Evolutionary genomics of early-diverging fungi living in the gut of insects

真菌在水生和陆地生态系统中都发挥着关键作用。它们积极影响并与各种生物相互作用。然而，我们仍然不清楚真菌是如何适应环境并进化出与其他生物实体交流的能力的。对早期分歧真菌群的研究有助于揭示真菌在古真核生物陆生化中的重要性。由于其重要的系统发育位置，对早期分歧真菌的进一步研究将有助于我们更多地了解它们的自然历史和共生作用的影响。Harpellales（Zoopagomycota）是传统的早期分歧真菌的分支，生活在双翅目昆虫幼虫的消化道中（例如，黑蝇、蠓、蚊子）。显微镜和初步的基因组检查都发现了Harpellales中意想不到的模式，包括水平基因转移，潜在的全基因组复制，以及真菌基底细胞中与昆虫肠道上皮相互作用表面的电子致密颗粒。然而，我们仍然缺乏一个全面的理解，以连接遥远的相关观察，以及一个“大图片”，以了解它们背后的进化故事。由于缺乏高质量的Harpellales基因组组装，我们无法测试有关Harpellales在疾病传播昆虫肠道中的潜在多方面作用的详细假设。我的研究计划的目标是了解Harpellales的进化基因组学，并解码这些真菌如何与双翅目宿主相互作用，使用实验和计算方法相结合。这一长期目标将通过三个直接的短期目标来实现。具体而言，我将：1）使用长读段测序数据组装高质量的Harpellales基因组，2）研究Harpellales在昆虫宿主存在和不存在的情况下的基因表达差异，以及3）检查两种Harpellales物种（Smittium cultured和Zancudomomericulisetae）的群体基因组学。总的来说，拟议的研究将有助于澄清微生物真菌如何进化并以Harpellales和Diptera为例与昆虫宿主相互作用。这种独特的共生系统也将创造新的机会来发现未被探索的生命规则。我的研究计划将使我们能够更好地了解真菌进化和宿主-微生物相互作用的详细机制，涵盖宿主选择/特异性，基因组复制，比较转录组学和群体基因组学的广泛主题。研究成果还将有助于开发新的和有效的生物防治方法，使用针对幼虫阶段的宿主特异性微生物真菌，而目前的方法主要集中在昆虫成虫上。通过这项研究，将为下一代生物学家提供高质量的培训，特别是在真菌学，昆虫学和进化微生物学领域。

Fungi play critical roles in both aquatic and terrestrial ecosystems. They actively influence and interact with various organisms. However, we are still unclear how fungi adapted to their environments and evolved abilities to communicate with other biological entities. Studies on early-diverging fungal groups have helped reveal the importance of fungi in the terrestrialization of ancient eukaryotes. Due to their crucial phylogenetic placement, further investigation of early-diverging fungi will help us understand more of their natural histories and impacts of symbiotic roles. Harpellales (Zoopagomycota) is a clade of traditional early-diverging fungi, living in the digestive tracts of Diptera insect larvae (e.g., black flies, midges, mosquitoes). Both microscopic and preliminary genomic examinations have identified unexpected patterns in Harpellales, including horizontal gene transfers, potential whole-genome duplications, and electron-dense particles in the fungal basal cells at the interacting surface with insect gut cuticles. However, we still lack a comprehensive understanding to connect the distantly related observations, as well as a "big picture" to make sense of the evolutionary stories behind them. The lack of high-quality genome assemblies of Harpellales prevents us from testing detailed hypotheses regarding the potential multifaceted roles of Harpellales in the gut of disease-transmitting insects. The goal of my research program is to understand the evolutionary genomics of Harpellales and to decode how these fungi interact with their Diptera hosts, using a combination of experimental and computational approaches. This long-term goal will be achieved with three straightforward short-term objectives. Specifically, I will: 1) assemble high-quality Harpellales genomes using long-read sequencing data, 2) investigate gene expression differences of Harpellales with the presence and absence of insect hosts, and 3) examine population genomics of two Harpellales species (Smittium culicis and Zancudomyces culisetae). Overall, the proposed research will aid in clarifying how microbial fungi evolve and interact with insect hosts by using Harpellales and Diptera as examples. This unique symbiotic system will also create novel opportunities to discover unexplored rules of life. My research program will allow us to better understand detailed mechanisms in fungal evolution and host-microbe interactions, covering broad topics of host choice/specificity, genomic duplication, comparative transcriptomics, and population genomics. The research output will also contribute to the development of novel and efficient biocontrol approaches using host-specific microbial fungi targeting larval stages, while current methods mostly focus on the insect adults. Through this research, high-quality training will be provided for the next generation of biologists, especially in fields of mycology, entomology, and evolutionary microbiology.