Department for Evolutionary Biology, Max Planck Institute for Developmental Biology, Max Planck Ring 9, 72076, Tübingen, Germany.
ISME J. 2020 Jun;14(6):1494-1507. doi: 10.1038/s41396-020-0626-2. Epub 2020 Mar 9.
Although the microbiota is known to affect host development, metabolism, and immunity, its impact on host behavior is only beginning to be understood. In order to better characterize behavior modulation by host-associated microorganisms, we investigated how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. This nematode is a predator that feeds on the larvae of other nematodes, including Caenorhabditis elegans. By growing P. pacificus on different bacteria and testing their ability to kill C. elegans, we reveal large differences in killing efficiencies, with a Novosphingobium species showing the strongest enhancement. This enhanced killing was not accompanied by an increase in feeding, which is a phenomenon known as surplus killing, whereby predators kill more prey than necessary for sustenance. Our RNA-seq data demonstrate widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated screening of bacterial mutants with altered transcriptional responses. We identified bacterial production of vitamin B as an important cause of such enhanced predatory behavior. Although vitamin B is an essential cofactor for detoxification and metabolite biosynthesis, shown previously to accelerate development in C. elegans, supplementation with this enzyme cofactor amplified surplus killing in P. pacificus, whereas mutants in vitamin B-dependent pathways reduced surplus killing. By demonstrating that production of vitamin B by host-associated microbiota can affect complex host behaviors, we reveal new connections between animal diet, microbiota, and nervous system.
尽管人们已经知道微生物组会影响宿主的发育、代谢和免疫，但它对宿主行为的影响才刚刚开始被理解。为了更好地描述宿主相关微生物对行为的调节作用，我们研究了细菌如何调节秀丽隐杆线虫这一模式生物的复杂行为。这种线虫是一种捕食者，以其他线虫的幼虫为食，包括秀丽隐杆线虫。我们通过在不同的细菌上培养秀丽隐杆线虫，并测试它们杀死秀丽隐杆线虫的能力，揭示了它们在杀伤效率上的巨大差异，其中一种新鞘氨醇单胞菌表现出最强的增强作用。这种增强的杀伤并不伴随着摄食的增加，这是一种被称为剩余杀伤的现象，即捕食者杀死的猎物数量超过维持自身生存所需的数量。我们的 RNA-seq 数据表明，在暴露于新鞘氨醇单胞菌后，秀丽隐杆线虫的新陈代谢发生了广泛的重排，这为筛选转录响应发生改变的细菌突变体提供了便利。我们发现细菌产生维生素 B 是这种增强捕食行为的一个重要原因。虽然维生素 B 是解毒和代谢物生物合成的必需辅因子，先前的研究表明它可以加速秀丽隐杆线虫的发育，但在秀丽隐杆线虫中补充这种酶辅因子会放大剩余杀伤，而维生素 B 依赖途径的突变体则会减少剩余杀伤。通过证明宿主相关微生物群产生的维生素 B 可以影响复杂的宿主行为，我们揭示了动物饮食、微生物群和神经系统之间的新联系。
