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Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA

The rumen microbiome is integral to efficient production in cattle and shows strong host specificity, yet little is known about what host factors shape rumen microbial composition. Secretory immunoglobulin A (SIgA) is produced in large amounts in the saliva, can coat both commensal and pathogenic mi...

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Autores principales: Fouhse, Janelle M., Smiegielski, Luke, Tuplin, Melanie, Guan, Le Luo, Willing, Benjamin P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5428161/
https://www.ncbi.nlm.nih.gov/pubmed/28553275
http://dx.doi.org/10.3389/fmicb.2017.00848
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author Fouhse, Janelle M.
Smiegielski, Luke
Tuplin, Melanie
Guan, Le Luo
Willing, Benjamin P.
author_facet Fouhse, Janelle M.
Smiegielski, Luke
Tuplin, Melanie
Guan, Le Luo
Willing, Benjamin P.
author_sort Fouhse, Janelle M.
collection PubMed
description The rumen microbiome is integral to efficient production in cattle and shows strong host specificity, yet little is known about what host factors shape rumen microbial composition. Secretory immunoglobulin A (SIgA) is produced in large amounts in the saliva, can coat both commensal and pathogenic microbes within the gut, and presents a plausible mechanism of host specificity. However, the role salivary SIgA plays in commensal bacteria selection in ruminants remains elusive. The main objectives of this study were to develop an immuno-affinity benchtop method to isolate SIgA-tagged microbiota and to determine if salivary SIgA preferentially binds selected bacteria. We hypothesized that SIgA-tagged bacteria would differ from total bacteria, thus supporting a potential host-derived mechanism in commensal bacterial selection. Whole rumen (n = 9) and oral secretion samples (n = 10) were incubated with magnetic beads conjugated with anti-secretory IgA antibodies to enrich SIgA-tagged microbiota. Microbial DNA from the oral secretion, whole rumen, SIgA-tagged oral secretion, and SIgA-tagged rumen was isolated for amplicon sequencing of V1–V3 region of 16S rDNA genes. Whole rumen and oral secretion had distinctive (P < 0.05) bacterial compositions indicated by the non-parametric multidimensional scaling plot using Euclidean distance metrics. The SIgA-tagged microbiota from rumen and oral secretion had similar abundance of Bacteroidetes, Actinobacteria, Fibrobacter, candidate phyla TM7, and Tenericutes and are clustered tightly. Composition of SIgA-tagged oral secretion microbiota was more similar to whole rumen microbiota than whole oral secretion due to enrichment of rumen bacteria (Lachnospiraceae) and depletion of oral taxa (Streptococcus, Rothia, Neisseriaceae, and Lactobacillales). In conclusion, SIgA-tagged oral secretion microbiota had an increased resemblance to whole rumen microbiota, suggesting salivary SIgA-coating may be one host-derived mechanism impacting commensal colonization. Further studies, to explore the variations in antibody affinity between different animals as a driver of microbial composition are warranted.
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spelling pubmed-54281612017-05-26 Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA Fouhse, Janelle M. Smiegielski, Luke Tuplin, Melanie Guan, Le Luo Willing, Benjamin P. Front Microbiol Microbiology The rumen microbiome is integral to efficient production in cattle and shows strong host specificity, yet little is known about what host factors shape rumen microbial composition. Secretory immunoglobulin A (SIgA) is produced in large amounts in the saliva, can coat both commensal and pathogenic microbes within the gut, and presents a plausible mechanism of host specificity. However, the role salivary SIgA plays in commensal bacteria selection in ruminants remains elusive. The main objectives of this study were to develop an immuno-affinity benchtop method to isolate SIgA-tagged microbiota and to determine if salivary SIgA preferentially binds selected bacteria. We hypothesized that SIgA-tagged bacteria would differ from total bacteria, thus supporting a potential host-derived mechanism in commensal bacterial selection. Whole rumen (n = 9) and oral secretion samples (n = 10) were incubated with magnetic beads conjugated with anti-secretory IgA antibodies to enrich SIgA-tagged microbiota. Microbial DNA from the oral secretion, whole rumen, SIgA-tagged oral secretion, and SIgA-tagged rumen was isolated for amplicon sequencing of V1–V3 region of 16S rDNA genes. Whole rumen and oral secretion had distinctive (P < 0.05) bacterial compositions indicated by the non-parametric multidimensional scaling plot using Euclidean distance metrics. The SIgA-tagged microbiota from rumen and oral secretion had similar abundance of Bacteroidetes, Actinobacteria, Fibrobacter, candidate phyla TM7, and Tenericutes and are clustered tightly. Composition of SIgA-tagged oral secretion microbiota was more similar to whole rumen microbiota than whole oral secretion due to enrichment of rumen bacteria (Lachnospiraceae) and depletion of oral taxa (Streptococcus, Rothia, Neisseriaceae, and Lactobacillales). In conclusion, SIgA-tagged oral secretion microbiota had an increased resemblance to whole rumen microbiota, suggesting salivary SIgA-coating may be one host-derived mechanism impacting commensal colonization. Further studies, to explore the variations in antibody affinity between different animals as a driver of microbial composition are warranted. Frontiers Media S.A. 2017-05-12 /pmc/articles/PMC5428161/ /pubmed/28553275 http://dx.doi.org/10.3389/fmicb.2017.00848 Text en Copyright © 2017 Fouhse, Smiegielski, Tuplin, Guan and Willing. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Fouhse, Janelle M.
Smiegielski, Luke
Tuplin, Melanie
Guan, Le Luo
Willing, Benjamin P.
Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title_full Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title_fullStr Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title_full_unstemmed Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title_short Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA
title_sort host immune selection of rumen bacteria through salivary secretory iga
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5428161/
https://www.ncbi.nlm.nih.gov/pubmed/28553275
http://dx.doi.org/10.3389/fmicb.2017.00848
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