<i>Dicer</i> regulates <i>Nosema ceranae</i> proliferation in honeybees

Huang, Qiang; Li, W.; Chen, Y.; Retschnig-Tanner, G.; Yañez, Orlando; Neumann, Peter; Evans, Jay D.

doi:10.1111/imb.12534

Cited by 17 publications

(6 citation statements)

References 62 publications

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“…Due to a lack of well-established tools for genetic manipulation, functional study on ATP/ADP carriers in microsporidian is extremely limited, especially in Nosema species. Given the severe influence of N. ceranae on the worldwide beekeeping industry, it’s necessary and significant to carry out experimental work on the function of identified members of ATP/ADP carrier family in N. ceranae adopting molecular approach such as RNAi, which has been proved to be efficient in knockdown of several N. ceranae genes ( Paldi et al, 2010 ; Li et al, 2016 ; Rodriguez-Garcia et al, 2018 ; Huang et al, 2019 ). We previously used purified spores of N. bombycis to infect Bombyx mori BmN cells, followed by transfection with a non-transposon vector pIZT/V5-His vector and the exogenous gfp gene was successfully inserted into the N. bombycis genome ( Guo et al, 2016 ).…”

Section: Resultsmentioning

confidence: 99%

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Genome and Evolutionary Analysis of Nosema ceranae: A Microsporidian Parasite of Honey Bees

Huang

et al. 2021

Front. Microbiol.

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Microsporidia comprise a phylum of single cell, intracellular parasites and represent the earliest diverging branch in the fungal kingdom. The microsporidian parasite Nosema ceranae primarily infects honey bee gut epithelial cells, leading to impaired memory, suppressed host immune responses and colony collapse under certain circumstances. As the genome of N. ceranae is challenging to assembly due to very high genetic diversity and repetitive region, the genome was re-sequenced using long reads. We present a robust 8.8 Mbp genome assembly of 2,280 protein coding genes, including a high number of genes involved in transporting nutrients and energy, as well as drug resistance when compared with sister species Nosema apis. We also describe the loss of the critical protein Dicer in approximately half of the microsporidian species, giving new insights into the availability of RNA interference pathway in this group. Our results provided new insights into the pathogenesis of N. ceranae and a blueprint for treatment strategies that target this parasite without harming honey bees. The unique infectious apparatus polar filament and transportation pathway members can help to identify treatments to control this parasite.

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Section: Resultsmentioning

confidence: 99%

“…Previously, we quantified N. ceranae gene expression profiles at various proliferation stages with RNA-seq ( Huang et al, 2019 ). To improve the gene annotation, we re-mapped those reads to the current N. ceranae genome assembly and retrieved the aligned reads using Hisat2 with default parameters ( Kim et al, 2013 ).…”

Section: Methodsmentioning

confidence: 99%

Genome and Evolutionary Analysis of Nosema ceranae: A Microsporidian Parasite of Honey Bees

Huang

et al. 2021

Front. Microbiol.

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“…However, an N. ceranae -infected bee model has been constructed and applied to functional studies on microsporidian proliferation-associated genes. Huang et al (2019) previously injected siRNA- Dicer into A. mellifera workers infected with N. ceranae , and observed that genes encoding two virulence factors, ABC transporter and hexokinase, were down-regulated while the spore load was significantly reduced, which indicated that Dicer gene silencing could suppress the N. ceranae proliferation. Recently, Kim et al (2020) conducted dsRNA-based RNAi of mitosome-related genes in N. ceranae , and the results showed that microsporidian proliferation was inhibited while the host survival rate was increased.…”

Section: Discussionmentioning

confidence: 99%

In-depth investigation of microRNA-mediated cross-kingdom regulation between Asian honey bee and microsporidian

Fan

Zhang

et al. 2022

Front. Microbiol.

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Asian honey bee Apis cerana is the original host for Nosema ceranae, a unicellular fungal parasite that causes bee nosemosis throughout the world. Currently, interaction between A. cerana and N. ceranae is largely unknown. Our group previously prepared A. c. cerana workers’ midguts at 7 days post inoculation (dpi) and 10 dpi with N. ceranae spores as well as corresponding un-inoculated workers’ midguts, followed by cDNA library construction and a combination of RNAs-seq and small RNA-seq. Meanwhile, we previously prepared clean spores of N. ceranae, which were then subjected to cDNA library construction and deep sequencing. Here, based on the gained high-quality transcriptome datasets, N. ceranae differentially expressed mRNAs (DEmiRNAs) targeted by host DEmiRNAs, and A. c. cerana DEmRNAs targeted by microsporidian DEmiRNAs were deeply investigated, with a focus on targets involved in N. ceranae glycolysis/glyconeogenesis as well as virulence factors, and A. c. cerana energy metabolism and immune response. In A. c. cerana worker’s midguts at 7 (10) dpi (days post inoculation), eight (seven) up-regulated and six (two) down-regulated miRNAs were observed to target 97 (44) down-regulated and 60 (15) up-regulated N. ceranae mRNAs, respectively. Additionally, two up-regulated miRNAs (miR-60-y and miR-676-y) in host midgut at 7 dpi could target genes engaged in N. ceranae spore wall protein and glycolysis/gluconeogenesis, indicating potential host miRNA-mediated regulation of microsporidian virulence factor and energy metabolism. Meanwhile, in N. ceranae at 7 (10) dpi, 121 (110) up-regulated and 112 (104) down-regulated miRNAs were found to, respectively, target 343 (247) down-regulated and 138 (110) down-regulated mRNAs in A. c. cerana workers’ midguts. These targets in host were relevant to several crucial cellular and humoral immune pathways, such as phagasome, endocytosis, lysosomes, regulation of autophagy, and Jak–STAT signaling pathway, indicative of the involvement of N. ceranae DEmiRNAs in regulating these cellular and humoral immune pathways. In addition, N. ceranae miR-21-x was up-regulated at 7 dpi and had a target relative to oxidative phosphorylation, suggesting that miR-21-x may be used as a weapon to modulate this pivotal energy metabolism pathway. Furthermore, potential targeting relationships between two pairs of host DEmiRNAs-microsporidian DEmRNAs and two pairs of microsporidian DEmiRNAs-host DEmRNAs were validated using RT-qPCR. Our findings not only lay a foundation for exploring the molecular mechanism underlying cross-kingdom regulation between A. c. cerana workers and N. ceranae, but also offer valuable insights into Asian honey bee-microsporidian interaction.

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“…In addition, since the entire genome sequence of N. ceranae has been revealed, the possibility of RNAi application to N. ceranae has been further increased. However, to date, RNAi studies related to the control of N. ceranae have not been conducted except for studies using ADP/ATP transporters (Paldi et al, 2010) and Dicer (Huang et al, 2019). As N. ceranae is known to possess Dicer, an important element of the RNA‐induced silencing complex, unlike other Nosema , its expression was suppressed by RNAi technology, and its spore production capacity was decreased.…”

Section: Introductionmentioning

confidence: 99%

Increased survival of the honey bee Apis mellifera infected with the microsporidian Nosema ceranae by effective gene silencing

Kim

Gwak

et al. 2020

Arch Insect Biochem Physiol

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This study examined the control of nosemosis caused by Nosema ceranae, one of the hard-to-control diseases of honey bees, using RNA interference (RNAi) technology. Double-stranded RNA (dsRNA) for RNAi application targeted the mitosome-related genes of N. ceranae. Among the various mitosome-related genes, NCER_100882, NCER_101456, NCER_100157, and NCER_100686 exhibited relatively low homologies with the orthologs of Apis mellifera. Four gene-specific dsRNAs were prepared against the target genes and applied to the infected A. mellifera to analyze Nosema proliferation and honey bee survival. Two dsRNAs specifics to NCER_101456 and NCER_100157 showed high inhibitory effects on spore production by exhibiting only 62% and 67%, respectively, compared with the control. In addition, these dsRNA treatments significantly rescued the honey bees from the fatal nosemosis. It was confirmed that the inhibition of Nosema spore proliferation and the increase in the survival rate of honey bees were resulted from a decrease in the expression level of each target gene by dsRNA treatment. However, dsRNA mixture treatment was no more effective than single treatments in the rescue from the nosemosis. It is expected that the four newly identified mitosome-related target genes in this study can be

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Dicer regulates Nosema ceranae proliferation in honeybees

Cited by 17 publications

References 62 publications

Genome and Evolutionary Analysis of Nosema ceranae: A Microsporidian Parasite of Honey Bees

Genome and Evolutionary Analysis of Nosema ceranae: A Microsporidian Parasite of Honey Bees

In-depth investigation of microRNA-mediated cross-kingdom regulation between Asian honey bee and microsporidian

Increased survival of the honey bee Apis mellifera infected with the microsporidian Nosema ceranae by effective gene silencing

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