Zombie Ants: Towards a Mechanistic Understanding of the Precise Control of Animal Behavior by a Microbial Parasite

自然界中最复杂的共生例子之一是微生物对动物行为的精确操纵。蛇纹草是一种感染僵尸蚂蚁的真菌。蚂蚁工蚁被数以千计的真菌细胞感染，导致工蚁离开蚁群，并通过他们的下颌附着在蚂蚁群落尾部上方的植物上而死亡。在那里，真菌利用死蚂蚁的身体产生孢子，感染其他蚂蚁。鉴于没有大脑的有机体控制有大脑的有机体的行为，这种操作既复杂又壮观。在这个项目中，研究小组将使用一种综合的方法来研究真菌如何将蚂蚁从其群体中的生产性成员转变为“穿着蚂蚁衣服的真菌？”该项目将使用基因表达、新陈代谢和组织结构的测量来研究在感染的3周期间，真菌如何有效地控制蚂蚁。这项工作将对寄生虫的本质提供许多一般性的见解，并可能具有更广泛的社会意义，因为这些真菌被认为是具有医学意义的小分子的重要来源。这项工作与NSF提高科学素养的更广泛使命有关，因为僵尸蚂蚁系统已被证明是传播自然系统的优雅和美丽的非常有用的工具。微生物如何控制动物的中枢神经系统？动物与微生物密切相关，微生物跨越了从互惠共生到寄生的范围。在某些情况下，动物的微生物寄生虫已经进化到通过增强寄生虫传播的方式来控制动物的行为。僵尸蚂蚁就是一个突出的例子。在这个系统中，一种真菌寄生虫(单边冬虫夏草)已经进化出对其感染的蚂蚁进行精确水平的行为控制。被单边原虫感染的工蚁会在一天中的准确时间从它们的蚁群迁出到森林树叶上高度特定的位置，在那里它们在死亡之前咬食植被。这种改变的行为为最终从蚂蚁身体长出的真菌茎中释放孢子提供了一个平台。这个惊人的系统涉及一个生命王国(真菌)中的有机体，它控制另一个生命王国(动物界)中的有机体的行为。没有大脑的有机体如何控制有大脑的有机体的行为？研究人员将通过时间序列感染研究来测量寄生虫及其宿主的化学变化，以解决这一问题。通过使用三种不同但互补的工具(序列区块面部扫描电子显微镜、代谢组学和转录组学)来检查这些随时间变化的情况，研究人员希望了解这些行为变化的基础。

One of the most complex examples of symbiosis in nature is the precise manipulation of animal behavior by a microbe. Ophiocordyceps is a fungus that infects zombie ants. Infection of ant workers by thousands of these fungal cells causes the workers to leave the colony and die attached by their mandibles to plants that overhang the trails of ant colonies. There the fungus uses the dead ant bodies to produce spores that infect other ants. The manipulation is complex and spectacular given the fact that an organism without a brain controls the behavior of one with a brain. In this project the research team will use an integrative approach to ask how fungi change ants from being productive members of their colony to "fungi in ant's clothing?". The project will use measurement of gene expression, metabolism and tissue structure to ask how, during the 3 week period of infection, the fungi effectively take control of the ant. This work will provide many general insights into the nature of parasitism and may have broader societal relevance because these fungi are known to be important sources of small molecules with medical relevance. The work is relevant to the broader mission of NSF to increase scientific literacy as the zombie ant system has been shown to be a very useful tool for communicating the elegance and beauty of natural systems. How can a microbe control the central nervous system of an animal? Animals are intimately associated with microbes that span the symbiotic spectrum from mutualism to parasitism. In some cases, microbial parasites of animals have evolved to control animal behavior in ways that enhance parasite transmission. The zombie ants represent one prominent example. In this system a fungal parasite (Ophiocordyceps unilateralis) has evolved a precise level of behavioral control over the ants it infects. Worker ants infected by O. unilateralis move out from their colonies at precise times of day to highly specific locations on leaves in forests, where they bite into vegetation before dying. This altered behavior provides a platform for the eventual release of spores from a long fungal stalk that grows from the cadaver of the ant. This striking system involves an organism in one kingdom of life (Fungi) that controls the behavior of an organism in another (Animalia). How does an organism without a brain control the behavior of one with a brain? The investigators will address this using time series infectionstudies to measure chemical changes in both the parasite and its host. By using three different but complementary tools (serial block face scanning electron microscopy, metabolomics and transcriptomics) to examine these changes across time, the investigators hope to understand the basis of these behavioral changes.