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- Title
Toll receptor ligand Spätzle 4 responses to the highly pathogenic Enterococcus faecalis from Varroa mites in honeybees.
- Authors
Zhang, Wenhao; Sun, Cheng; Lang, Haoyu; Wang, Jieni; Li, Xinyu; Guo, Jun; Zhang, Zijing; Zheng, Hao
- Abstract
Honeybees play a major role in crop pollination, which supports the agricultural economy and international food supply. The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Recently, it shows that V. destructor may also transmit bacteria through the feeding wound, yet it remains unclear whether the invading bacteria can exhibit pathogenicity to the honeybees. Here, we incidentally isolate Enterococcus faecalis, one of the most abundant bacteria in Varroa mites, from dead bees during our routine generation of microbiota-free bees in the lab. In vivo tests show that E. faecalis is only pathogenic in Apis mellifera but not in Apis cerana. The expression of antimicrobial peptide genes is elevated following infection in A. cerana. The gene-based molecular evolution analysis identifies positive selection of genes encoding Späetzle 4 (Spz4) in A. cerana, a signaling protein in the Toll pathway. The amino acid sites under positive selection are related to structural changes in Spz4 protein, suggesting improvement of immunity in A. cerana. The knock-down of Spz4 in A. cerana significantly reduces the survival rates under E. faecalis challenge and the expression of antimicrobial peptide genes. Our results indicate that bacteria associated with Varroa mites are pathogenic to adult bees, and the positively selected gene Spz4 in A. cerana is crucial in response to this mite-related pathogen. Author summary: Multiple factors contribute to the decline of honeybee colonies, including climate change, the spread of pests and pathogens, and pesticide use. Varroa mites and the viruses they carry pose a severe threat to honeybee health. However, it is still unknown whether the bacteria from Varroa mites are also responsible for the death of worker bees. Indeed, these bacterial pathogens were underestimated since infected adult workers tend to abandon their hives. Here, we characterized the virulence of E. faecalis strains isolated from the gut of A. mellifera originating from mite-infected hives. Our results indicate that E. faecalis, an opportunistic pathogen of many plants and animals, poses a significant threat to A. mellifera but not A. cerana. Infection of E. faecalis stimulates the Toll signaling pathway and the downstream expression of AMPs in A. cerana. Specifically, Spz4 protein has been selected in a relatively longer evolutionary process in A. cerana, and is the key mechanism of A. cerana to defend against E. faecalis. Our results suggest that eastern and western honeybees may possess different innate immune responses against the V. destructor-associated bacterial pathogens.
- Subjects
VARROA destructor; ENTEROCOCCUS faecalis; VARROA; BEE colonies; ANTIMICROBIAL peptides; APIS cerana; ACARICIDES
- Publication
PLoS Pathogens, 2023, Vol 19, Issue 12, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1011897