Mitochondrial Genome Analyses Suggest Multiple Trichuris Species in Humans, Baboons, and Pigs from Different Geographical Regions

BackgroundThe whipworms Trichuris trichiura and Trichuris suis are two parasitic nematodes of humans and pigs, respectively. Although whipworms in human and non-human primates historically have been referred to as T. trichiura, recent reports suggest that several Trichuris spp. are found in primates.Methods and FindingsWe sequenced and annotated complete mitochondrial genomes of Trichuris recovered from a human in Uganda, an olive baboon in the US, a hamadryas baboon in Denmark, and two pigs from Denmark and Uganda. Comparative analyses using other published mitochondrial genomes of Trichuris recovered from a human and a porcine host in China and from a françois’ leaf-monkey (China) were performed, including phylogenetic analyses and pairwise genetic and amino acid distances. Genetic and protein distances between human Trichuris in Uganda and China were high (~19% and 15%, respectively) suggesting that they represented different species. Trichuris from the olive baboon in US was genetically related to human Trichuris in China, while the other from the hamadryas baboon in Denmark was nearly identical to human Trichuris from Uganda. Baboon-derived Trichuris was genetically distinct from Trichuris from françois’ leaf monkey, suggesting multiple whipworm species circulating among non-human primates. The genetic and protein distances between pig Trichuris from Denmark and other regions were roughly 9% and 6%, respectively, while Chinese and Ugandan whipworms were more closely related.Conclusion and SignificanceOur results indicate that Trichuris species infecting humans and pigs are phylogenetically distinct across geographical regions, which might have important implications for the implementation of suitable and effective control strategies in different regions. Moreover, we provide support for the hypothesis that Trichuris infecting primates represents a complex of cryptic species with some species being able to infect both humans and non-human primates.

【研究背景】鞭虫（whipworm）类群中的毛首鞭形线虫（Trichuris trichiura）与猪鞭虫（Trichuris suis），分别为寄生于人类与猪的寄生线虫。尽管长期以来，人类及非人灵长类体内的鞭虫均被归为毛首鞭形线虫（T. trichiura），但近期研究表明，灵长类体内可检出多种毛首线虫属（Trichuris）物种。【研究方法与结果】本研究对分别从乌干达一名感染者、美国一只橄榄狒狒、丹麦一只阿拉伯狒狒，以及丹麦和乌干达的两头猪体内分离得到的毛首线虫（Trichuris）完成了完整线粒体基因组（mitochondrial genome）的测序与注释。此外，本研究还利用已发表的其他毛首线虫线粒体基因组数据开展比较分析，这些基因组分别分离自中国的人类宿主与猪宿主，以及中国的白头叶猴（François' leaf-monkey）。分析内容包括系统发育分析、两两遗传距离与氨基酸距离计算。结果显示，乌干达与中国的人体感染毛首线虫之间的遗传距离与蛋白质距离分别高达约19%与15%，提示二者为不同物种。美国橄榄狒狒体内的毛首线虫与中国人体感染毛首线虫存在遗传亲缘关系，而丹麦阿拉伯狒狒体内的毛首线虫则与乌干达人体感染毛首线虫几乎完全一致。狒狒来源的毛首线虫与白头叶猴来源的毛首线虫存在遗传差异，表明非人灵长类体内存在多种循环传播的鞭虫物种。丹麦猪源毛首线虫与其他地区猪源毛首线虫的遗传距离与蛋白质距离分别约为9%与6%，而中国与乌干达的猪源鞭虫则亲缘关系较近。【结论与意义】本研究结果表明，感染人类与猪的毛首线虫物种存在地理驱动的系统发育分化，这一发现对不同地区制定适配且高效的鞭虫防控策略具有重要指导意义。此外，本研究为相关假说提供了支撑：感染灵长类的毛首线虫是一个隐存物种复合类群，其中部分物种可同时感染人类与非人灵长类。