3.7 Ascomycota

With about 64,000 species known, Ascomycota (informally, ascomycetes) is the largest group in Kingdom Fungi. Like the fungi that belong to its sister group, the Basidiomycota, the majority of species within the Ascomycota are filamentous fungi that produce a mycelium in which the hyphae are regularly septate. What characterised the Ascomycota is that their sexual spores (ascospores) are formed within a sac-like structure hyphal cell which is called an ascus (from the Greek askos which means ‘bag’).

Ascomycota includes many species of great importance. Names to look out for include the plant pathogens Fusarium, Magnaporthe, and Cryphonectria, as well as medically important genera like Candida and Pneumocystis that cause human disease, and Penicillium chrysogenum, the producer of penicillin, the first antibiotic to be discovered, and Penicillium citrinum and Aspergillus terreus which were among the first moulds shown to produce precursors of today’s ‘wonder drugs’ the statins, which are currently crucial to cholesterol-management by many millions of patients (see Section 10.13).

The majority of the lichenised fungi belong to the Ascomycota, as does the yeast used in our baking and brewing industries, Saccharomyces cerevisiae. As we’ll see later (Section 5.2) this yeast, in particular, has been used as a model organism for science experimentation for well over a century, and is the best characterised of all eukaryotic cells.

Ascomycota contribute to other foods: Penicillium camembertii and P. roqueforti condition cheese, Fusarium venenatum provides the mycoprotein™ used to make the vegetarian meat substitute Quorn, and two celebrated edible fungi are the morel, Morchella esculenta, and truffle Tuber magnatum (white truffle of Northern Italy) and T. melanosporum (black truffle of the Périgord region in France)(see Chapter 11). Some of these moulds (especially Aspergillus spp.) produce metabolites that spoil food and, like aflatoxins, can be extremely toxic (see Section 13.4).

Ascomycota also includes the majority of fungi for which sexual reproduction has not been observed. In traditional classifications (based largely on morphological features) these asexual fungi have been placed in a separate group, variously called Deuteromycetes, Deuteromycotina or Deuteromycota (according to whether the taxonomist concerned though they deserved the status of Class, Subphylum or Phylum). Molecular techniques now permit them to be classified among their sexually reproducing relatives from comparison of nucleic acid sequences, which makes this separation redundant.

The AFTOL review of the phylogeny of phylum Ascomycota (Blackwell et al., 2006) remains current, with just some minor changes to reflect more recent improvements in understanding. AFTOL divided the phylum into three major evolutionary lineages, given the rank of subphylum:

  • Taphrinomycotina, also known, informally, as the archiascomycetes; for example: Protomyces, Taphrina, Pneumocystis.
  • Saccharomycotina, also known, informally, as the hemiascomycetes; for example: Saccharomyces, Pichia, Candida.
  • Pezizomycotina, also known, informally, as the euascomycetes; for example: Aspergillus, Neurospora, Peziza.

Kurtzman & Sugiyama (2015) discuss the ecology, physiology, molecular biology, biotechnology, phylogeny, and systematics of Saccharomycotina and Taphrinomycotina, and focus on changes in knowledge resulting from molecular studies.

Members of the Taphrinomycotina do not make fruit bodies (called ascomata in this phylum). The group includes a varied collection of organisms, including the filamentous plant pathogen Taphrina. Taphrina deformans causes peach leaf curl, and witches’ broom disease of birch is caused by T. betulina; other species attack, oak, poplar, maple and many others). Taphrina normally grows in a yeast form until it infects plant tissues in which typical filamentous hyphae are formed. Ultimately the fungus forms a naked layer of asci on the deformed, frequently brightly pigmented surfaces of their hosts. CLICK HERE to see a page of illustrations.

The fission yeast Schizosaccharomyces pombe is also placed in the Taphrinomycotina. This species, first isolated in 1893 from East African millet beer (‘pombe’ is the Swahili word for beer), has been used as a model organism in molecular and cell biology for over 50 years. These yeast cells grow by apical extension, and then divide by medial fission through a new, centrally-placed, septum to produce two daughter cells of equal sizes. The regularity of this process, coupled with ease of cultivation, makes them a powerful tool in cell cycle research.

The fission yeast researcher Sir Paul Nurse won the 2001 Nobel Prize in Physiology or Medicine for his work on cyclin dependent kinases in cell cycle regulation, together with Lee Hartwell (who developed the genetic analysis of the cell cycle in budding yeast, Saccharomyces cerevisiae, and introduced the concept of checkpoints) and Tim Hunt (who discovered cyclins in sea urchins).

Other, even more enigmatic inclusions in the Taphrinomycotina are the human pathogen Pneumocystis and the widely-distributed genus Neolecta. Long considered to be a protozoan, Pneumocystis is now clearly accepted as a yeast-like fungus. Pneumocystis pneumonia (PCP) is caused by Pneumocystis jirovecii named in honour of the Czech parasitologist Otto Jirovec. Pneumocystosis is one of the most common infections in immunosuppressed patients because AIDS and other immunity impairments such as immunodeficiencies, steroid treatment, organ transplantation medication and cancers predispose the patient to Pneumocyctis infection.

Neolecta has been found in Asia, North and South America, and Northern Europe, in association with trees. The fungus produces club-shaped and brightly coloured fruiting bodies, known as ‘earth tongues’, which are a few to several cm tall. Neolecta vitellina grows from rootlets of its host, but it is not known whether the fungus is parasitic, saprotrophic, or symbiotic.

The Saccharomycotina contains a single order, the Saccharomycetales that includes the majority of the ascomycetous yeasts, including the economically important genera Saccharomyces and Candida. Yeasts usually grow as single cells that reproduce by budding or less frequently by fission. Asci and ascospores are not enclosed in the fruiting bodies (ascomata) commonly found in the filamentous ascomycetes.

Louis Pasteur, in 1857, demonstrated that yeasts caused the fermentation of grape juice to wine and eventually, yeasts were recognised as fungi. The name Saccharomyces means ‘sugar fungus’. However, historical records from ancient Egypt and China depict brewing and baking 8,000 to 10,000 years ago, and analysis of whole-genome sequences of over a thousand different Saccharomyces cerevisiae yeast strains isolated around the world from varied ecological niches in nature as well as baking and brewing industries demonstrated that S. cerevisiae originated in East Asia about 15,000 years ago (Peter et al., 2018). The authors showed that while domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates was mainly driven by the accumulation of single nucleotide polymorphisms, most of which are present at very low frequencies. Several independent domestication events spread budding yeast around the globe; genomic markers of domestication appeared about 4,000 years ago in sake yeast isolates, though such markers appeared in wine yeast isolates only 1,500 years ago.

Yeast cellular morphology is rather simple (CLICK HERE to see a page of illustrations), and yeast genomes tend to be smaller than those of filamentous fungi, but it is a highly adapted growth form. Not all yeasts are ascomycetes; there are members of the Basidiomycota that adopt a yeast form and the term ‘yeast-like’ also has been applied to dimorphic members of the zygomycete genus Mucor. Ascomycete yeasts are usually found in specialised habitats, which tend to be small volumes of liquid rich in organic carbon (for example, flower nectaries). Basidiomycete yeasts, in contrast, seem to be adapted to colonising solid surfaces that are poor in nutrients.

Candida albicans is commensal on humans, its success being apparently the combination of an extracellular lipase activity, the ability to form invasive hyphae and the ability to grow at 37°C. Candida albicans lives on the skin, in the mouth and gut and other mucous membranes of about 80% of the human population, and for most of the time with no harmful effect. When the balance between the normal microorganisms is lost, for example because of antibiotic treatment, hormonal disturbance or immunocompromise, overgrowth of C. albicans results in candidiasis, or ‘thrush’. This common condition is usually easily cured, but in immunocompromised patients, such as HIV-positive individuals, the yeast form of Candida reacts to environmental cues by switching into an invasive filamentous growth form and a systemic and very serious infection can result.

The Pezizomycotina or euascomycetes (‘true-ascomycetes) make up the majority (about 90%) of the Ascomycota, and includes most lichen fungi. These are the filamentous ascomycetes and their characteristic feature is that sexually reproducing species produce ascomata within which their sexual spores are formed in a sac-like ascus. Inevitably with such a large range of organisms, its members can be found in all aquatic and terrestrial habitats and participating in all ecosystems, including wood and litter decay, animal and plant pathogens, mycorrhizas and lichens (with only a few exceptions, all lichenised fungi belong to this group).

Prior to the application of molecular phylogenetics, classification of Pezizomycotina was based on the morphology and development of ascomata and asci. The four main ascoma morphologies are:

  • Apothecia.
  • Perithecia.
  • Cleistothecia.
  • Ascostromata.

Organisms that produced these fruit bodies are said to be apothecial, perithecial, cleistothecial or ascostromatic, as appropriate.

Apothecia are typically disk- to cup-shaped to spoon-shaped (spathulate) and produce their asci in a well defined tissue layer, a hymenium, which is exposed to the air.

Perithecia and cleistothecia are, respectively, partially or completely closed ascomata; their asci are formed in the central cavity (‘centrum’) of the ascoma. In perithecia, which are considered to be ‘true’ ascomata, the inner wall of the fruit body forms at the same time as the ascogenous hyphae develop. Asci are formed in a defined hymenium and are frequently mixed with sterile paraphyses arising from the subhymenial tissue although paraphyses are absent in some lineages (e.g. Hypocreales). The term hamathecium or hamathecial tissue is a general term applied to whatever tissue separates asci within the ascoma (it’s derived from the Greek háma, meaning ‘all together’). It may originate from different parts of the fruit body, be composed of paraphyses or other sterile cells, be generally-distributed or localised; it may even be absent (e.g. Dothidea).

In acostromata, the asci develop in preformed spaces, called locules, and the stroma often forms a flask-shaped (pseudothecia) or open, cup-shaped (hysterothecia and thyriothecia) structure that resembles the gross morphology of perithecia or apothecia.

Ascus walls appear to be multilayered in transmission electron micrographs, so a classification of asci has developed based on the number and thickness of wall layers as well as on the mechanism by which the ascospores are released (= dehiscence). The descriptive names for the major ascus types include:

  • unitunicate, ascus with relatively thin walls; encompassing operculate, inoperculate and prototunicate asci.
    • prototunicate, produced by apothecial, cleistothecial and perithecial fungi; thin-walled, globose to broadly club-shaped, ascospores released passively by disintegration of the ascus wall.
    • operculate, found in apothecial fungi; release ascospores through a defined opening with a ‘lid’ (operculum) that is formed either at the ascus apex or just below it.
    • inoperculate, produced by apothecial, cleistothecial and perithecial fungi; typically thin-walled, the tip of the ascus usually has a small pore filled with loose wall material; the spores are discharged through this pore, or if there is no pore, dehiscence by rupture of the ascus apex.
  • bitunicate, conspicuously thick-walled with two walls, called the exotunica and endotunica; produced by ascostromatic lichenised and nonlichenised species and ascohymenial lichens. In the traditional definition of bitunicate asci, fissitunicate dehiscence occurs (a fissitunicate ascus is a double-walled ascus where the inner wall pops completely out of the outer wall during dehiscence in a jack-in-the-box manner; it happens when the endotunica ruptures through the exotunica). Other dehiscence mechanisms exist among ‘bitunicate’ ascus morphologies involving little to no wall separation; these occur especially in lichenised taxa.

Some of these morphologies most likely represent ancestral traits for the Pezizomycotina (e.g. apothecium), while others have occurred several times through convergent evolution (e.g. cleistothecium, prototunicate asci). CLICK HERE to see a page of illustrations.

The current classification, based mainly on DNA phylogenies of Ascomycota divides Pezizomycotina into ten Classes (Spatafora et al., 2006); in the following list we show (in brackets) their ascoma and ascus morphologies and we also show some names to look out for:

  • Arthoniomycetes (apothecia; bitunicate asci); includes the lichen Lecanactis abietina (Schoch & Grube, 2015).
  • Dothideomycetes (ascostromata; bitunicate asci); contains Dothidia, Aureobasidium,
    Pleospora, Tyrannosorus (yes, honestly) and Tubeufia (Schoch & Grube, 2015).
  • Eurotiomycetes (perithecia, cleistothecia, ascostromata; bitunicate or prototunicate asci); contains Aspergillus, Penicillium, Histoplasma and Coccidioides (Geiser et al., 2015).
  • Laboulbeniomycetes (perithecia; prototunicate asci); comprises ectoparasites of insects and other arthropods (Laboulbeniales), e.g. Herpomyces, and mycoparasites and coprophiles (Pyxidiophorales), e.g. Pyxidiophora and Rhynchonectria; ascospores characterised by holdfasts.
  • Sordariomycetes (perithecia, cleistothecia; inoperculate, prototunicate asci); contains the bulk of the traditional ‘pyrenomycetes’, including Sordaria, Cordyceps, Neurospora, Hypocrea, Verticillium, Bombardia, Xylaria and Diaporthe (Zhang & Wang, 2015; Hyde et al., 2017).
  • Lecanoromycetes (apothecia, perithecia; bitunicate, inoperculate, prototunicate asci); composed exclusively of lichen-forming ascomycetes like Lecanora, Cladonia, Usnea, Peltigera, and Lobaria (Gueidan et al., 2015).
  • Leotiomycetes (apothecia, cleistothecia; inoperculate, prototunicate asci); contains Leotia, Sclerotinia, Monilinia, Mitrula, Hymenoscyphus, Microglossum and Cudonia (Zhang & Wang, 2015).
  • Lichinomycetes (apothecia; bitunicate, inoperculate, prototunicate asci); includes the lichen Lempholemma, Peltula, Geoglossum and Trichoglossum.
  • Orbiliomycetes (apothecia; inoperculate asci); contains Orbilia (Pfister, 2015).
  • Pezizomycetes (apothecia; operculate asci); includes the ‘discomycetes’ Peziza, Aleuria, Morchella, Gyromitra, Tuber and Pyronema (Pfister, 2015).

To these may be added:

  • Geoglossomycetes, Geoglossum and Trichoglossum, commonly called earth tongues, were previously included in the Leotiomycetes but rejected as members of that class by DNA analyses (Spatafora, 2007, in the Tree of Life Web Project at http://tolweb.org/Pezizomycotina/29296/2007.12.19).
  •  Xylonomycetes, this group is an example of the discovery of new fungi by multigene phylogenetic analyses of ‘exotic’ habitats; this new major lineage of Ascomycota was discovered in a survey of endophytic fungi cultured from living sapwood and leaves of rubber trees (Hevea spp.) in remote forests of Peru (Gazis et al., 2012).
  • Coniocybomycetes, a heterogeneous assemblage of fungi sharing the presence of a mazaedium (a fruiting body of some lichens in which the ascospores lie freely in a powdery mass that is enclosed in an ascome wall, or peridium) separated from within the Arthoniomycetes, Eurotiomycetes, Lecanoromycetes and Leotiomycetes by multigene phylogenetic analyses (Prieto et al., 2013).

The AFTOL data (Spatafora et al., 2006) strongly indicated Orbiliomycetes and Pezizomycetes as the most basal classes of Pezizomycotina, both consist of species that produce apothecia. The fossil genus Paleopyrenomycites from the Early Devonian Rhynie Chert (about 400 million years old) is the oldest accepted fossil member of Pezizomycotina, although its position within this subphylum is unclear (Beimforde et al., 2014).

Updated January, 2020