Dataset Information

Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA.

ABSTRACT: 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.

SUBMITTER: Fouhse JM

PROVIDER: S-EPMC5428161 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA.

Fouhse Janelle M JM Smiegielski Luke L Tuplin Melanie M Guan Le Luo LL Willing Benjamin P BP

Frontiers in microbiology 20170512

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 o ...[more]

PMID: 28553275

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Project description:Host microbiomes are important regulators of organismal fitness, physiology, and ecology. Microbiomes promote the fitness of their host in part by buffering the host from the full effects of fluctuating conditions and stressors imposed by the external environment. Whether the host conversely serves as a buffer for their associated microbes against variation in the external environment is less clear. Here, we test if bacteria inhabiting the microbiome of a host are locally adapted to nutrient levels in their surrounding external environment. We used a system in which the host, the phytoplankter Microcystis aeruginosa, has strains that are locally adapted to low-nutrient versus high-nutrient lakes. Assessing 40 metagenome-assembled genomes belonging to four taxonomic groups of heterotrophic bacteria residing within the host microbiome, we found consistent phylogenetic divergence between strains originating from low-nutrient versus high-nutrient environments. Bacteria found in association with low-nutrient host genotypes obtained from low-nutrient lakes demonstrated genome streamlining, including reduced genome size and fewer sigma factors. These bacterial genomes have features that would facilitate survival in low-nutrient lakes, including (i) greater number of alkaline phosphatase genes that are essential for phosphorus acquisition and (ii) positive selection within genes involved in phosphorus metabolism. Overall, our results demonstrate that despite living in close association with host organisms, bacteria residing within microbiomes may have evolved and undergone environmental selection to stressors external to their host, demonstrating similar patterns of adaptation to those that might be expected to develop among free-living bacteria. IMPORTANCE Understanding how natural selection has historically shaped the traits of microbial populations comprising host microbiomes would help predict how the functions of these microbes may continue to evolve over space and time. Numerous host-associated microbes have been found to adapt to their host, sometimes becoming obligate symbionts, whereas free-living microbes are best known to adapt to their surrounding environment. Our study assessed the selective pressures of both the host environment and the surrounding external environment in shaping the functional potential of host-associated bacteria. Despite residing within the resource-rich microbiome of their hosts, we demonstrate that host-associated heterotrophic bacteria show evidence of trait selection that matches the nutrient availability of their broader surrounding environment. These findings illustrate the complex mix of selective pressures that likely shape the present-day function of bacteria found inhabiting host microbiomes. Our study lends insight into the shifts in function that may occur as environments fluctuate over time.

Dataset Information

Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA.

Publications

Host Immune Selection of Rumen Bacteria through Salivary Secretory IgA.

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