A hotspot of Toxoplasma gondii Africa 1 lineage in Benin: How new genotypes from West Africa contribute to understand the parasite genetic diversity worldwide.

A hotspot of Toxoplasma gondii Africa 1 lineage in Benin: How new genotypes from West Africa contribute to understand the parasite genetic diversity worldwide.
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刚地弓形虫非洲1系在贝宁的研究热点:来自西非的新基因型如何有助于了解全球寄生虫的遗传多样性

DOI:
10.1371/journal.pntd.0008980
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发表时间:
2021-03
影响因子:
3.8
通讯作者:
Mercier A
Mercier A
中科院分区:
医学2区
文献类型:
--
作者:
Hamidović A;Etougbétché JR;Tonouhewa ABN;Galal L;Dobigny G;Houémènou G;Da Zoclanclounon H;Amagbégnon R;Laleye A;Fievet N;Piry S;Berthier K;Pena HFJ;Dardé ML;Mercier A

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通过国际贸易,欧洲、非洲和南美有着悠久的交流历史,潜在的病原体交流。我们使用世界范围内的弓形虫寄生虫来检验贝宁的病原体遗传多样性受到历史影响的假设,贝宁是一个有着悠久海上贸易历史的西非国家。在非洲,弓形虫的空间结构仍然没有得到统一的研究,到目前为止,很少有文章报道动物群和临床形式的弓形虫菌株遗传多样性,即使在非洲散居国外也是如此。用改良凝集试验(MAT)对两个沿海地区(科托努和欧达)和两个内陆地区(帕拉库和纳提丁古)的758只家畜(主要是家禽)的血清进行了弓形虫抗体检测。采集了69只血清阳性动物的心脏和大脑,用于小鼠生物试验中的寄生虫分离。共获得45株菌株,15个微卫星基因分型可描述39个基因型别,其中以非洲本土血统非洲1为主(36/39)。其余基因分型为非洲4个变异型TUB2(1/39)和2个相同的III型分离株(克隆)(2/39)。内陆采样点和沿海采样点之间的基因分布没有差异。特别是,与塞内加尔的情况相反,在沿海城市的家禽中没有分离出II型(主要存在于欧洲)。这一结果似乎驳斥了欧洲在贝宁的海上贸易可能发挥的作用,尽管贝宁是奴隶贸易时期最重要的枢纽之一。然而,巴西存在非洲1型基因,贝宁的基因分析表明,三角贸易是基因菌株从非洲向南美洲洲际传播的一条途径。这支持了人类和动物受到潜在输入毒力菌株污染的可能性。弓形虫寄生虫是一种分布于世界各地的病原体,能够感染所有温血动物。感染的临床表现有重要差异,与寄生虫的遗传图谱有直接关系。在一些地区,其遗传多样性的地理结构表明,人类活动在某些谱系的引入或分类中起着至关重要的作用。贝宁是一个有着广泛跨洲交流历史的西非国家。我们在贝宁对弓形虫的遗传研究显示出令人惊讶的同质性和原生多样性,这与其他西非和中非国家之前的研究形成了鲜明对比。在贝宁,欧洲弓形虫血统的缺失可能是因为家鼠(Mus Musculus)的极端稀有,这是一种宿主物种,以前被描述为对具有老鼠毒力的非洲菌株高度敏感。贝宁可能是非洲1血统的起源地区,我们的结果表明,几内亚湾海岸可能是奴隶贸易期间向南美洲,特别是巴西的血统的起点。作为一个整体,本研究对弓形虫最近的进化史及其对人类和动物健康的影响提供了进一步的见解。
Through international trades, Europe, Africa and South America share a long history of exchanges, potentially of pathogens. We used the worldwide parasite Toxoplasma gondii to test the hypothesis of a historical influence on pathogen genetic diversity in Benin, a West African country with a longstanding sea trade history. In Africa, T. gondii spatial structure is still non-uniformly studied and very few articles have reported strain genetic diversity in fauna and clinical forms of human toxoplasmosis so far, even in African diaspora. Sera from 758 domestic animals (mainly poultry) in two coastal areas (Cotonou and Ouidah) and two inland areas (Parakou and Natitingou) were tested for T. gondii antibodies using a Modified Agglutination Test (MAT). The hearts and brains of 69 seropositive animals were collected for parasite isolation in a mouse bioassay. Forty-five strains were obtained and 39 genotypes could be described via 15-microsatellite genotyping, with a predominance of the autochthonous African lineage Africa 1 (36/39). The remaining genotypes were Africa 4 variant TUB2 (1/39) and two identical isolates (clone) of Type III (2/39). No difference in terms of genotype distribution between inland and coastal sampling sites was found. In particular, contrarily to what has been described in Senegal, no type II (mostly present in Europe) was isolated in poultry from coastal cities. This result seems to refute a possible role of European maritime trade in Benin despite it was one of the most important hubs during the slave trade period. However, the presence of the Africa 1 genotype in Brazil, predominant in Benin, and genetic analyses suggest that the triangular trade was a route for the intercontinental dissemination of genetic strains from Africa to South America. This supports the possibility of contamination in humans and animals with potentially imported virulent strains. The parasite Toxoplasma gondii is a worldwide-distributed pathogen, able to infect all warm-blooded animals. There are important differences in the clinical expression of the infection in direct relation with the parasite genetic profile. In some regions, the geographical structuration of its genetic diversity points towards a crucial role of human activities in some lineages introduction or sorting. Benin is a West African country with a history of extensive transcontinental exchanges. Our genetic study of Toxoplasma in Benin shows a surprisingly homogeneous and autochthonous diversity, which contrasts with previous studies from other West and Central African countries. In Benin, the absence of European Toxoplasma lineages may be explained by the extreme rarity of the house mouse (Mus musculus), a host species that was previously described as highly susceptible to the mouse-virulent African strains. Might Benin be the origin region for the Africa 1 lineage, our results suggest that Guinean Gulf coasts may be a starting point of this lineage towards South America, especially Brazil, during the slave trade. As a whole, the present study provides further insights into the recent evolutionary history of Toxoplasma gondii and its consequences on human and animal health.
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