Harnessing the power of phylogenomics to disentangle the directionality and signatures of interkingdom host jumping in the parasitic fungal genus <i>Tolypocladium</i>

Host specialization is common among parasitic fungi; however, there are examples when transitions in host specificity between disparately related hosts have occurred. Here, we examine the interkingdom host jump from insect pathogenicity and mycoparasitism in <i>Tolypocladium</i>. Previous phylogenetic inferences made using only a few genes and with poor support reconstructed an ancestral character state of insect pathogenesis, a transition to mycoparasitism, and reversions to insect pathogenesis. To further explore the directionality and genes underlying the transitions in host, we sequenced two additional species of <i>Tolypocladium</i> (<i>T. capitatum</i> and <i>T. paradoxum</i>) and used phylogenomics to compare two insect pathogens and two mycoparasites. Our whole-genome-scale analysis suggests that the diversification of <i>Tolypocladium</i> species happened relatively quickly and that the truffle parasites form a monophyletic, derived lineage within the genus that is the result of a single ecological transition or host jump from insects to fungi. A significant amount of gene tree/species tree discordance occurs within the data set, and we infer this to be the product of both an historical hybridization event and incomplete lineage sorting that was likely because of the rapid diversification of the clade. Furthermore, comparative genomic analyses revealed a set of genes that are exclusive to the mycoparasitic species. These potentially mycoparasitic gene clusters were characterized by a reduced proportion of secreted proteins when compared with entomopathogen-enriched genes and involved the reshaping of the fungal secretome in the ecological context of mycoparasitism.

寄生真菌中宿主专化现象十分普遍；不过亦存在类群亲缘关系甚远的宿主间发生宿主特异性转换的案例。本研究聚焦弯颈霉属（Tolypocladium）中从昆虫致病到菌寄生的界间宿主跃迁现象。此前仅基于少量基因且支持度欠佳的系统发育研究，曾重建出该类群的祖先性状为昆虫致病，随后出现向菌寄生的演化转换，之后又发生了向昆虫致病的逆转。为进一步探究宿主转换的方向性及其背后的遗传基础，我们新增测序了弯颈霉属的两个物种：头状弯颈霉（T. capitatum）与奇异弯颈霉（T. paradoxum），并采用系统基因组学方法，对2株昆虫病原真菌与2株菌寄生真菌开展比较分析。全基因组规模的分析结果显示，弯颈霉属物种的分化进程相对迅速；而块菌寄生类群构成该属内一个单系衍生支系，其起源于一次从昆虫宿主到真菌宿主的单一生态转换或宿主跃迁。本数据集存在显著的基因树与物种树不一致现象，我们推断这是历史杂交事件与不完全谱系分选共同作用的结果，而该现象大概率源于该演化支的快速分化。此外，比较基因组分析还鉴定出一套仅存在于菌寄生物种中的专属基因家族。相较于富集昆虫病原相关的基因，这类潜在菌寄生基因簇的分泌蛋白占比更低，且在菌寄生的生态背景下，真菌分泌组发生了适应性重塑。