Dataset Information

Immune system stimulation by the native gut microbiota of honey bees.

ABSTRACT: Gut microbial communities can greatly affect host health by modulating the host's immune system. For many important insects, however, the relationship between the gut microbiota and immune function remains poorly understood. Here, we test whether the gut microbial symbionts of the honey bee can induce expression of antimicrobial peptides (AMPs), a crucial component of insect innate immunity. We find that bees up-regulate gene expression of the AMPs apidaecin and hymenoptaecin in gut tissue when the microbiota is present. Using targeted proteomics, we detected apidaecin in both the gut lumen and the haemolymph; higher apidaecin concentrations were found in bees harbouring the normal gut microbiota than in bees lacking gut microbiota. In in vitro assays, cultured strains of the microbiota showed variable susceptibility to honey bee AMPs, although many seem to possess elevated resistance compared to Escherichia coli. In some trials, colonization by normal gut symbionts resulted in improved survivorship following injection with E. coli. Our results show that the native, non-pathogenic gut flora induces immune responses in the bee host. Such responses might be a host mechanism to regulate the microbiota, and could potentially benefit host health by priming the immune system against future pathogenic infections.

SUBMITTER: Kwong WK

PROVIDER: S-EPMC5367273 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Immune system stimulation by the native gut microbiota of honey bees.

Kwong Waldan K WK Mancenido Amanda L AL Moran Nancy A NA

Royal Society open science 20170208 2

Gut microbial communities can greatly affect host health by modulating the host's immune system. For many important insects, however, the relationship between the gut microbiota and immune function remains poorly understood. Here, we test whether the gut microbial symbionts of the honey bee can induce expression of antimicrobial peptides (AMPs), a crucial component of insect innate immunity. We find that bees up-regulate gene expression of the AMPs apidaecin and hymenoptaecin in gut tissue when ...[more]

PMID: 28386455

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Project description:The highly social honey bee has dense populations but a significantly reduced repertoire of immune genes relative to solitary species, suggesting a greater reliance on social immunity. Here we investigate immune gene expression and gut microbial succession in queens during colony introduction. Recently mated queens were placed into an active colony or a storage hive for multiple queens: a queen-bank. Feeding intensity, social context, and metabolic demand differ greatly between the two environments. After 3 weeks, we examined gene expression associated with oxidative stress and immunity and performed high-throughput sequencing of the queen gut microbiome across four alimentary tract niches. Microbiota and gene expression in the queen hindgut differed by time, queen breeder source, and metabolic environment. In the ileum, upregulation of most immune and oxidative stress genes occurred regardless of treatment conditions, suggesting postmating effects on gut gene expression. Counterintuitively, queens exposed to the more social colony environment contained significantly less bacterial diversity indicative of social immune factors shaping the queens microbiome. Queen bank queens resembled much older queens with decreased Alpha 2.1, greater abundance of Lactobacillus firm5 and Bifidobacterium in the hindgut, and significantly larger ileum microbiotas, dominated by blooms of Snodgrassella alvi. Combined with earlier findings, we conclude that the queen gut microbiota experiences an extended period of microbial succession associated with queen breeder source, postmating development, and colony assimilation. IMPORTANCE In modern agriculture, honey bee queen failure is repeatedly cited as one of the major reasons for yearly colony loss. Here we discovered that the honey bee queen gut microbiota alters according to early social environment and is strongly tied to the identity of the queen breeder. Like human examples, this early life variation appears to set the trajectory for ecological succession associated with social assimilation and queen productivity. The high metabolic demand of natural colony assimilation is associated with less bacterial diversity, a smaller hindgut microbiome, and a downregulation of genes that control pathogens and oxidative stress. Queens placed in less social environments with low metabolic demand (queen banks) developed a gut microbiota that resembled much older queens that produce fewer eggs. The queens key reproductive role in the colony may rely in part on a gut microbiome shaped by social immunity and the early queen rearing environment.

Dataset Information

Immune system stimulation by the native gut microbiota of honey bees.

Publications

Immune system stimulation by the native gut microbiota of honey bees.

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