Wolbachia and mosquitoes: Exploring transmission modes and coevolutionary dynamics in Shandong Province, China

IF 3.8 2区 医学 Q1 Medicine PLoS Neglected Tropical Diseases Pub Date : 2024-09-12 DOI:10.1371/journal.pntd.0011944
Chuanhui Zang, Xuejun Wang, Yan Liu, Haifang Wang, Qintong Sun, Peng Cheng, Ye Zhang, Maoqing Gong, Hongmei Liu
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Abstract

Vector-borne diseases leave a large footprint on global health. Notable culprits include West Nile virus (WNV), St. Louis encephalitis virus (SLEV), and Japanese encephalitis virus (JEV), all transmitted by Culex mosquitoes. Chemical insecticides have been widely used to reduce the spread of mosquito-borne diseases. Still, mosquitoes are becoming more and more resistant to most chemical insecticides which cause particular harm to the ecology. Wolbachia belongs to the family Ehrlichiaceae in the order Rickettsiales and is a matrilineally inherited endosymbiont present in 60% of insects in nature. Wolbachia is capable of inducing a wide range of reproductive abnormalities in its hosts, such as cytoplasmic incompatibility, and can alter mosquito resistance to pathogen infection. Wolbachia has been proposed as a biological alternative to chemical vector control, and specific research progress and effectiveness have been achieved. Despite the importance of Wolbachia, this strategy has not been tested in Culex pipiens pallens, the most prevalent mosquito species in Shandong Province, China. Little is known about how the mass release of Wolbachia-infected mosquitoes may impact the genetic structure of Culex pipiens pallens, and how the symbiotic bacterium Wolbachia interacts with mitochondria during host mosquito transmission. Based on the population genetic structure of Culex pipiens pallens in Shandong Province, this study investigated the infection rate and infection type of Wolbachia in Shandong Province and jointly analysed the evolutionary relationship between the host mosquito and the symbiotic bacterium Wolbachia. Our study showed that Wolbachia naturally infected by Culex pipiens pallens in Shandong Province was less homologous to Wolbachia infected by Aedes albopictus released from mosquito factory in Guangzhou. Our results also show that Culex pipiens pallens is undergoing demographic expansion in Shandong Province. The overall Wolbachia infection rate of Culex pipiens pallens was 92.8%, and a total of 15 WSP haplotypes were detected. We found that the genetic diversity of Wolbachia was low in Culex pipiens pallens from Shandong Province, and the mosquitoes were infected only with type B Wolbachia. Visualizing the relationship between Culex pipiens pallens and Wolbachia using a tanglegram revealed patterns of widespread associations. A specific coevolutionary relationship exists between the host mosquito and Wolbachia. Knowledge of this mosquito–Wolbachia relationship will provide essential scientific information required for Wolbachia-based vector control approaches in Shandong Province and will lead to a better understanding of the diversity and evolution of Wolbachia for its utility as a biocontrol agent.
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沃尔巴克氏体与蚊子:探索中国山东省的传播模式和共同进化动态
病媒传染的疾病给全球健康留下了巨大的影响。主要的罪魁祸首包括西尼罗河病毒(WNV)、圣路易斯脑炎病毒(SLEV)和日本脑炎病毒(JEV),它们都是由库蚊传播的。化学杀虫剂已被广泛用于减少蚊媒疾病的传播。然而,蚊子对大多数化学杀虫剂的抗药性越来越强,这对生态造成了特别大的危害。沃尔巴克氏菌属于立克次体目埃希氏菌科,是一种母系遗传的内共生体,存在于自然界 60% 的昆虫体内。沃尔巴克氏体能诱导宿主出现多种生殖异常,如细胞质不相容,并能改变蚊子对病原体感染的抵抗力。沃尔巴克氏菌已被提出作为化学病媒控制的生物替代品,并取得了具体的研究进展和成效。尽管沃尔巴克氏体非常重要,但这一策略尚未在中国山东省最普遍的蚊子物种库蚊(Culex pipiens pallens)中进行过测试。人们对大量释放沃尔巴克氏体感染蚊子会如何影响淡色库蚊的遗传结构,以及在宿主蚊子传播过程中沃尔巴克氏体共生细菌如何与线粒体相互作用知之甚少。本研究以山东省萍蚊种群遗传结构为基础,调查了沃尔巴克氏菌在山东省的感染率和感染类型,并共同分析了宿主蚊与共生细菌沃尔巴克氏菌之间的进化关系。我们的研究表明,山东省库蚊自然感染的沃尔巴克氏体与广州蚊虫工厂释放的白纹伊蚊感染的沃尔巴克氏体同源性较低。我们的研究结果还表明,山东省的白纹伊蚊正在进行种群扩张。白纹库蚊的总体沃尔巴克氏体感染率为 92.8%,共检测到 15 种 WSP 单倍型。我们发现,山东省苍白库蚊的沃尔巴克氏体遗传多样性较低,蚊子只感染了 B 型沃尔巴克氏体。利用切线图观察淡色库蚊与沃尔巴克氏体之间的关系,发现了广泛的关联模式。宿主蚊子与沃尔巴克氏体之间存在着一种特殊的共同进化关系。了解这种蚊子与沃尔巴克氏体的关系将为山东省基于沃尔巴克氏体的病媒控制方法提供必要的科学信息,并将有助于更好地了解沃尔巴克氏体的多样性和进化,从而使其成为一种生物控制剂。
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来源期刊
PLoS Neglected Tropical Diseases
PLoS Neglected Tropical Diseases Medicine-Infectious Diseases
CiteScore
7.40
自引率
10.50%
发文量
723
审稿时长
2-3 weeks
期刊介绍: PLOS Neglected Tropical Diseases publishes research devoted to the pathology, epidemiology, prevention, treatment and control of the neglected tropical diseases (NTDs), as well as relevant public policy. The NTDs are defined as a group of poverty-promoting chronic infectious diseases, which primarily occur in rural areas and poor urban areas of low-income and middle-income countries. Their impact on child health and development, pregnancy, and worker productivity, as well as their stigmatizing features limit economic stability. All aspects of these diseases are considered, including: Pathogenesis Clinical features Pharmacology and treatment Diagnosis Epidemiology Vector biology Vaccinology and prevention Demographic, ecological and social determinants Public health and policy aspects (including cost-effectiveness analyses).
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