
METHODS
We applied IgA-seq analysis to nasal microbiota samples from male and female healthy volunteers, to identify which bacterial genera and species are targeted by sIgA on the level of the individual host. Furthermore, we used nasal sIgA from the same individuals in sIgA deposition experiments to validate the IgA-seq outcomes.
CONCLUSIONS
We observed that the amount of sIgA secreted into the nasal mucosa by the host varied substantially and was negatively correlated with the bacterial density, suggesting that nasal sIgA limits the overall bacterial capacity to colonize. The interaction between mucosal sIgA antibodies and the nasal microbiota was highly individual with no obvious differences between potentially invasive and non-invasive bacterial species. Importantly, we could show that for the clinically relevant opportunistic pathogen and frequent nasal resident Staphylococcus aureus, sIgA reactivity was in part the result of epitope-independent interaction of sIgA with the antibody-binding protein SpA through binding of sIgA Fab regions. This study thereby offers a first comprehensive insight into the targeting of the nasal microbiota by sIgA antibodies. It thereby helps to better understand the shaping and homeostasis of the nasal microbiome by the host and may guide the development of effective mucosal vaccines against bacterial pathogens. Video Abstract.

Identifiants

pubmed: 37865781
doi: 10.1186/s40168-023-01675-y
pii: 10.1186/s40168-023-01675-y
pmc: PMC10589987
doi:

Substances chimiques

Immunoglobulin A, Secretory 0

Types de publication

Video-Audio Media Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

233

Informations de copyright

© 2023. BioMed Central Ltd., part of Springer Nature.

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Auteurs

Rob van Dalen (R)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany. r.vandalen@amsterdamumc.nl.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany. r.vandalen@amsterdamumc.nl.
Present Address: Department of Medical Microbiology and Infection Prevention, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands. r.vandalen@amsterdamumc.nl.

Ahmed M A Elsherbini (AMA)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany.

Mareike Harms (M)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany.

Svenja Alber (S)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany.

Regine Stemmler (R)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany.

Andreas Peschel (A)

Interfaculty Institute of Microbiology and Infection Medicine, Department of Infection Biology, University of Tübingen, Tübingen, Germany. andreas.peschel@uni-tuebingen.de.
Cluster of Excellence EXC2124 Controlling Microbes to Fight Infections, University of Tübingen, Tübingen, Germany. andreas.peschel@uni-tuebingen.de.
German Center for Infection Research (DZIF), Partner Site Tübingen, Tübingen, Germany. andreas.peschel@uni-tuebingen.de.

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