A natural symbiotic bacterium drives mosquito refractoriness to Plasmodium infection via secretion of an antimalarial lipase

Gao, Han; Bai, Liang; Jiang, Yongmao; Huang, Wei; Wang, Lili; Li, Shengguo; Zhu, Guoding; Wang, Duoquan; Huang, Zhenghui; Xishang, Li; Cao, Jun; Jiang, Lubing; Jacobs-­Lorena, Marcelo; Zhan, Shuai; Wang, Sibao

doi:10.1038/s41564-021-00899-8

Cited by 55 publications

(44 citation statements)

References 66 publications

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“…Similarly, efficient spread of recombinant bacteria into mosquito populations has been demonstrated in a laboratory setting (, 14 this work), indicating a promising path toward the field implementation of the most efficient [transgenesis + paratransgenesis] strategy. The recent finding that a naturally occurring and non-modified Serratia can spread through mosquito populations while strongly suppressing Plasmodium development, 30 significantly increases the feasibility of moving paratransgenesis into the field, as it bypasses concerns relating to the release of genetically modified organisms in nature. In the field, we envision the use of attractive sugar feeding stations for Serratia introduction into mosquito populations.…”

Section: Discussionmentioning

confidence: 99%

Combining transgenesis with paratransgenesis to fight malaria

Huang

Vega-Rodríguez

Kizito

et al. 2022

Preprint

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Malaria is among the deadliest infectious diseases. Two promising strategies to curb parasite transmission are transgenesis, consisting of genetically engineering mosquitoes to express anti-malarial effector molecules and paratransgenesis, consisting of introducing into the mosquito, commensal bacteria engineered to express anti-malarial effector molecules. Although both approaches restrict parasite development in the mosquito, it is not known how their effectiveness compares. Here we provide an in-depth assessment of transgenesis and paratransgenesis and evaluate the combination of the two approaches. We engineered mosquitoes and Serratia, a commensal bacterium capable to spread through mosquito populations, to produce and secrete two effectors – scorpine and the MP2 peptide. Whereas the mosquito- and bacteria-based approaches reduced parasite load, a substantially stronger reduction was achieved when they were combined. Most importantly, transmission from infected to naïve mice was maximally inhibited by the combination of the two approaches. This combination promises to become a powerful approach to combat malaria.

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Section: Discussionmentioning

confidence: 99%

Combining transgenesis with paratransgenesis to fight malaria

Huang

Vega-Rodríguez

Kizito

et al. 2022

Preprint

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“…proved that the bacteria can be introduced into adult mosquitoes by artificial feeding but also established a model to study the effect of introduced bacteria on the normal physiological activities and life cycle of Ae. albopictus [46]. To study the mechanism of S. oryzae induced resistance, female susceptible mosquitoes were treated with sterilized and increasing concentrations of bacteria, and then changes in the metabolic detoxification enzyme activity were estimated.…”

Section: Plos Neglected Tropical Diseasesmentioning

confidence: 99%

A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide

Wang

Peng

et al. 2022

PLoS Negl Trop Dis

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Background The increasing insecticide resistance of Aedes albopictus puts many countries in Asia and Africa, including China, at great risk of a mosquito-borne virus epidemic. To date, a growing number of researches have focused on the relationship between intestinal symbiotic bacteria and their hosts’ resistance to insecticides. This provides a novel aspect to the study of resistant mechanisms. Methods/Findings This study reveals significant composition and dynamic changes in the intestinal symbiotic bacteria of Ae. albopictus between the resistant and susceptible strains based on full-length sequencing technology. The relative abundance of Serratia oryzae was significantly higher in the resistance strain than in the susceptible strains; also, the relative abundance of S. oryzae was significantly higher in deltamethrin-induced Ae. albopictus than in their counterpart. These suggested that S. oryzae may be involved in the development of insecticide resistance in Ae. albopictus. To explore the insecticide resistance mechanism, adult mosquitoes were fed with GFP-tagged S. oryzae, which resulted in stable bacterial enrichment in the mosquito gut without affecting the normal physiology, longevity, oviposition, and hatching rates of the host. The resistance measurements were made based on bioassays as per the WHO guidelines. The results showed that the survival rate of S. oryzae-enriched Ae. albopictus was significantly higher than the untreated mosquitoes, indicating the enhanced resistance of S. oryzae-enriched Ae. albopictus. Also, the activities of three metabolic detoxification enzymes in S. oryzae-enriched mosquitoes were increased to varying degrees. Meanwhile, the activity of extracellular enzymes released by S. oryzae was measured, but only carboxylesterase activity was detected. HPLC and UHPLC were respectively used to measure deltamethrin residue concentration and metabolite qualitative analysis, showing that the deltamethrin degradation efficiency of S. oryzae was positively correlated with time and bacterial amount. Deltamethrin was broken down into 1-Oleoyl-2-hydroxy-sn-glycero-3-PE and 2’,2’-Dibromo-2’-deoxyguanosine. Transcriptome analysis revealed that 9 cytochrome P450s, 8 GSTs and 7 CarEs genes were significantly upregulated. Conclusions S. oryzae can be accumulated into adult Ae. albopictus by artificial feeding, which enhances deltamethrin resistance by inducing the metabolic detoxification genes and autocrine metabolic enzymes. S. oryzae is vertically transmitted in Ae. albopictus population. Importantly, S. oryzae can degrade deltamethrin in vitro, and use deltamethrin as the sole carbon source for their growths. Therefore, in the future, S. oryzae may also be commercially used to break down the residual insecticides in the farmland and lakes to protect the environment.

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“…As for paratransgenesis, the news is excellent. Recently, a Serratia has been isolated in China that not only can spread through mosquito populations, but also naturally (without genetic engineering) strongly inhibit Plasmodium development in mosquitoes (Gao et al 2021). Experiments are under way to verify the effectiveness of these bacteria to spread and inhibit parasite transmission under field conditions.…”

Section: Prospectsmentioning

confidence: 99%

New weapons to fight malaria transmission: A historical view

Huang

Cha

Lorena

2022

Entomological Research

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The stagnation of our fight against malaria in recent years, mainly due to the development of mosquito insecticide resistance, argues for the urgent development of new weapons. The dramatic evolution of molecular tools in the last few decades led to a better understanding of parasite-mosquito interactions and coalesced in the development of novel tools namely, mosquito transgenesis and paratransgenesis.Here we provide a historical view of the development of these new tools and point to some remaining challenges for their implementation in the field.

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A natural symbiotic bacterium drives mosquito refractoriness to Plasmodium infection via secretion of an antimalarial lipase

Cited by 55 publications

References 66 publications

Combining transgenesis with paratransgenesis to fight malaria

Combining transgenesis with paratransgenesis to fight malaria

A symbiotic gut bacterium enhances Aedes albopictus resistance to insecticide

New weapons to fight malaria transmission: A historical view

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