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

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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.