Fungi grow within their food, externally digesting it and absorbing nutrients across a semirigid chitinous cell wall. Members of the new phylum Cryptomycota were proposed to represent intermediate ...fungal forms, lacking a chitinous cell wall during feeding and known almost exclusively from ubiquitous environmental ribosomal RNA sequences that cluster at the base of the fungal tree 1, 2. Here, we sequence the first Cryptomycotan genome (the water mold endoparasite Rozella allomycis) and unite the Cryptomycota with another group of endoparasites, the microsporidia, based on phylogenomics and shared genomic traits. We propose that Cryptomycota and microsporidia share a common endoparasitic ancestor, with the clade unified by a chitinous cell wall used to develop turgor pressure in the infection process 3, 4. Shared genomic elements include a nucleotide transporter that is used by microsporidia for stealing energy in the form of ATP from their hosts 5. Rozella harbors a mitochondrion that contains a very rapidly evolving genome and lacks complex I of the respiratory chain. These degenerate features are offset by the presence of nuclear genes for alternative respiratory pathways. The Rozella proteome has not undergone major contraction like microsporidia; instead, several classes have undergone expansion, such as host-effector, signal-transduction, and folding proteins.
•Phylogenomics demonstrates Rozella and microsporidia are closely related early fungi•The Rozella genome encodes four chitin synthases, including one with a myosin domain•The Rozella mitochondrial genome shows evidence of rapid evolution and degeneration•The Rozella nuclear genome lacks a large number of genes for primary metabolism
As decomposers or plant pathogens, fungi deploy invasive growth and powerful carbohydrate active enzymes to reduce multicellular plant tissues to humus and simple sugars. Fungi are perhaps also the ...most important mutualistic symbionts in modern ecosystems, transporting poorly soluble mineral nutrients to plants and thus enhancing the growth of vegetation. However, at their origin over a billion years ago, fungi, like plants and animals, were unicellular marine microbes. Like the other multicellular kingdoms, Fungi evolved increased size, complexity, and metabolic functioning. Interactions of fungi with plants changed terrestrial ecology and geology and modified the Earth's atmosphere. In this review, we discuss the diversification and ecological roles of the fungi over their first 600 million years, from their origin through their colonization of land, drawing on phylogenomic evidence for their relationships and metabolic capabilities and on molecular dating, fossils, and modeling of Earth's paleoclimate.
Synopsis
Eukaryotes have evolved myriad ways of uniting gametes during sexual reproduction. A repeated pattern is the convergent evolution of a mating system with the fusion of larger gametes with ...smaller gametes (anisogamy) from that of fusion between morphologically identical gametes (isogamy). In anisogamous species, sexes are defined as individuals that produce only one gamete type. Although sexes abound throughout Eukarya, in fungi there are no biological sexes, because even in anisogamous species, individuals are hermaphroditic and produce both gamete types. For this reason, the term mating types is preferred over sexes, and, thus defined, only individuals of differing mating types can mate (homoallelic incompatibility). In anisogamous fungal species, there is scant evidence that there are more than two mating types, and this may be linked to genetic constraints, such as the use of mating types to determine the inheritance of cytoplasmic genomes. However, the mushroom fungi (Agaricomycetes) stand out as having both large numbers of mating types within a species, which will allow nearly all individuals to be compatible with each other, and reciprocal exchange of nuclei during mating, which will avoid cytoplasmic mixing and cyto-nuclear conflicts. Although the limitation of mating types to two in most fungi is consistent with the cyto-nuclear conflicts model, there are many facets of the Agaricomycete life cycle that also suggest they will demand a high outbreeding efficiency. Specifically, they are mostly obligately sexual and outcrossing, inhabit complex competitive niches, and display broadcast spore dispersal. Subsequently, the Agaricomycete individual pays a high cost to being choosy when encountering a mate. Here, I discuss the costs of mate finding and choice and demonstrate how most fungi have multiple ways of reducing these costs, which can explain why mating types are mostly limited to two per species. Nevertheless, it is perplexing that fungi have not evolved multiple mating types on more occasions nor evolved sexes. The few exceptions to these rules suggest that it is dictated by both molecular and evolutionary constraints.
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 strains. In tetrapolar basidiomycete fungi, sexual type is determined by two unlinked loci, MATA and MATB. Genes in both loci define 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 strains of three Trichaptum species. We characterized the chromosomal location of MATA and MATB, the molecular structure of MAT regions and their allelic richness. The sequencing effort was sufficient to molecularly characterize multiple MAT alleles segregating before the speciation event of Trichaptum species. 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. 17,550 mating types were predicted based on the allelic classes. In vitro crosses allowed 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. We conclude that the genetic diversity of mating loci in Trichaptum is due to long-term balancing selection, with limited recombination and duplication activity. The large number of sequenced strains 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.
The frequency of sex in fungi Nieuwenhuis, Bart P. S.; James, Timothy Y.
Philosophical transactions - Royal Society. Biological sciences,
10/2016, Letnik:
371, Številka:
1706
Journal Article
Recenzirano
Odprti dostop
Fungi are a diverse group of organisms with a huge variation in reproductive strategy. While almost all species can reproduce sexually, many reproduce asexually most of the time. When sexual ...reproduction does occur, large variation exists in the amount of in- and out-breeding. While budding yeast is expected to outcross only once every 10 000 generations, other fungi are obligate outcrossers with well-mixed panmictic populations. In this review, we give an overview of the costs and benefits of sexual and asexual reproduction in fungi, and the mechanisms that evolved in fungi to reduce the costs of either mode. The proximate molecular mechanisms potentiating outcrossing and meiosis appear to be present in nearly all fungi, making them of little use for predicting outcrossing rates, but also suggesting the absence of true ancient asexual lineages. We review how population genetic methods can be used to estimate the frequency of sex in fungi and provide empirical data that support a mixed mode of reproduction in many species with rare to frequent sex in between rounds of mitotic reproduction. Finally, we highlight how these estimates might be affected by the fungus-specific mechanisms that evolved to reduce the costs of sexual and asexual reproduction.
This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.
Marine fungi Gladfelter, Amy S.; James, Timothy Y.; Amend, Anthony S.
CB/Current biology,
03/2019, Letnik:
29, Številka:
6
Journal Article
Recenzirano
Odprti dostop
Fungi play a dominant role in terrestrial environments where they thrive in symbiotic associations with plants and animals and are integral to nutrient cycling in diverse ecosystems. Everywhere that ...moisture and a carbon source coexist in the terrestrial biosphere, fungi are expected to occur. We know that fungi can be devastating to agricultural crops, both in the field and during their storage, and cause mortality in immunocompromised patients in numbers that rival the deaths from malaria. Yet fungi can also be harnessed as sources of food, chemicals and biofuels when humans exploit fungal metabolism. Despite their central role in the health and disease of the terrestrial biosphere, much less is known about the function and potential of marine fungi. Are fungi ubiquitous in marine environments as they are on land? Do they play the same or similar roles in these ecosystems? Here we describe the state of knowledge about the abundance and functions of fungi in the marine environment with a goal to stimulate new inquiry in this very open area.
Despite the central role of fungi in the health of the terrestrial biosphere, the functions of marine fungi are largely unexplored. Here, Gladfelter et al., explore the biology and impact of these lesser known organisms.
Mycoviruses Myers, Jillian M.; James, Timothy Y.
CB/Current biology,
02/2022, Letnik:
32, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Viruses infect virtually all forms of cellular life, and fungi are no exception. Knowledge regarding the diverse fungal viruses, or mycoviruses, including their genome structures, host ranges, and ...phenotypic effects, is growing at a fast pace. Mycovirus research has been stimulated by the idea that they could be an effective tool for biocontrol of fungal pathogens. In many cases, mycoviruses are known to reduce the growth rate of their host and/or reduce their virulence. This observation, however, creates a paradox as most mycoviruses are predominately transmitted vertically, which, according to theoretical predictions, should select for more mutualistic interactions. It is possible, therefore, that widespread mutualism between mycoviruses and their hosts has been overlooked. To properly weaponize mycoviruses as biocontrol agents, a better understanding of their basic biology, including transmission modes and molecular mechanisms of parasitism, is needed. In this primer we highlight what is known about the types of viruses that have been detected in fungi and their phenotypic effects. We pay special attention to three well-studied models — the hypovirulence-causing viruses (hypoviruses or Hypoviridae) of the chestnut blight fungus, the Sclerotinia sclerotiorum ssDNA virus SsHADV-1, and the killer viruses of Saccharomyces cerevisiae — and highlight avenues for further exploration.
Like virtually all other forms of life, fungi play host to a diverse array of viruses. In this Primer, Myers and James introduce the diverse biology and ecology of the ‘mycoviruses’.
Interactions between fungi and plants, including parasitism, mutualism, and saprotrophy, have been invoked as key to their respective macroevolutionary success. Here we evaluate the origins of ...plant-fungal symbioses and saprotrophy using a time-calibrated phylogenetic framework that reveals linked and drastic shifts in diversification rates of each kingdom. Fungal colonization of land was associated with at least two origins of terrestrial green algae and preceded embryophytes (as evidenced by losses of fungal flagellum, ca. 720 Ma), likely facilitating terrestriality through endomycorrhizal and possibly endophytic symbioses. The largest radiation of fungi (Leotiomyceta), the origin of arbuscular mycorrhizae, and the diversification of extant embryophytes occurred ca. 480 Ma. This was followed by the origin of extant lichens. Saprotrophic mushrooms diversified in the Late Paleozoic as forests of seed plants started to dominate the landscape. The subsequent diversification and explosive radiation of Agaricomycetes, and eventually of ectomycorrhizal mushrooms, were associated with the evolution of Pinaceae in the Mesozoic, and establishment of angiosperm-dominated biomes in the Cretaceous.
The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth-limiting nutrient to their plant host, has ...important implications for our understanding of plant–fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem-level biogeochemistry.
PDF
