Honeybees play an important role in pollinating native plants and agricultural crops and produce valuable hive products. Within the last decade, honeybee colonies have been reported to be in decline, due to both biotic and abiotic stress factors including pathogens and pesticides. This study evaluated the impact of different isolates of Nosema spp.[Nosema apis spores (NA), Nosema ceranae from Apis mellifera from France (NF), N. ceranae from Apis cerana from Thailand (NC1), and N. ceranae from A. mellifera from Thailand (NC2)] on the different gut sections of newly emerged adult A. mellifera bees. With an attempt to decipher the early impact of Nosema spp. on the first barrier against Nosema infection, we used off-gel bottom-up proteomics on the different anatomical sections of the gut four days post inoculation. A total of 2185 identified proteins in the esophagus, 2095 in the crop, 1571 in the midgut, 2552 in the ileum, and 3173 in the rectum were obtained. Using label-free quantification, we observed that the response of the host varies according to the Nosema spp. (N. apis versus N. ceranae) and the geographical origin of Nosema. The proteins in the midgut of A. mellifera, orally inoculated with spores of N. ceranae isolated from France, were the most altered, when compared with controls, exhibiting 50 proteins down-regulated and 16 up-regulated. We thereby established the first massspectrometry-based proteomics of different anatomical sections of the gut tissue of Nosema-infected A. mellifera four days post inoculation, following infection by different isolates of Nosema spp. that provoked differential host responses. We reported an alteration of proteins involved in the metabolic pathways and specifically eight proteins of the oxidative phosphorylation pathway. More importantly, we propose that the collagen IV NC1 domain-containing protein may represent an early prognostic marker of the impact of Nosema spores on the A. mellifera health status. Data are available via ProteomeXchange with the identifier PXD021848.

Nosema ceranae infects midgut epithelial cells of the Apis species and has jumped from its original host A. cerana to A. mellifera worldwide, raising questions about the response of the new host. We compared the responses of these two species to N. ceranae isolates from A. cerana, A. mellifera from Thailand and A. mellifera from France. Proteomics and transcriptomics results were combined to better understand the impact on the immunity of the two species. This is the first combination of omics analyses to evaluate the impact of N. ceranae spores from different origins and provides new insights into the differential immune responses in honeybees inoculated with N. ceranae from original A. cerana. No difference in the antimicrobial peptides (AMPs) was observed in A. mellifera, whereas these peptides were altered in A. cerana compared to controls. Inoculation of A. mellifera or A. cerana with N. ceranae upregulated AMP genes and cellular-mediated immune genes but did not significantly alter apoptosis-related gene expression. A. cerana showed a stronger immune response than A. mellifera after inoculation with different N. ceranae isolates. N. ceranae from A. cerana had a strong negative impact on the health of A. mellifera and A. cerana compared to other Nosema isolates.

Widespread parasites, along with emerging threats, globalization, and climate change, have greatly affected honey bees’ health, leading to colony losses worldwide. In this study, we investigated the detection of biotic stressors (i.e., viruses, microsporidian, bacteria, and fungi) in Apis cerana by surveying the colonies across different regions of Thailand (Chiang Mai in the north, Nong Khai and Khon Kaen in the northeast, and Chumphon and Surat Thani in the south, in addition to the Samui and Pha-ngan islands). In this study, we detected ABPV, BQCV, LSV, and Nosema ceranae in A. cerana samples through RT-PCR. ABPV was only detected from the samples of Chiang Mai, whereas we found BQCV only in those from Chumphon. LSV was detected only in the samples from the Samui and Pha-ngan islands, where historically no managed bees are known. Nosema ceranae was found in all of the regions except for Nong Khai and Khon Kaen in northeastern Thailand. Paenibacillus larvae and Ascosphaera apis were not detected in any of the A. cerana samples in this survey. The phylogenetic tree analysis of the pathogens provided insights into the pathogens’ movements and their distribution ranges across different landscapes, indicating the flow of pathogens among the honey bees. Here, we describe the presence of emerging pathogens in the Asian honey bee as a valuable step in our understanding of these pathogens in terms of the decline in eastern honey bee populations.

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