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1. Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

   https://doi.org/10.1093/gbe/evad046  

   Wang, Yan; Chang, Ying; Ortañez, Jericho; Peña, Jesús F; Carter-House, Derreck; Reynolds, Nicole K; Smith, Matthew E; Benny, Gerald; Mondo, Stephen J; Salamov, Asaf; et al (April 2023, Genome Biology and Evolution)

   Ma, Li-Jun (Ed.)

   Abstract Fungi have evolved over millions of years and their species diversity is predicted to be the second largest on the earth. Fungi have cross-kingdom interactions with many organisms that have mutually shaped their evolutionary trajectories. Zygomycete fungi hold a pivotal position in the fungal tree of life and provide important perspectives on the early evolution of fungi from aquatic to terrestrial environments. Phylogenomic analyses have found that zygomycete fungi diversified into two separate clades, the Mucoromycota which are frequently associated with plants and Zoopagomycota that are commonly animal-associated fungi. Genetic elements that contributed to the fitness and divergence of these lineages may have been shaped by the varied interactions these fungi have had with plants, animals, bacteria, and other microbes. To investigate this, we performed comparative genomic analyses of the two clades of zygomycetes in the context of Kingdom Fungi, benefiting from our generation of a new collection of zygomycete genomes, including nine produced for this study. We identified lineage-specific genomic content that may contribute to the disparate biology observed in these zygomycetes. Our findings include the discovery of undescribed diversity in CotH, a Mucormycosis pathogenicity factor, which was found in a broad set of zygomycetes. Reconciliation analysis identified multiple duplication events and an expansion of CotH copies throughout the Mucoromycotina, Mortierellomycotina, Neocallimastigomycota, and Basidiobolus lineages. A kingdom-level phylogenomic analysis also identified new evolutionary relationships within the subphyla of Mucoromycota and Zoopagomycota, including supporting the sister-clade relationship between Glomeromycotina and Mortierellomycotina and the placement of Basidiobolus as sister to other Zoopagomycota lineages. 

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2. Ploidy evolution in a wild yeast is linked to an interaction between cell type and metabolism

   https://doi.org/10.1371/journal.pbio.3001909  

   Crandall, Johnathan G; Fisher, Kaitlin J; Sato, Trey K; Hittinger, Chris Todd (November 2023, PLOS Biology)

   Zanders, Sarah E (Ed.)

   Ploidy is an evolutionarily labile trait, and its variation across the tree of life has profound impacts on evolutionary trajectories and life histories. The immediate consequences and molecular causes of ploidy variation on organismal fitness are frequently less clear, although extreme mating type skews in some fungi hint at links between cell type and adaptive traits. Here, we report an unusual recurrent ploidy reduction in replicate populations of the budding yeastSaccharomyces eubayanusexperimentally evolved for improvement of a key metabolic trait, the ability to use maltose as a carbon source. We find that haploids have a substantial, but conditional, fitness advantage in the absence of other genetic variation. Using engineered genotypes that decouple the effects of ploidy and cell type, we show that increased fitness is primarily due to the distinct transcriptional program deployed by haploid-like cell types, with a significant but smaller contribution from absolute ploidy. The link between cell-type specification and the carbon metabolism adaptation can be traced to the noncanonical regulation of a maltose transporter by a haploid-specific gene. This study provides novel mechanistic insight into the molecular basis of an environment–cell type fitness interaction and illustrates how selection on traits unexpectedly linked to ploidy states or cell types can drive karyotypic evolution in fungi. 

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3. Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses

   https://doi.org/10.1128/mBio.02027-20  

   Myers, J. M.; Bonds, A. E.; Clemons, R. A.; Thapa, N. A.; Simmons, D. R.; Carter-House, D.; Ortanez, J.; Liu, P.; Miralles-Durán, A.; Desirò, A.; et al (October 2020, mBio)

   Taylor, John W. (Ed.)

   ABSTRACT Mycoviruses are widespread and purportedly common throughout the fungal kingdom, although most are known from hosts in the two most recently diverged phyla, Ascomycota and Basidiomycota, together called Dikarya. To augment our knowledge of mycovirus prevalence and diversity in underexplored fungi, we conducted a large-scale survey of fungi in the earlier-diverging lineages, using both culture-based and transcriptome-mining approaches to search for RNA viruses. In total, 21.6% of 333 isolates were positive for RNA mycoviruses. This is a greater proportion than expected based on previous taxonomically broad mycovirus surveys and is suggestive of a strong phylogenetic component to mycoviral infection. Our newly found viral sequences are diverse, composed of double-stranded RNA, positive-sense single-stranded RNA (ssRNA), and negative-sense ssRNA genomes and include novel lineages lacking representation in the public databases. These identified viruses could be classified into 2 orders, 5 families, and 5 genera; however, half of the viruses remain taxonomically unassigned. Further, we identified a lineage of virus-like sequences in the genomes of members of Phycomycetaceae and Mortierellales that appear to be novel genes derived from integration of a viral RNA-dependent RNA polymerase gene. The two screening methods largely agreed in their detection of viruses; thus, we suggest that the culture-based assay is a cost-effective means to quickly assess whether a laboratory culture is virally infected. This study used culture collections and publicly available transcriptomes to demonstrate that mycoviruses are abundant in laboratory cultures of early-diverging fungal lineages. The function and diversity of mycoviruses found here will help guide future studies into mycovirus origins and ecological functions. IMPORTANCE Viruses are key drivers of evolution and ecosystem function and are increasingly recognized as symbionts of fungi. Fungi in early-diverging lineages are widespread, ecologically important, and comprise the majority of the phylogenetic diversity of the kingdom. Viruses infecting early-diverging lineages of fungi have been almost entirely unstudied. In this study, we screened fungi for viruses by two alternative approaches: a classic culture-based method and by transcriptome-mining. The results of our large-scale survey demonstrate that early-diverging lineages have higher infection rates than have been previously reported in other fungal taxa and that laboratory strains worldwide are host to infections, the implications of which are unknown. The function and diversity of mycoviruses found in these basal fungal lineages will help guide future studies into mycovirus origins and their evolutionary ramifications and ecological impacts. 

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4. Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi

   https://doi.org/10.1038/s41598-021-82607-4  

   Chang, Ying; Rochon, D’Ann; Sekimoto, Satoshi; Wang, Yan; Chovatia, Mansi; Sandor, Laura; Salamov, Asaf; Grigoriev, Igor V.; Stajich, Jason E.; Spatafora, Joseph W. (February 2021, Scientific Reports)

   Abstract The zoosporic obligate endoparasites,Olpidium,hold a pivotal position to the reconstruction of the flagellum loss in fungi, one of the key morphological transitions associated with the colonization of land by the early fungi. We generated genome and transcriptome data from non-axenic zoospores ofOlpidium bornovanusand used a metagenome approach to extract phylogenetically informative fungal markers. Our phylogenetic reconstruction strongly supportedOlpidiumas the closest zoosporic relative of the non-flagellated terrestrial fungi. Super-alignment analyses resolvedOlpidiumas sister to the non-flagellated terrestrial fungi, whereas a super-tree approach recovered different placements ofOlpidium,but without strong support. Further investigations detected little conflicting signal among the sampled markers but revealed a potential polytomy in early fungal evolution associated with the branching order amongOlpidium, Zoopagomycota and Mucoromycota. The branches defining the evolutionary relationships of these lineages were characterized by short branch lengths and low phylogenetic content and received equivocal support for alternative phylogenetic hypotheses from individual markers. These nodes were marked by important morphological innovations, including the transition to hyphal growth and the loss of flagellum, which enabled early fungi to explore new niches and resulted in rapid and temporally concurrent Precambrian diversifications of the ancestors of several phyla of fungi. 

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5. Asymmetric genome merging leads to gene expression novelty through nucleo‐cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids

   https://doi.org/10.1111/nph.20249  

   Prost‐Boxoen, Lucas; Bafort, Quinten; Van_de_Vloet, Antoine; Almeida‐Silva, Fabricio; Paing, Yunn Thet; Casteleyn, Griet; D'hondt, Sofie; De_Clerck, Olivier; Van_de_Peer, Yves (January 2025, New Phytologist)

   Summary Genome merging is a common phenomenon causing a wide range of consequences on phenotype, adaptation, and gene expression, yet its broader implications are not well‐understood. Two consequences of genome merging on gene expression remain particularly poorly understood: dosage effects and evolution of expression.We employedChlamydomonas reinhardtiias a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection experiment.Utilizing fitness assays, flow cytometry, and RNA‐Seq, we assessed the immediate consequences of genome merging and subsequent evolution. Our findings reveal substantial alterations in genome size, gene expression, protein homeostasis, and cytonuclear stoichiometry. Gene expression exhibited expression‐level dominance and transgressivity (i.e. expression level higher or lower than either parent). Ongoing expression‐level dominance and a pattern of ‘functional dominance’ from the haploid parent was observed.Despite major genomic and nucleo‐cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging inChlamydomonas reinhardtiiand possibly other systems. 

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