Engineered symbiotic bacteria interfering Nosema redox system inhibit microsporidia parasitism in honeybees

Haoyu Lang, Hao Wang, Haoqing Wang, Zhaopeng Zhong, Xianbing Xie, Wenhao Zhang, Jun Guo, Liang Meng, Xiaosong Hu, Xue Zhang and Hao Zheng ()
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Haoyu Lang: China Agricultural University
Hao Wang: China Agricultural University
Haoqing Wang: China Agricultural University
Zhaopeng Zhong: China Agricultural University
Xianbing Xie: Nanchang University
Wenhao Zhang: Kunming University of Science and Technology
Jun Guo: Kunming University of Science and Technology
Liang Meng: BGI-Qingdao, BGI-Shenzhen
Xiaosong Hu: China Agricultural University
Xue Zhang: China Agricultural University
Hao Zheng: China Agricultural University

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Nosema ceranae is an intracellular parasite invading the midgut of honeybees, which causes serious nosemosis implicated in honeybee colony losses worldwide. The core gut microbiota is involved in protecting against parasitism, and the genetically engineering of the native gut symbionts provides a novel and efficient way to fight pathogens. Here, using laboratory-generated bees mono-associated with gut members, we find that Snodgrassella alvi inhibit microsporidia proliferation, potentially via the stimulation of host oxidant-mediated immune response. Accordingly, N. ceranae employs the thioredoxin and glutathione systems to defend against oxidative stress and maintain a balanced redox equilibrium, which is essential for the infection process. We knock down the gene expression using nanoparticle-mediated RNA interference, which targets the γ-glutamyl-cysteine synthetase and thioredoxin reductase genes of microsporidia. It significantly reduces the spore load, confirming the importance of the antioxidant mechanism for the intracellular invasion of the N. ceranae parasite. Finally, we genetically modify the symbiotic S. alvi to deliver dsRNA corresponding to the genes involved in the redox system of the microsporidia. The engineered S. alvi induces RNA interference and represses parasite gene expression, thereby inhibits the parasitism significantly. Specifically, N. ceranae is most suppressed by the recombinant strain corresponding to the glutathione synthetase or by a mixture of bacteria expressing variable dsRNA. Our findings extend our previous understanding of the protection of gut symbionts against N. ceranae and provide a symbiont-mediated RNAi system for inhibiting microsporidia infection in honeybees.

Date: 2023
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DOI: 10.1038/s41467-023-38498-2

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