Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut

ABSTRACT Interactions between the gut microbiome and immunoglobulin A (IgA) in the gut during infancy are important for future health. IgM and IgG are also present in the gut; however, their interactions with the microbiome in the developing infant remain to be characterized. Using stool samples sam...

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Autores principales: Anders Janzon, Julia K. Goodrich, Omry Koren, Jillian L. Waters, Ruth E. Ley
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Lenguaje:EN
Publicado: American Society for Microbiology 2019
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Acceso en línea:https://doaj.org/article/1a9f3623fea34a5695f65950d40dd9f1
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spelling oai:doaj.org-article:1a9f3623fea34a5695f65950d40dd9f12021-12-02T19:46:17ZInteractions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut10.1128/mSystems.00612-192379-5077https://doaj.org/article/1a9f3623fea34a5695f65950d40dd9f12019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00612-19https://doaj.org/toc/2379-5077ABSTRACT Interactions between the gut microbiome and immunoglobulin A (IgA) in the gut during infancy are important for future health. IgM and IgG are also present in the gut; however, their interactions with the microbiome in the developing infant remain to be characterized. Using stool samples sampled 15 times in infancy from 32 healthy subjects at 4 locations in 3 countries, we characterized patterns of microbiome development in relation to fecal levels of IgA, IgG, and IgM. For 8 infants from a single location, we used fluorescence-activated cell sorting of microbial cells from stool by Ig-coating status over 18 months. We used 16S rRNA gene profiling on full and sorted microbiomes to assess patterns of antibody coating in relation to age and other factors. All antibodies decreased in concentration with age but were augmented by breastmilk feeding regardless of infant age. Levels of IgA correlated with relative abundances of operational taxonomic units (OTUs) belonging to the Bifidobacteria and Enterobacteriaceae, which dominated the early microbiome, and IgG levels correlated with Haemophilus. The diversity of Ig-coated microbiota was influenced by breastfeeding and age. IgA and IgM coated the same microbiota, which reflected the overall diversity of the microbiome, while IgG targeted a different subset. Blautia generally evaded antibody coating, while members of the Bifidobacteria and Enterobacteriaceae were high in IgA/M. IgA/M displayed similar dynamics, generally coating the microbiome proportionally, and were influenced by breastfeeding status. IgG only coated a small fraction of the commensal microbiota and differed from the proportion targeted by IgA and IgM. IMPORTANCE Antibodies are secreted into the gut and attach to roughly half of the trillions of bacterial cells present. When babies are born, the breastmilk supplies these antibodies until the baby’s own immune system takes over this task after a few weeks. The vast majority of these antibodies are IgA, but two other types, IgG and IgM, are also present in the gut. Here, we ask if these three different antibody types target different types of bacteria in the infant gut as the infant develops from birth to 18 months old and how patterns of antibody coating of bacteria change with age. In this study of healthy infant samples over time, we found that IgA and IgM coat the same bacteria, which are generally representative of the diversity present, with a few exceptions that were more or less antibody coated than expected. IgG coated a separate suite of bacteria. These results provide a better understanding of how these antibodies interact with the developing infant gut microbiome.Anders JanzonJulia K. GoodrichOmry KorenJillian L. WatersRuth E. LeyAmerican Society for Microbiologyarticlegut microbiomeinfantdiabetesimmunoglobulinsIgAIgMMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic gut microbiome
infant
diabetes
immunoglobulins
IgA
IgM
Microbiology
QR1-502
spellingShingle gut microbiome
infant
diabetes
immunoglobulins
IgA
IgM
Microbiology
QR1-502
Anders Janzon
Julia K. Goodrich
Omry Koren
Jillian L. Waters
Ruth E. Ley
Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
description ABSTRACT Interactions between the gut microbiome and immunoglobulin A (IgA) in the gut during infancy are important for future health. IgM and IgG are also present in the gut; however, their interactions with the microbiome in the developing infant remain to be characterized. Using stool samples sampled 15 times in infancy from 32 healthy subjects at 4 locations in 3 countries, we characterized patterns of microbiome development in relation to fecal levels of IgA, IgG, and IgM. For 8 infants from a single location, we used fluorescence-activated cell sorting of microbial cells from stool by Ig-coating status over 18 months. We used 16S rRNA gene profiling on full and sorted microbiomes to assess patterns of antibody coating in relation to age and other factors. All antibodies decreased in concentration with age but were augmented by breastmilk feeding regardless of infant age. Levels of IgA correlated with relative abundances of operational taxonomic units (OTUs) belonging to the Bifidobacteria and Enterobacteriaceae, which dominated the early microbiome, and IgG levels correlated with Haemophilus. The diversity of Ig-coated microbiota was influenced by breastfeeding and age. IgA and IgM coated the same microbiota, which reflected the overall diversity of the microbiome, while IgG targeted a different subset. Blautia generally evaded antibody coating, while members of the Bifidobacteria and Enterobacteriaceae were high in IgA/M. IgA/M displayed similar dynamics, generally coating the microbiome proportionally, and were influenced by breastfeeding status. IgG only coated a small fraction of the commensal microbiota and differed from the proportion targeted by IgA and IgM. IMPORTANCE Antibodies are secreted into the gut and attach to roughly half of the trillions of bacterial cells present. When babies are born, the breastmilk supplies these antibodies until the baby’s own immune system takes over this task after a few weeks. The vast majority of these antibodies are IgA, but two other types, IgG and IgM, are also present in the gut. Here, we ask if these three different antibody types target different types of bacteria in the infant gut as the infant develops from birth to 18 months old and how patterns of antibody coating of bacteria change with age. In this study of healthy infant samples over time, we found that IgA and IgM coat the same bacteria, which are generally representative of the diversity present, with a few exceptions that were more or less antibody coated than expected. IgG coated a separate suite of bacteria. These results provide a better understanding of how these antibodies interact with the developing infant gut microbiome.
format article
author Anders Janzon
Julia K. Goodrich
Omry Koren
Jillian L. Waters
Ruth E. Ley
author_facet Anders Janzon
Julia K. Goodrich
Omry Koren
Jillian L. Waters
Ruth E. Ley
author_sort Anders Janzon
title Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
title_short Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
title_full Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
title_fullStr Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
title_full_unstemmed Interactions between the Gut Microbiome and Mucosal Immunoglobulins A, M, and G in the Developing Infant Gut
title_sort interactions between the gut microbiome and mucosal immunoglobulins a, m, and g in the developing infant gut
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/1a9f3623fea34a5695f65950d40dd9f1
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