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Field-Realistic Tylosin Exposure Impacts Honey Bee Microbiota and Pathogen Susceptibility, Which Is Ameliorated by Native Gut Probiotics.

ABSTRACT: Antibiotics have been applied to honey bee (Apis mellifera) hives for decades to treat Paenibacillus larvae, which causes American foulbrood disease and kills honey bee larvae. One of the few antibiotics approved in apiculture is tylosin tartrate. This study examined how a realistic hive treatment regimen of tylosin affected the gut microbiota of bees and susceptibility to a bacterial pathogen. Tylosin treatment reduced bacterial species richness and phylogenetic diversity and reduced the absolute abundances and strain diversity of the beneficial core gut bacteria Snodgrassella alvi and Bifidobacterium spp. Bees from hives treated with tylosin died more quickly after being fed a bacterial pathogen (Serratia marcescens) in the laboratory. We then tested whether a probiotic cocktail of core bee gut species could bolster pathogen resistance. Probiotic exposure increased survival of bees from both control and tylosin-treated hives. Finally, we measured tylosin tolerance of core bee gut bacteria by plating cultured isolates on media with different tylosin concentrations. We observed highly variable responses, including large differences among strains of both S. alvi and Gilliamella spp. Thus, probiotic treatments using cultured bee gut bacteria may ameliorate harmful perturbations of the gut microbiota caused by antibiotics or other factors. IMPORTANCE The antibiotic tylosin tartrate is used to treat honey bee hives to control Paenibacillus larvae, the bacterium that causes American foulbrood. We found that bees from tylosin-treated hives had gut microbiomes with depleted overall diversity as well as reduced absolute abundances and strain diversity of the beneficial bee gut bacteria Snodgrassella alvi and Bifidobacterium spp. Furthermore, bees from treated hives suffered higher mortality when challenged with an opportunistic pathogen. Bees receiving a probiotic treatment, consisting of a cocktail of cultured isolates of native bee gut bacteria, had increased survival following pathogen challenge. Thus, probiotic treatment with native gut bacteria may ameliorate negative effects of antibiotic exposure.

SUBMITTER: Powell JE

PROVIDER: S-EPMC8552731 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:American foulbrood disease of honey bees is caused by the bacterium Paenibacillus larvae. Infection occurs per os in larvae and systemic infection requires a breaching of the host peritrophic matrix and midgut epithelium. Genetic variation exists for both bacterial virulence and host resistance, and a general immunity is achieved by larvae as they age, the basis of which has not been identified. To quickly identify a pool of candidate genes responsive to P. larvae infection, we sequenced transcripts from larvae inoculated with P. larvae at 12 hours post-emergence and incubated for 72 hours, and compared expression levels to a control cohort. We identified 75 genes with significantly higher expression and six genes with significantly lower expression. In addition to several antimicrobial peptides, two genes encoding peritrophic-matrix domains were also up-regulated. Extracellular matrix proteins, proteases/protease inhibitors, and members of the Osiris gene family were prevalent among differentially regulated genes. However, analysis of Drosophila homologs of differentially expressed genes revealed spatial and temporal patterns consistent with developmental asynchrony as a likely confounder of our results. We therefore used qPCR to measure the consistency of gene expression changes for a subset of differentially expressed genes. A replicate experiment sampled at both 48 and 72 hours post infection allowed further discrimination of genes likely to be involved in host response. The consistently responsive genes in our test set included a hymenopteran-specific protein tyrosine kinase, a hymenopteran specific serine endopeptidase, a cytochrome P450 (CYP9Q1), and a homolog of trynity, a zona pellucida domain protein. Of the known honey bee antimicrobial peptides, apidaecin was responsive at both time-points studied whereas hymenoptaecin was more consistent in its level of change between biological replicates and had the greatest increase in expression by RNA-seq analysis.

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Field-Realistic Tylosin Exposure Impacts Honey Bee Microbiota and Pathogen Susceptibility, Which Is Ameliorated by Native Gut Probiotics.

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