Research

We study fungal ecology and evolution by integrating modern genomics with traditional taxonomic methods, with a specific focus on the early-diverging groups (e.g., Zoopagomycota and Neocallimastigomycota—the former Zygomycota and Chytridiomycota lineages). We use Harpellales fungi (symbionts) and lower Dipteran insects (e.g., black flies, mosquitoes, midges) as the model to study genomic interations between gut fungal symbionts and their disease-bearing insect hosts.

------ Mosquito ------- - Midge ------------ Black fly

 
Specific Topics:

1) Horizontal Gene Transfer (HGT) in Fungi
Since they diverged from animals over 1 billion years ago, some fungal descendants have established interactions with many organisms in nature and have become well adapted to various lifestyles. Genetic interactions between fungi and bacteria are not uncommon and HGT has proven to be one of the major factors to influence each other along the evolution. This process in eukaryotes is still underexplored and there are only a few cases reported sparsely up to date. It is hypothesized that HGT could be one of universal mechanisms to acquire new genes during eukaryotic evolution as well. However, tests of this hypothesis are limited due to the paucity of available eukaryotic genomes. During my Ph.D. study, I generated the first set of whole genome sequences of Harpellales fungi (Zoopagomycota) that live in the gut of disease-bearing insects (e.g., mosquitos and black flies). I developed a tool (https://github.com/YanWangTF/HGTfilter) to identify eukaryote-origin HGT elements in fungal genomes based on sequence similarities and documented symbiotic relationships. One gene that encodes a mosquito-like polyubiquitin chain was successfully identified with further confirmation from phylogenetics, amino acid compositions, and secondary structures (Wang et al. 2016 MBE). Similarly, the tool has helped reveal more examples of HGT from animals (e.g., galactose binding lectin) and plants (e.g., rhamnogalacturonate lyase) to another early-diverging fungal lineage—Neocallimastigomycota (Wang et al. 2019 mSystems).


Fig. 1 A schematic diagram of the Horizontal Gene Transfer (HGT) events recently revealed in fungal genomes that have eukaryotic origins. Genes (a, b, and c) found in fungi may have different evolutionary histories. Some of them (represented by "gene a") universally exist in the Kingdom Fungi and have been found in both plants and animals as well. They are derived from the most recent common ancestor of all eukaryotes. While other genes ("b" or "c") are maintained by certain lineages on the Fungal Tree of Life but missing from the rest branches. These genes could resemble the plant homologs (i.e., gene "b") or the animal ones (i.e., gene "c"). Usually, their foreign origin can be confirmed by phylogenetic analyses based on sequence similarities.

2) Symbiosis and Comparative Genomics
A classic question in evolution is how organisms form symbiotic relationships. Another focus of my research is the origin and molecular mechanisms of fungus-animal associations, with specific interests in the early-stage establishment. In a recent study (Wang et al. 2018 mBio), my collaborators and I identified a set of genetic tools that are shared among insect-associated fungi (both commensals and pathogens) but are missing in free-living ones. These Fungus-Insect Symbiotic Core Genes (FISCoG) were assigned with important biological functions ranging from adhesion, hydrolysis, to host immune repression, which mirror the essential steps to initialize a symbiotic interaction. In a separate study, a comparative genomic method was developed that helped reveal a unique set of protein family domains maintained by the mammal gut fungi (Neocallimastigomycota), but lost in the rest of fungal kingdom (Wang et al. 2019 mSystems). These elements were suggested to be important in explaining the exceptional ability to degrade plant biomass in the rumen for their herbivore hosts


Fig. 2 Comparative genomics between the entomopathogenic fungi (Ascomycota in red and Zoopagomycota in green) and insect commensals of the Harpellales (in blue). (a) Venn diagram derived from interphylum homologues with the aim to sort out fungus-insect symbiotic core genes (FISCoGs), using pathogenic representatives both from Ascomycota and Zoopagomycota and commensals from Harpellales. (b) Box plot comparisons of genome-wide PHI genes, signal peptides, and transmembrane helices among the three groups. (c) Cladogram exhibiting the phylogenetic relationship of the included taxa based on 29 shared single-copy genes. (d) Heat map enrichment of the FISCoG toolbox among the insect-associated fungi (analyzed by removing the 1,612 false-positive hits with non-insect-associated Zoopagomycota genomes from those corresponding to the 1,620 shared genes in panel a). (e) Heat map comparison showing the enrichment pattern of genome-wide Pfam domains.

3) Fungal Phylogeny and Divergence Time Estimation
Phylogenetic reconstruction and divergence time estimations are informative in recovering the evolutionary kinships of various fungal organisms and deciphering how they have occupied the current territory. These approaches allow us to predict and investigate the roles of fungi in shaping the environment. Taking advantage of the development of molecular phylogenetic markers with increasing resolving powers, I have applied modern phylogenetic methods to establish a new fungal genus (Wang et al. 2013 Mycologia), delimitate species complexes (Wang et al. 2014 MPE), estimate divergence time of certain fungal clades (Wang et al. 2019 mSystems), and study the co-evolutionary relationship with symbiotic partners (Wang et al. 2019 MPE).


Fig. 3 Bayesian Maximum Clade Credibility tree showing the estimated divergence time of the Smittium sensu lato clade. Interested nodes are labeled with the mean divergence times (Ma) and blue bars representing the 95% Highest-Probability Density (HPD) range. Bayesian posterior probabilities (BPP out of 1.0) are denoted on the branches.
 

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