Biology subjects

James, T. Y.

Publications and source records attributed to James, T. Y..

8 recordsLinked to original sources

bioRxiv2023

Genomic analysis of Ancylistes closterii, an enigmatic alga parasitic fungus in the arthropod-associated Entomophthoromycotina

Recent advances in fungal genome sequencing have dramatically altered our understanding of the phylogeny and evolution of Fungi. However, there are still many poorly studied obligate parasitic or symbiotic fungi for which we lack any genomic information or knowledge of where they fit in the fungal phylogeny. Ancylistes, an endoparasite of desmid green algae, is such an understudied fungal genus. This genus has been taxonomically placed in the group of arthropod pathogens and saprobes, Entomophthoromycotina in Zoopagomycota. Understanding the phylogenetic position of Ancylistes provides insights into the nutritional evolution of Zoopagomycota, which is primarily composed of animal-associated fungi. In this study, we found and cultivated Ancylistes closterii with its host Closterium sp. and sequenced its genome to investigate its phylogenetic position and evolution. Phylogenetic analyses using rDNA and genome-scale datasets showed that A. closterii was sister to other Entomophthoromycotina fungi, confirming the taxonomic position of Ancylistes. Despite the ecological distinctiveness between Ancylistes and other Entomophthoromycotina fungi, our comparative genomic analyses revealed many shared traits of these fungi such as lineage-specific subtilases and hybrid histidine kinases. Ancylistes also possessed unique genes among Zoopagomycota fungi, such as plant cell wall degrading enzymes which could be important for infection of algae. SignificanceImproved taxon sampling is important for inferring a robust phylogeny of Fungi. However, there are still poorly studied obligate parasitic taxa whose DNA sequencing is challenging, especially in Zoopagomycota, one of the early diverging lineages of Fungi. This study focused on a long-neglected algal parasite, Ancylistes closterii, which belongs to the arthropod-associated group, Entomophthoromycotina. We rediscovered A. closterii and established a dual culture of fungus and its host alga, which enabled the first molecular analysis of this enigmatic parasite. Our results provide new insights into the nutritional evolution of primarily animal-associated Zoopagomycota.

evolutionary biology↗

bioRxiv2023

Reticulate evolution and rapid development of reproductive barriers upon secondary contact pose challenges for species delineation in a forest fungus

Reproductive barriers within morphospecies of the mushroom-forming fungi tend to be stronger between sympatric lineages, leading to speculation on whether they are being reinforced by selection against hybrids. In this study we use population genomic analyses together with in vitro crosses of a global sample of the wood decay fungus Trichaptum abietinum to investigate reproductive barriers within this morphotaxon and the processes that have shaped them. Our phylogeographic analyses show that the morphospecies is delimited into six major lineages, one in Asia, two in Europe, and three in North America. The two lineages present in Europe are interfertile and admixed, whereas our crosses show that the North American lineages are reproductively isolated. In Asia a more complex pattern appears, with partial intersterility between multiple sub-lineages that likely originated independently and more recently than the reproductive barriers in North America. We found pre-mating barriers in T. abietinum to be moderately correlated with genomic divergence, whereas fitness of the mated hybrids showed a strong positive correlation with increasing genomic divergence. Genome wide association analyses identified candidate genes with programmed cell death annotations, which are known to be involved in intersterility in distantly related fungi. Our demographic modelling and phylogenetic network analyses suggest that reproductive barriers in Trichaptum abietinum could have been reinforced upon secondary contact between lineages that diverged in allopatry during the Pleistocene glacial cycles. Our combination of experimental and genomic approaches demonstrate how T. abietinum is a tractable system for studying speciation mechanims.

evolutionary biology↗

bioRxiv2023

DNA virus BdDV-1 of the amphibian pathogen Batrachochytrium dendrobatidis is associated with hypervirulence

The Global Panzootic Lineage (GPL) of the pathogenic fungus Batrachochytrium dendrobatidis (Bd) has caused severe amphibian population declines, yet the drivers underlying the high frequency of GPL in regions of amphibian decline are unclear. Using publicly available Bd genome sequences, we identified multiple non-GPL Bd isolates that contain a circular Rep-encoding single stranded DNA (CRESS)-like virus which we named BdDV-1. We further sequenced and constructed genome assemblies with long read sequences to find that the virus is integrated into the nuclear genome in some strains. Attempts to cure virus positive isolates were unsuccessful, however, phenotypic differences between naturally virus positive and virus negative Bd isolates suggested that BdDV-1 decreases the growth of its host in vitro but increases the virulence of its host in vivo. BdDV-1 is the first described CRESS DNA mycovirus of zoosporic true fungi with a distribution inversely associated with the emergence of the panzootic lineage.

microbiology↗

bioRxiv2022

Human commensal Candida albicans strains demonstrate substantial within-host diversity and retained pathogenic potential

Candida albicans is a frequent colonizer of human mucosal surfaces as well as an opportunistic pathogen. C. albicans is remarkably versatile in its ability to colonize diverse host sites with differences in oxygen and nutrient availability, pH, immune responses, and resident microbes, among other cues. It is unclear how the genetic background of a commensal colonizing population can influence the shift to pathogenicity. Therefore, we undertook an examination of commensal isolates from healthy donors with a goal of identifying site-specific phenotypic adaptation and genetic variation associated with these phenotypes. We demonstrate that healthy people are reservoirs for genotypically and phenotypically diverse C. albicans strains, and that this genetic diversity includes both SNVs and structural rearrangements. Using limited diversity exploitation, we identified a single nucleotide change in the uncharacterized ZMS1 transcription factor that was sufficient to drive hyper invasion into agar. However, our commensal strains retained the capacity to cause disease in systemic models of infection, including outcompeting the SC5314 reference strain during systemic competition assays. This study provides a global view of commensal strain variation and within-host strain diversity of C. albicans and suggests that selection for commensalism in humans does not result in a fitness cost for invasive disease.

microbiology↗

bioRxiv2021

Long-term balancing selection in highly dynamic mating loci generates trans-species polymorphisms in fungi

Balancing selection, an evolutionary force that retains genetic diversity, has been detected in multiple genes and organisms, such as the sexual mating loci in fungi. However, to quantify the strength of balancing selection and define the mating-related genes require a large number of specimens. In tetrapolar basidiomycete fungi, sexual type is determined by two unlinked loci, MATA and MATB. Genes in both loci defines mating type identity, control successful mating and completion of the life cycle. These loci are usually highly diverse. Previous studies have speculated, based on culture crosses, that species of the non-model genus Trichaptum (Hymenochaetales, Basidiomycota) possess a tetrapolar mating system, with multiple alleles. Here, we sequenced a hundred and eighty specimens of three Trichaptum species. We characterized the chromosomal location of MATA and MATB, the molecular structure of MAT regions and their allelic richness. Our sequencing effort was sufficient to molecularly characterize multiple MAT alleles segregating before the speciation event of Trichaptum species. Our analyses suggested that long-term balancing selection has generated trans-species polymorphisms. Mating sequences were classified in different allelic classes based on an amino acid identity (AAI) threshold supported by phylogenetics. The inferred allelic information mirrored the outcome of in vitro crosses, thus allowing us to support the degree of allelic divergence needed for successful mating. Even with the high amount of divergence, key amino acids in functional domains are conserved. The observed allelic classes could potentially generate 14,560 different mating types. We conclude that the genetic diversity of mating in Trichaptum loci is due to long-term balancing selection, with limited recombination and duplication activity. Our large number of sequenced specimens highlighted the importance of sequencing multiple individuals from different species to detect the mating-related genes, the mechanisms generating diversity and the evolutionary forces maintaining them. Author summaryFungi have complex mating systems, and basidiomycete fungi can encode thousands of mating types. Individuals with the same mating type cannot mate. This sexual system has evolved to facilitate sexual mating, increasing the chances to recombine into advantageous allelic combination and prune deleterious alleles. We explored the genomes of hundred and eighty specimens, combined with experimental mating studies of selected specimens, from a non-model organism (Trichaptum). We characterized the genomic regions controlling sex. The mating ability of the specimens confirmed the role of the mating alleles observed in the genomic data. The detailed analyses of many specimens allowed us to observe gene duplication and rearrangements within the mating loci, increasing the diversity within these loci. We supported previous suggestions of balancing selection in this region, an evolutionary force that maintains genomic diversity. These results supports that our fungal specimens are prone to outcross, which might facilitate the adaptation to new conditions.

genomics↗

bioRxiv2021

Clonal evolution in serially passaged Cryptococcus neoformans x deneoformans hybrids reveals a heterogenous landscape of mitotic recombination

Cryptococcus neoformans x deneoformans hybrids (also known as serotype AD hybrids) are basidiomycete yeasts that are common in a clinical setting. Like many hybrids, the AD hybrids are largely locked at the F1 stage and are mostly unable to undergo normal meiotic reproduction. However, these F1 hybrids, which display a high ([~]10%) sequence divergence are known to genetically diversify through mitotic recombination and aneuploidy, and this diversification may be adaptive. In this study, we evolved a single AD hybrid genotype in six diverse environments by serial passaging and then used genome resequencing of evolved clones to determine evolutionary mechanisms of adaptation. The evolved clones generally increased fitness after passaging, accompanied by an average of 3.3 point mutations, 2.9 loss of heterozygosity (LOH) events, and 0.7 trisomic chromosomes per clone. LOH occurred through nondisjunction of chromosomes, crossing over consistent with break-induced replication, and gene conversion, in that order of prevalence. The breakpoints of these recombination events were significantly associated with regions of the genome with lower sequence divergence between the parents and clustered in subtelomeric regions, notably in regions that had undergone introgression between the two parental species. Parallel evolution was observed, particularly through repeated homozygosity via nondisjunction, yet there was little evidence of environment-specific parallel change for either LOH, aneuploidy, or mutations. These data show that AD hybrids have both a remarkable genomic plasticity and yet are challenged in the ability to recombine through sequence divergence and chromosomal rearrangements, a scenario likely limiting the precision of adaptive evolution to novel environments.

genetics↗

bioRxiv2020

A genome-scale phylogeny of Fungi; insights into early evolution, radiations, and the relationship between taxonomy and phylogeny

Phylogenomic studies based on genome-scale amounts of data have greatly improved understanding of the tree of life. Despite their diversity, ecological significance, and biomedical and industrial importance, large-scale phylogenomic studies of Fungi are lacking. Furthermore, several evolutionary relationships among major fungal lineages remain controversial, especially those at the base of the fungal phylogeny. To begin filling these gaps and assess progress toward a genome-scale phylogeny of the entire fungal kingdom, we compiled a phylogenomic data matrix of 290 genes from the genomes of 1,644 fungal species that includes representatives from most major fungal lineages; we also compiled 11 additional data matrices by subsampling genes or taxa based on filtering criteria previously shown to improve phylogenomic inference. Analyses of these 12 data matrices using concatenation- and coalescent-based approaches yielded a robust phylogeny of the kingdom in which [~]85% of internal branches were congruent across data matrices and approaches used. We found support for several relationships that have been historically contentious (e.g., for the placement of Wallemiomycotina (Basidiomycota), as sister to Agaricomycotina), as well as evidence for polytomies likely stemming from episodes of ancient diversification (e.g., at the base of Basidiomycota). By examining the relative evolutionary divergence of taxonomic groups of equivalent rank, we found that fungal taxonomy is broadly aligned with genome sequence divergence, but also identified lineages, such as the subphylum Saccharomycotina, where current taxonomic circumscription does not fully account for their high levels of evolutionary divergence. Our results provide a robust phylogenomic framework to explore the tempo and mode of fungal evolution and directions for future fungal phylogenetic and taxonomic studies.

evolutionary biology↗

bioRxiv2018

Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens

Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but select species keep insects alive while sporulating, which enhances dispersal. Transcriptomics and metabolomics studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses, yet mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which appear to represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

ecology↗