Mystery Fungus

For this week's semi-random taxon, I drew the fungal genus Trichangium. Unfortunately, there's not much I can say about this one. The single species of this genus, Trichangium vinosum was described by German mycologist Wilhelm Kirchstein in 1935 in a volume of the journal Annales Mycologici to which I don't have access (there are other volumes of this journal available at archive.org but seemingly not this one). The original collection was found growing on bark of a pear tree. Since then, Kirchstein's species seems to have gone largely unrecognised. I could find no further records under this name and recent synopses of ascomycete genera (e.g. Lumbsch & Huhndorf 2010) list it incertae sedis in the order Helotiales. Helotiales are mostly minute fungi with cup-shaped fruiting bodies that most commonly grow as saprobes on organic substrates such as fallen logs or humus.

Fruiting body of Unguiculella robergei, copyright Abel Flahaut.

However, in 1962 the British mycologist Richard Dennis noted that Kirchstein's description of Trichangium vinosum bore a close resemblance to another bark-living fungus, Unguiculella robergei, and suggested that the two might be the same species. Unguiculella robergei is itself a very rare fungus, otherwise only known from a handful of records in France and Scotland, seemingly all in the month of April (see MycoDB). It has been recorded from bark and dead twigs of mistletoe and roses, producing dark red, disk- or cup-shaped fruiting bodies less than a millimetre in diameter. These fruiting bodies are covered with small glassy hairs; the hooked shape of these hairs was presumably the inspiration for the genus name meaning a small claw or nail. It is possible, of course, that this fungus is more common than realised: with something this small, you need to be looking for it.

REFERENCE

Dennis, R. W. G. 1962. New or interesting British Helotiales. Kew Bulletin 16 (2): 317–327.

Lumbsch, H. T., & S. M. Huhndorf. 2010. Myconet volume 14. Part One. Outline of Ascomycota—2009. Part Two. Notes on ascomycete systematics. Nos 4751–5113. Fieldiana: Life and Earth Sciences, N.S. 1: 1–64.

Psoraceae

Psora decipiens, copyright Troy McMullin.

Just a very quick one today. The photo above is of a member of the Psoraceae, a group of lichens sometimes referred to as 'fishscale lichens'. As their vernacular name indicates, Psoraceae are characterised by a scaly appearance, together with a preference for growing on soil or rock crevices (Ekman & Blaalid 2011). The scaly appearance also gives the family its botanical name: Psora comes from the Greek for 'itch'.

Psora vallesiaca, copyright Leif Stridvall.

Molecular phylogenetic analyses have supported the inclusion of three genera in the Psoraceae, Psora, Protoblastenia and Brianaria (Ekman & Svensson 2014). The last genus was only described recently to include a group of species previously included in a different genus Micarea belonging to an entirely different lichen family, the Pilocarpaceae. Micarea lichens closely resemble Brianaria species in overall appearance but differ in some features including the nature of their algal symbiont. Past authors often assumed that symbiont associations provided little guidance to lichen relationships; it was thought that a germinating lichen fungus would pretty much form a connection with whatever algal species was available. However, more recent investigations have found that the tastes of lichen fungi are more discriminating. Micarea species form associations with small algal cells, four to seven microns in diameter, with thin cell walls that are often found in pairs within the lichen thallus. Brianaria species, in contrast, have larger algal symbionts that are always isolated in the thallus (Andersen & Ekman 2005).

REFERENCES

Andersen, H. L., & S. Ekman. 2005. Disintegration of the Micareaceae (lichenized Ascomycota): a molecular phylogeny based on mitochondrial rDNA sequences. Mycological Research 109 (1): 21–30.

Ekman, S., & R. Blaalid. 2011. The devil in the details: interactions between the branch-length prior and likelihood model affect node support and branch lengths in the phylogeny of the Psoraceae. Systematic Biology 60 (4): 541–561.

Ekman, S., & M. Svensson. 2014. Brianaria (Psoraceae), a new genus to accomodate the Micarea sylvicola group. Lichenologist 46 (3): 285–294.

Rust, Anyone?

At certain times of year, when the weather is warm, you may see patches of yellow or orange appear on plant leaves. It is often particularly notable on grass. These patches are known as rust and are the fruiting bodies of parasitic fungi. In some cases, they may be merely a nuisance or an eyesore. In other cases, their effects can be devastating. Rust fungi may cause enormous damage to commercial crops. One particularly nasty strain of the stem rust Puccinia graminis that goes by the label of TTKSK or Ug99 has been spreading through Africa and Asia since its discovery in Uganda in 1999, causing up to 100% losses in wheat crops where it hits. A similar strain of the same species was recently involved in outbreaks in southern Europe. And this rust can't just be covered over with a bit of bog.

Stem rust Puccinia graminis uredia on wheat, from the US Dept of Agriculture.

Puccinia is the largest genus of rusts with around 3000 known species (Liu & Hambleton 2010), infecting a wide range of host plants. Many rusts have complicated life cycles...or perhaps that should be 'insane'. Some of you may be aware that, until recently, mycologists (researchers of fungi) maintained a system of dual nomenclature that classified sexual and asexual forms of fungi separately, due to the difficulty in matching one to the other*. Rust fungi can have a life cycle involving a sexually reproducing stage and two different asexually reproducing stages on two different hosts, all of them distinct in appearance, so many rust fungal species could masquerade under no less than three distinct names! But then, some species might have simpler life cycles dropping one or more of the possible stages, and some might restrict their attentions to a single host. The difficulty of wrapping one's head around rust life cycles may perhaps best be conveyed by reproducing one paragraph from the review by Petersen (1974), which I invite you to look upon below in all its hideous hideousness:

*I believe that the botanical code of nomenclature was recently changed to no longer allow this set-up as a formal system, but I presume that it's going to take a long time to work that one through.

A complex system of nomenclature has been developed to quickly indicate the stages found in any particular life cycle in the rusts. While easily understood by students of the group with some experi- ence, the system at first appears bewildering. Those taxa which exhibit all five stages during their life history are called Euforms. They may be Heter-Eu- (infecting more than one host) or Aut-Eu- (occurring on a single host). In some rusts, the aecial stage is deleted, or the aecia and aeciospores are morphologically identical to uredia and uredospores, these organisms being termed Brachy-forms. All these forms are autoecious, thus enabling the "aut-" prefix to be dropped. For those organisms in which spermogonia and spermatia are missing, Maire used Cata- as a prefix, but this usage is rarely seen nowadays. When the uredial stage has been dropped, the organism is called an Opsis-form. This may be used as a prefix, such as Opsis- Gymnosporangium, or more commonly as a suffix, such as Gymno- sporangiopsis. Again, forms can be Heter-Opsis-, or Aut-Opsis-. If this life cycle also deleted spermogonia, it was dubbed Catopsis- by Maire. In more general terminology, rust fungi exhibiting chiefly teliospores (with or without spermogonia) are known as Micro-forms, but Maire again specified those which exhibited both telia and spermogonia as Hypo-forms. In these forms, the teliospores are normal in that they require a resting period before germination. In some taxa, teliospore-like propagules are produced which are lighter in color, exhibit thinner walls, and more obscure germ pores, and which require no resting period before germination, often germinat- ing in situ. These spores have been called leptospores, and the life cycle, otherwise identical to that of Micro-forms, is known as Lepto- form. Occasionally, only uredospores and teliospores are found (these sometimes are thought of as imperfect rusts in which other stages will hopefully be found), and these are called Hemi-forms. Finally, in some taxa the teliospores are cytologically similar to aeciospores, in which case the life cycle is called Endo-, the species with such structures often segregated in the genus Endophyllum.

Life cycle of stem rust Puccinia graminis, from US Dept of Agriculture.

A typical 'full' rust life cycle is the one gone through by stem rust, shown in the diagram above. Stem rust alternates between two hosts, grasses such as wheat (it also infects related species such as barley or rye) and barberry. Sexual reproduction occurs on barberry near the beginning of the growing season when haploid spores known as spermatia or pycniospores are produced from fruiting bodies called spermatogonia or pycnia. In Puccinia species, these spermatogonia are flask-shaped and tend to be evenly spaced across the host tissue; other rust fungi may produce more irregular and irregularly-spaced spermatogonia. At the sides of the flask's opening are protruding hyphae to which spermatia from other spermatogonia fuse. Now, in animals such as ourselves, fusion of sperm and ovum is usually immediately followed by fusion of their respective haploid nuclei to form the diploid daughter nucleus. In rusts, however, the haploid parent cells fuse but their nuclei do not. Instead, the daughter cell grows and divides as a dikaryotic organism with two nuclear lineages remaining associated but distinct in each cell. The dikaryotic mycelium produced from fusion of spermatium and receptive hypha gives rise to a fruiting body known as an aecium which in Puccinia is cup-shaped. The aecium produces its own spores that are shed to infect the alternate host, the grass, to which they gain access through the host's stomata. Germinating aeciospores grow into a mycelium that penetrates host cells, absorbing nutrients directly from the host cytoplasm. When the time comes for the next reproductive stage, the rust produces a compacted layer called a uredinium that gives rise to yet another spore type, urediniospores. Unlike aeciospores that travel from one host to another, urediniospores are able to re-infect the same host, giving rise to a new uredinial stage of the life cycle. This asexual sub-cycle continues indefinitely for as long as growing conditions remain good for the rust. When conditions deteriorate, the rust stops producing urediniospores and begins producing thick-walled teliospores that are able to persist through the cold winter. It is within the teliospores that the dikaryotic nuclei finally fuse, giving rise to daughter nuclei that then themselves undergo meiosis so the teliospore germinates at the beginning of the next season to release haploid basidiospores, that infect a barberry to begin the cycle anew.

Arum rust Puccinia sessilis aecia on leaf of Arum maculatum, copyright Velella.

Because of the need for two hosts in the life cycle, crop pests such as stem rust may potentially be controlled by eradicating the second host. However, first you have to know what to target. Stripe rust Puccinia striiformis is another significant pest of grass crops whose alternate host was not identified as barberry until 2010 (Jin et al. 2010). And in warmer climates where urediniospores can survive all year round, rusts may be able to persist asexually even without a suitable alternate host.

REFERENCES

Jin, Y., L. J. Szabo & M. Carson. 2010. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternative host. Phytopathology 100: 432–435.

Liu, M., & S. Hambleton. 2010. Taxonomic study of stipe rust, Puccinia striiformis sensu lato, based on molecular and morphological evidence. Fungal Biology 114: 881–899.

Petersen, R. H. 1974. The rust fungus life cycle. Botanical Review 40 (4): 453–513.

The Colours of Rot

Bracket fungi Fomitopsis pinicola, copyright Marek Novotnak.

Apart from those species readily purchased at the supermarket, perhaps the macrofungi most likely to be encountered by the average person are the brackets. Bracket fungi are the hard, woody, shelf-like fungi that may be found growing from tree-stumps and fallen logs. Whereas other fungal fruiting bodies may emerge, release their spores, and collapse away within a matter of hours, those produced by bracket fungi (properly known as 'conks', apparently) may persist for years with a new layer of reproductive tissue added each cycle.

Phlebiopsis gigantea, a resupinate member of the Polyporales, copyright Jerzy Opioła.

The majority of brackets belong to the fungal order Polyporales, one of the major subgroups of the basidiomycetes with about 1800 known species (Binder et al. 2013). While brackets may be the most familiar Polyporales, the order is morphologically diverse. Indeed, no one morphological feature characterises the Polyporales as currently recognised; it has only been recognised as a clade following the advent of molecular analyses. Some members of the Polyporales produce persistent fruiting bodies like brackets, others are more ephemeral. They may be sessile and shelf-like, or they may be raised on a stalk. The spore-producing layer may appear as minute pores, as gills, as protruding teeth, or may be entirely smooth. There are also a large number of Polyporales species that are what is known as resupinate: that is, they don't produce discrete fruiting bodies at all. Instead, the reproductive structures are produced as a more or less undifferentiated crust spreading over their substrate.

Hexagonal-pored polypore Polyporus alveolaris, copyright Andreas Kunze.

The greater number of Polyporales are associated with decaying wood; they play an integral role in breaking down and releasing nutrients that might otherwise be locked away from environmental cycles. Most species only grow on wood that is already deceased but there are some that are pathogenic on living trees. Based on the appearance of the wood being broken down, Polyporales may be divided between 'white-rot' and 'brown-rot' species. The difference is not merely an aesthetic one. Wood is made up primarily of two organic polymers, cellulose and lignin. Both these chemicals are difficult to metabolise (we ourselves, for instance, cannot digest either) but lignin is a particularly tough nut to crack. White-rot fungi are able to digest both cellulose and lignin but brown-rot fungi digest the cellulose only. White-rot fungi extract more nutrients from the wood overall but brown-rot fungi extract nutrients faster. And while the efforts of white-rot fungi may result in almost the entire carbon quotient of the wood being released to the environment, brown-rot fungi leave a lignin-rich residue that is largely indigestable by any other organism. Genomes have been sequenced from both white- and brown-rot taxa and a fair amount of effort has been invested into studying the different chemical pathways underlying the different rot types.

Caulifower fungus Sparassis brevipes, copyright AL'S.

Phylogenetically speaking, Justo et al. (2017) recently recognised eighteen families within Polyporales corresponding to well-established molecular clades (plus a handful of taxa that could not yet be confidently placed in a 'family') but these show the same challenges to morphological characterisation as the order as a whole. Many of these families include both fruiting and resupinate taxa, and transitions in fruiting body morphology are the rule more than the exception. Interestingly, one 'morphological' feature that does show a fair degree of phylogenetic consistency is the rot-type. It seems clear that the ancestor of the Polyporales was a white-rot fungus with the majority of brown-rot fungi forming a single clade within the order. Only one known brown-rot fungus genus , Lentiporus, definitely evolved separately from the rest (another genus, Auriporia, may or may not represent a further origin of brown rot). One question that remains to be answered is whether the chemical basis of brown rot in Laetiporus is the same as that in the main brown-rot clade.

Ganoderma pfeifferi, copyright Bloodworm.

Apart from their role in breaking down wood, not too many Polyporales have a direct economic significance. Some, notably the lingzhi Ganoderma lucidum, are grown commercially for use in Chinese medicine. Some species with more fleshy fruiting bodies are edible: notable examples include the cauliflower fungi Sparassis species and the chicken of the woods Laetiporus sulphureus (guess what it's supposed to taste like). According to its Wikipedia page, chicken of the woods may cause a toxic reaction to some diners but there seems to be some question about whether this is due to toxins produced by the fungus itself or whether the fungus is absorbing toxins contained in the wood it is growing from. For other polypores, the question of toxicity may be rendered moot by the fact that any attempt to eat one would break one's teeth.

REFERENCES

Binder, M., A. Justo, R. Riley, A. Salamov, F. Lopez-Giraldez, E. Sjökvist, A. Copeland, B. Foster, H. Sun, E. Larsson, K.-H. Larsson, J. Townsend, I. V. Grigoriev & D. S. Hibbett. 2013. Phylogenetic and phylogenomic overview of the Polyporales. Mycologia 105 (6): 1350–1373.

Justo, A., O. Miettinen, D. Floudas, B. Ortiz-Santana, E. Sjökvist, D. Lindner, K. Nakasone, T. Niemelä, K.-H. Larsson, L. Ryvarden & D. S. Hibbett. 2017. A revised family-level classification of the Polyporales (Basidiomycota). Fungal Biology 121: 798–824.

When the Wolf Breaks Wind

Common puffballs Lycoperdon perlatum, copyright H. Krisp.

In an earlier post, I described the way in which the 'gasteromycetes' of historical fungal classifications have come to be expunged as a category. The enclosure of spore-producing structures within a contained fruiting body such as a puffball, instead of exposed on a membrane such as on the underside of a mushroom cap, is something that has evolved many times in fungal history. One possible suggestion for why this may occur is as a protection against moisture loss, allowing the fungus to thrive in drier or more exposed habitats than before.

In that earlier post, I also mentioned off-hand that one of the best known groups of 'gasteromycetes', the puffballs of the Lycoperdaceae, are in fact close relatives of some of the best known typical mushrooms in the Agaricaceae. Indeed, it appears that recent authors may go so far as to synonymise the two families. Puffballs emerge as globular fruiting bodies that become packed with spores as they mature, until one or more openings develop in the external skin of the fruiting body and allow the pores to escape. Supposedly many puffballs are quite edible if collected before the spores begin to develop, though I've never tried myself. Particularly sought in this regard is the giant puffball Calvatia gigantea whose fruiting bodies grow particularly large; supposedly, examples have been found over a metre in diameter and weighing up to twenty kilogrammes.

Giant puffball Calvatia gigantea, copyright Alan Wolf.

Dispersal of spores from puffballs may be achieved in a number of ways. In species found in habitats with more regular rainfall, such as species of the genus Lycoperdon, spores are spread by 'boleohydrochory' (Gube & Dörfelt 2011). '-Chory' means dispersal, '-hydro-' obviously means water, 'boleo-' I think may mean something like 'throw'. The puffball opens through a hole in the top, and drops of rain (or other sources of pressure such as being tapped by an animal) cause a puff of spores to be squeezed out. The water may then carry the spores away. The name Lycoperdon, as it happens, literally translates as 'wolf fart', and this is another one of those names I am completely at a loss to explain. The 'fart', obviously, refers to the appearance of the spore puffs, but what on earth do they have to do with wolves?

Tumbling puffballs Bovista pila, copyright Dan Molter.

Other puffballs may spread their spores via 'anemochory', dispersal by wind. This is particularly the case with species found in drier habitats. Some species, such as some members of the genus Bovista, exhibit a variation on this called 'geanemochory' in which the entire puffball becomes detached and blown about by the wind, with the spores escaping through openings in the external shell like pepper being shaken from a pepper-pot. Differences in dispersal method between puffball species are generally reflected by differences in their spore morphology. Hydrochorous species usually have strong ornamentation, with the outside of the spore being covered with warts or the like. These warts provide more surface area for the water to catch onto; they may also help prevent the spores from clumping together. In contrast, anemochorous species have spores that are smooth, making them more streamlined for being blown through the air or, particularly in the case of geanemochorous species, making them less likely to become trapped by hyphae or other structures inside the fruiting body itself and so facilitating their escape.

REFERENCE

Gube, M., & H. Dörfelt. 2011. Gasteromycetation in Agaricaceae s. l. (Basidiomycota): morphological and ecological implementations. Feddes Repertorium 122 (5–6): 367–390.

Harden Up, Puffball!

Near my home back in Australia, there's a park where we walk the dog most days. During the summer, when Perth receives little rain, the grass in the park dries off and the ground becomes hard. In some particularly dry spots, ground cover is absent completely (there's a large bare patch that used to house a meat ant colony; the ants died off a few years back but the nest site has never been re-claimed by grass). As autumn approaches, cream-coloured lumps can be seen in these bare patches, pushing their way through cracks in the ground. The lumps eventually crack and split, turning to dust over the course of several weeks. These lumps are Pisolithus puffballs.

Mature Pisolithus 'arhizus' puffballs, copyright Paul Venter.

A long-established system in the classification of basidiomycete fungi (the class of fungi that includes most familiar mushroom-forming species) divided many of the species between two groups, the hymenomycetes and the gasteromycetes. Hymenomycetes (the name means 'membrane fungi') included the classic mushrooms, with spores produced on an exposed membrane on the open fruiting body (often underneath) from which they were expelled when mature. Gasteromycetes ('stomach fungi') were forms such as puffballs in which spore-producing structures were completely enclosed within a sealed fruiting body; these structures would break apart at maturity and only then would the fruiting body open up to release the freed spores. However, while the hymenomycete-gasteromycete division was certainly convenient, it was not entirely watertight. For instance, ink-cap mushrooms were clearly hymenomycetes going by their exposed membranes, but the way their fruiting bodies dissolved to release their spores was more than a little gasteromycete-like. When molecular phylogenetic studies came to be included in the mix, it became clear that the two groups were not phylogenetically distinct. Indeed, the usual poster-children for gasteromycetes, the Lycoperdaceae puffballs, have turned out to be close relatives to the most familiar of all hymenomycetes, the field mushroom Agaricus bisporus. 'Gasteromycetes' have evolved from 'hymenomycete' ancestors on several different occasions; a puffball is basically a mushroom that doesn't open.

When molecular studies came to examine Pisolithus and a number of related 'gasteromycete' taxa, they turned out to be related to the 'hymenomycete' boletes in the order Boletales. Boletes are spongy mushrooms in which the spore-producing section on the underside of the cap is divided into pores rather than gills. Some boletes are highly regarded for their edibility, if you can get to them before other animals and insects that find them equally tasty do (others, however, are toxic, so as always with mushroom-hunting you need to know what you're eating). A new lineage in the Boletales, the Sclerodermatineae, was recognised for Pisolithus and its relatives; this lineage includes some forms that would have been recognised in the past as gasteromycetes and some that would have been called hymenomycetes. As with other members of the Boletales, most if not all members of the Sclerodermatineae are ectomycorrhizal, forming close symbiotic associations with the roots of certain trees. In most cases, these associations are essential to the well-being of both members of the partnership as the two exchange nutrients.

Salmon gum mushroom Phlebopus marginatus, copyright Ian Sutton.

'Hymenomycete' genera of the sclerodermatines include Gyroporus, Boletinellus and Phlebopus. Members of these genera are more or less similar in overall appearance to other boletes, though Boletinellus has thin caps on which the stalk may be displaced to one side rather than central and the pores on the underside are less distinct. Gyroporus boletes may be characterised by features of the stalk, in which the centre has a fluffy section that dissolves over time to leave a hollow core. The fruiting bodies produced by species of Phlebopus can be absolutely massive: weights of up to 30 kg have been recorded for a single mushroom. Boletinellus and Phlebopus (which together form the Boletinellaceae) are remarkable in that their ectomycorrhizae are actually harmful to the trees with which they associate. Hyphae of Boletinellaceae form sheaths or crusts around the roots of trees that are not normally involved in ectomycorrhizal associations (ash in the case of Boletinellus merulioides, various trees such as citrus and coffee in the case of Phlebopus species) that provide a home for aphids or mealybugs. The bugs have a sheltered place to live, and the fungus gains nutrients excreted by the bugs as they feed on the tree roots.

Phylogenetic analyses indicate that the Boletinellaceae are the sister group to other Sclerodermatineae (Wilson et al. 2012) but whether the 'gasteromycete' sclerodermatines are monophyletic to Gyroporus or not is more of an open question. Gasteroid sclerodermatines include the earthballs Scleroderma and the horse dung fungus Pisolithus. Members of these genera have hard, puffball-like fruiting bodies; in the case of Pisolithus, these fruiting bodies are so hard that they may sometimes be seen forcing their way through road asphalt or concrete. Both Scleroderma and Pisolithus have been widely used in inoculating soil for forestry and revegetation, in part because they form ectomycorrhizal associations with a wide variety of tree species. However, more recent studies have suggested that some of this apparent egalitarianism may be due to confusion between cryptic species; individual strains of the two genera may be more host-selective than previously recognised (Watling 2006). Inoculation with the wrong strain might then lead to tree growth not being helped, or even being hindered. Another example of the practical consequences of poor taxonomy!

Barometer earthstars Astraeus hygrometricus, copyright Richard Sullivan.

Similar taxonomic questions surround the barometer earthstars of the genus Astraeus, long recognised as a single cosmopolitan species A. hygrometricus but probably a complex of more localised species. Earthstars have a double-layered covering (peridium) to the fruiting body; the outer layer of the peridium is leathery and splits open when mature into several pointed rays, hence the fungus' vernacular name. A double-layered peridium is also found in the fruiting bodies of another sclerodermatine genus, Calostoma, but in this case the outer layer is gelatinous. The inner layer of the peridium is brightly coloured, and the appearance of the Calostoma fruiting body as the outer layer breaks open has led to the vernacular name of 'prettymouth'.

Mature prettymouth Calostoma cinnabarina, copyright Dan Molter.

Other members of the Sclerodermatineae are less well known. Diplocystis wrightii is a sclerodermatine known from various locations around the Caribbean that produces clusters of small globular fruiting bodies arising from a basal stroma (hyphal mass). As the upper surface of the peridium becomes dry and papery, it splits apart to turn the fruiting body into an open cup. A similar arrangement of clustered, cup-shaped fruiting bodies is known in a fungus species found in Burmese amber, Palaeogaster micromorpha (Poinar et al. 2014), though structural differences argue against a direct relationship between the two. Finally, there are many other unusual 'gasteromycetes' whose affinities remain uncertain; future studies may yet assign further exemplars to the spectrum of sclerodermatine diversity.

Preserved Palaeogaster micromorpha in Burmese amber, from Poinar et al. (2014).

REFERENCES

Poinar, G. O., Jr, D. da Silva Alfredo & I. G. Baseia. 2014. A gasteroid fungus, Palaeogaster micromorpha gen. & sp. nov. (Boletales) in Cretaceous Myanmar amber. Journal of the Botanical Research Institute of Texas 8 (1): 139–143.

Watling, R. 2006. The sclerodermatoid fungi. Mycoscience 47: 18–24.

Wilson, A. W., M. Binder & D. S. Hibbett. 2012. Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytologist 194: 1079–1095.

Sordariomycetidae: Soil Fungi A-Plenty

I'm pretty sure I've commented before that, although most of us tend to associate the word 'fungi' with mushrooms and other eye-catching fruiting bodies, the vast majority of fungal diversity is minute and tends to go unnoticed. Nevertheless, despite their obscurity, many of these microfungi are crucial to our own continued existence. These are the decomposers, the organisms that break down fallen plant matter and animal wastes in their own search for nourishment and so contribute to the release of locked-up nutrients back into the environmental cycle.

Neurospora growing on sugar cane waste, from here.

The group of fungi that I drew for today's post, the Sordariomycetidae, is primarily made up of these minute decomposers. Sordariomycetids have already made an appearance here at Catalogue of Organisms, in a post from ten years ago on black mildews. Depending on how broadly the group is circumscribed, the Diaporthales could also be included. Due to a simple morphology that provides few distinct characters, the Sordariomycetidae are primarily defined on the basis of molecular phylogenies. The difficulty of classifying microfungi by morphology alone is underlined by cases where species previously classified within the same genus have proven to belong to entirely distinct fungal lineages.

In general, the vegetative body of most Sordariomycetidae consists of little more than disassociated hyphae embedded in their substrate, with the only distinct structures being the reproductive fruiting bodies. These are perithecia: that is, globular or flask-shaped fruiting bodies with a single small opening or ostiole at the top through which the mature spores are released. In some cases, the internal structure of the mature perithecium will simply dissolve, freeing the spores to escape through the ostiole in the manner of a miniature puffball. In others, the spores become entangled in a long strand or seta that is then extruded through the ostiole like toothpaste being squeezed out of a tube.

Perithecium of Chaetomium extruding spore-bearing setae, from here.

Sordariomycetids are found in almost every habitat imaginable: as well as soil- and dung-dwelling forms, they may also be found in aquatic and even marine habitats. Perhaps the best-known sordariomycetid is Neurospora crassa, red bread mould, which is widely used in laboratories as a model organism for genetic research. Indeed, it was investigations into N. crassa in the 1950s that first led to the proposal of the 'one gene, one enzyme' model that became a cornerstone of molecular genetics.

What Value a Sporangium?

Regular readers of this site will know that I select the subject of most posts by assigning myself a taxon semi-randomly and then trying to find something to say about it. And sometimes when I spin the wheel, what comes out can be a little obscure. It's time for another entry in "Taxon Names that No-one Uses"!

Colony of Dimargaris cristalligena (Dimargaritaceae), from here.

As far as I can tell, the name 'Meromycetidae' has been used in the literature once, and once only. In 1998, Tom Cavalier-Smith coined it as a label for a subclass of fungi in his "Revised six-kingdom system of life". Even compared to other fungal classifications current at the time, Cavalier-Smith's system for fungi contained a lot of features that seemed a little odd (Laboulbeniales as trichomycetes?) and most of his novel propositions were to subsequently sink without a trace. The 'Meromycetidae' were intended to be a subgroup of what most other authors of the time would have called the 'zygomycetes'. Zygomycetes, as generally recognised, were mostly microscopic fungi that lack the dikaryotic phase* of more familiar macrofungi such as mushrooms, and lack the flagellated spores of other microscopic fungi. The most familiar zygomycetes are various household moulds. It is now well established, however, that 'zygomycetes' are a non-monophyletic grade within fungal evolution, leading to their dissolution as a formal class though one may still encounter the name being used informally for convenience.

*A period in the reproductive life cycle of many fungi where the nuclei from two parents have entered a single cell, but continue to function and divide separately without yet fusing to form a daughter nucleus.

Mature sporangiophore of Syncephalastrum racemosum, showing merosporangia radiating from central vesicle. Copyright George Barron.

It is not always easy to tell how Cavalier-Smith's (1998) taxa were supposed to be applied, but it seems evident that the Meromycetidae were intended to cover those zygomycetes that produced merosporangia. Merosporangia are elongate sporangia that may contain one to several asexually-produced spores in series. In a review of fungi with merosporangia, Benjamin (1966) identified four groups that might be described as possessing such structures: Syncephalastrum, Piptocephalidaceae, Kickxellaceae and Dimargaritaceae. Syncephalastrum and the Kickxellaceae are minute soil saprobes; the Piptocephalidaceae and Dimargaritaceae are parasites of other fungi, mostly of other zygomycetes. However, Bejamin noted that the differences between these groups were such that only the Kickxellaceae and Dimargaritaceae could be considered as likely to be related to each other. The others differed in features of their hyphal structure, and also in details of how their merosporangia developed. More recent molecular studies have sided with Benjamin rather than with Cavalier-Smith: the production of a merosporangium does not tally with a single ancestry, and the various merosporangium-producing fungi can be placed in quite distinct lineages.

Young sporangiophore of Syncephalis nodosa, a representative of the Piptocephalidaceae. Copyright George Barron.

Syncephalastrum, for instance, belongs to the Mucorales, in the same fungal order as the house moulds Mucor and Rhizopus. This tallies with the observation by Benjamin that, but for its unusual sporangia, Syncephalastrum could be considered a fairly typical member of that group. The Piptocephalidaceae belong to the Zoopagales, other members of which are also parasites or predators, attacking minute animals such as nematodes or protozoa such as amoebae.

Comparative diagrams of sporangiophores of Coemansia (Kickxellaceae) and Smittium (Harpellales), showing similarities in overall structure, from Moss & Young (1978).

The Kickxellaceae and Dimargaritaceae together belong to a recently recognised fungal group dubbed the Kickxellomycotina, all members of which share a hyphal structure that is unique among fungi. Whereas other 'zygomycetes' have the hyphae more or less coenocytic (without regular division into cells), Kickxellomycotina have the hyphae divided by regular septa. The septa each contain a disciform pore that is sealed by a lenticular plug. This group also includes two other orders of fungi, the Harpellales and Asellariales, that have been referred to in the past as the trichomycetes. Members of these two orders are symbionts in the guts of arthropods, usually in aquatic or damp habitats. Their reproductive structures are very similar to those of Kickxellaceae, with single-spored sporangia developing as side branches of a septate sporangiophore. Indeed, if Kickxellaceae are to be described as producing merosporangia, then Harpellales and Asellariales should as well. Molecular phylogenetic analyses also support a close relationship between these three groups to the exclusion of the more distinctive Dimargaritaceae (Tretter et al. 2014).

Diagrams of sporangiophores and merosporangia of Dimargaris arida (Dimargaritaceae), from here.

The higher relationships of the various 'zygomycete' subgroups are still being investigated. It is fairly well established at this point that no close relationship exists between Syncephalastrum in the Mucorales and the other merosporangial fungi. A number of analyses, on the other hand, have suggested some sort of relationship between the Kickxellomycotina and the Zoopagales, but so far only with low support. Because the organisms involved are so derived, and have possible undergone fairly rapid rates of evolution, mycologists have been reluctant to read too much into these analyses, and new hypotheses may be yet to come.

REFERENCES

Benjamin, R. K. 1966. The merosporangium. Mycologia 58 (1): 1–42.

Cavalier-Smith, T. 1998. A revised six-kingdom system of life. Biological Reviews 73: 203–208.

Tretter, E. D., E. M. Johnson, G. L. Benny, R. W. Lichtwardt, Y. Wang, P. Kandel, S. J. Novak, J. F. Smith & M. M. White. 2014. An eight-gene molecular phylogeny of the Kickxellomycotina, including the first phylogenetic placement of Asellariales. Mycologia 106 (5): 912–935.

The Pseudoperisporiaceae: Fungi on Leaves, Fungi on Fungi

Leaves of savin juniper Juniperus sabina, with fruiting bodies of the pseudoperisporiaceous fungus Chaetoscutula juniperi visible as black spots, from Tian et al. (2014). Scale bar = 1 mm.

As has been noted on this site before, the world of microscopic fungi includes a bewildering array of species that may never come to your attention but are in fact all around you. These organisms quietly live out their lives, often serving to break down the refuse that larger organisms such as plants shed over the course of their lives. Sometimes they are not so patient, instead attacking the plant while it is still green and growing. The subjects of today's post, the Pseudoperisporiaceae, include examples of both.

The Pseudoperisporiaceae are a widespread group of minute fungi that are most diverse in the tropical parts of the world. Because of their small size and lack (so far as is known) of significant economic effects, they are rarely noticed and little studied. However, they are by no means rare; in fact, one species in the family, Raciborskiomyces longisetosum, has been shown by molecular studies to be a major component of the soil community (e.g. Valinsky et al. 2002). The majority of members of the family grow on the leaves of plants, either as saprobes on leaf litter or as parasites on live plants. Alternatively, they may be parasites of other fungi, particularly sooty moulds. The more or less globular fruiting bodies (which are at most about 200 µm in size) are superficial on the surface of the host substrate, and are surrounded by a brown mycelium (mass of vegetative strands). Other distinctive features of the family include fusoid-ellipsoid ascospores (i.e. sexually produced reproductive spores) that are minutely warty and have rounded, subacute ends (Tian et al. 2014).

Closer view of fruiting body of Wentiomyces, from Wilk et al. (2014). Note the ostiole towards the lower left, surrounded by bilobed setae. Scale bar = 20 µm.

Pseudoperisporiaceae belong to the class of fungi known as the Dothideomycetes, a major subdivision of the Ascomycetes. Dothideomycetes include the majority of what used to be called the loculoascomycetes, so-called because of the way their fruiting bodies grow. A distinctive hollow, or locule, forms in the vegetative mycelium of the parent fungus, and the fruiting body develops within this hollow. In most Dothideomycetes (including the Pseudoperisporiaceae), the resulting fruiting body is almost entirely closed with a single opening (the ostiole) at the top through which the spores are released. Pseudoperisporiaceae also resemble other Dothideomycetes in having fissitunicate asci: that is, the asci (which are finger-shaped structures inside the fruiting body in which spores are formed) have a double-layered wall, with the outer layer being more rigid than the inner. As the inner layer swells with moisture, it causes the outer layer to split and the spores end up being expelled from the end of the ascus. Dothideomycetes are not the only fungi to show locular development, hence the dropping of loculoascomycetes as a formal group; the Chaetothyriomycetidae also grow their fruiting bodies from locules (Hyde et al. 2013).

The exact relationships of the Pseudoperisporiaceae with other Dothideomycetes remain uncertain; in their review of dothideomycete families, Hyde et al. (2013) left Pseudoperisporiaceae unassigned to an order within the class. Indeed, it is unclear to what extent Pseudoperisporiaceae are even related to themselves. Few members of the family have been studied from a molecular perspective, and those few that have been have not come out in the same place in the dothideomycete family tree. At least one supposed member of the family, the genus Epibryon, turns out not to even be a dothideomycete but is instead a chaetothyriomycete (Stenroos et al. 2010). Not for the first time on this site, I find that a seemingly simple outer morphology may be disguising a much greater diversity.

REFERENCES

Hyde, K. D., E. B. G. Jones, J.-K. Liu, H. Ariyawansa, E. Boehm, S. Boonmee, U. Braun, P. Chomnunti, P. W. Crous, D.-Q. Dai, P. Diederich, A. Dissanayake, M. Doilom, F. Doveri, S. Hongsanan, R. Jayawardena, J. D. Lawrey, Y.-M. Li, Y.-X. Liu, R. Lücking, J. Monkai, L. Muggia, M. P. Nelsen, K.-L. Pang, R. Phookamsak, I. C. Senanayake, C. A. Shearer, S. Suetrong, K. Tanaka, K. M. Thambugala, N. N. Wijayawardene, S. Wikee, H.-X. Wu, Y. Zhang, B. Aguirre-Hudson, S. A. Alias, A. Aptroot, A. H. Bahkali, J. L. Bezerra, D. J. Bhat, E. Camporesi, E. Chukeatirote, C. Gueidan, D. L. Hawksworth, K. Hirayama, S. De Hoog, J.-C. Kang, K. Knudsen, W.-J. Li, X.-H. Li, Z.-Y. Liu, A. Mapook, E. H. C. McKenzie, A. N. Miller, P. E. Mortimer, A. J. L. Phillips, H. A. Raja, C. Scheuer, F. Schumm, J. E. Taylor, Q. Tian, S. Tibpromma, D. N. Wanasinghe, Y. Wang, J.-C. Xu, S. Yacharoen, J.-Y. Yan & M. Zhang. 2013. Families of Dothideomyctes. Fungal Diversity 63: 1–313.

Stenroos, S., T. Laukka, S. Huhtinen, P. Döbbeler, L. Myllys, K. Syrjänen & Jaakko Hyvönen. 2010. Multiple origins of symbioses between ascomycetes and bryophytes suggested by a five-gene phylogeny. Cladistics 26: 281–300.

Tian, Q., P. Chomnunti, J. D. Bhat, S. A. Alias, P. E. Mortimer & K. D. Hyde. 2014. Towards a natural classification of Dothideomycetes 5: The genera Ascostratum, Chaetoscutula, Ceratocarpia, Cystocoleus, and Colensoniella (Dothideomycetes incertae sedis). Phytotaxa 176 (1): 42–54.

Valinsky, L., G. Della Vedova, T. Jiang, & J. Borneman. 2002. Oligonucleotide fingerprinting of rRNA genes for analysis of fungal community composition. Applied and Environmental Microbiology 68 (12): 5999–6004.

Wilk, M., J. Pawłowska & M. Wrzosek. 2014. Wentiomyces sp. from plant litter on poor fen in northeastern Poland. Acta Mycologica 49 (2): 237–247.

In a Pichia

Culture of Pichia membranifaciens, from Tomas Linder.

In my previous post, I alluded to the revolutionary effect that DNA analysis had on the classification of bacteria. A similar thing happened for the study of yeasts. Previously, the taxonomy of yeasts (i.e. unicellular fungi) had suffered for the same reasons as bacterial taxonomy: a dearth of usable morphological features combined with uncertainty about the significance or otherwise of metabolic variations. With the availability of genetic information, the relations between yeast taxa became far easier to ascertain.

Needless to say, this lead to a significant shake-up in our understanding of individual yeast taxa. One of the harder-hit taxa was the genus Pichia, previously recognised as a large genus of close to 100 species. Molecular phylogenetic analyses showed that the various species of Pichia were widely scattered within the Saccharomycotina, a fungal clade that includes a large number of yeast species (including such familiar taxa as the brewer's or baker's yeast Saccharomyces cerevisiae). This probably did not come as a huge shock: part of the reason for Pichia's size was that it had not been very stringently defined. Members of this genus were characterised by multilateral budding (that is, buds could develop anywhere along the side of the yeast cell) on a narrow base. They could produce hyphae and/or pseudohyphae (except when they didn't), they might ferment sugars (except when they couldn't), and nitrate might be used as their sole source of nitrogen (except when it wasn't). Pichia spores might be hat-shaped, hemispheroidal or spherical, and they might or might not have a ledge or rim around the equator (Kurtzman 2011).

All of which adds up to a genus that probably tended to be defined as 'the genus that includes any yeast not belonging to these other genera'. In other words, the classic concept of a wastebasket taxon. As a result, the genus has been progressively pared down to a smaller array of species concentrated around the type, Pichia membranifaciens. This is a yeast commonly found as a spoilage organism on foods such as fruit or cheese. Among its other sins, it may grow as a film in the surface of wine, giving the wine an off taste. However, it's not all bad news: recently, P. membranifaciens has been studied as a potential biocontrol agent as it may produce a toxin that has an inhibitory effect on other contaminating fungi (Santos et al. 2009).

A growing culture of Komagataella pastoris, from here.

Somewhat unfortunately, one of the species to be expelled from Pichia is perhaps the best-studied: the yeast formerly known as Pichia pastoris (now supposed to be referred to as Komagataella pastoris though a quick Google Scholar search suggests that a great many authors are pretending that hasn't happened). This species can be grown using methanol as a sole carbon source, and protocols were developed in the 1970s for growing it in high densities at an industrial scale. The original plan was for it to be used for high-protein stock-feed using methanol produced as a by-product of oil refining (the modern agricultural industry has been described as the process of turning oil into food; this would have been a somewhat literal example). Rising oil prices rendered this proposal economically inviable but the P. pastoris industry was to have a reprieve, as the culture method was adopted as a means of producing active proteins (Cereghino & Cregg 2000). Procedures were developed for inserting foreign genes into the yeast, with the resulting pure methanol-based culture allowing the target protein to be generated at a greater rate and higher purity than might be possibly with a culture of the original source organism. Enzymes for laboratory studies, vaccines, medical products such as insulin: whatsitsname pastoris has been used in the production of them all.

REFERENCES

Cereghino, J. L., & J. M. Cregg. 2000. Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiology Reviews 24: 45–66.

Kurtzman, C. P. 2011. Phylogeny of the ascomycetous yeasts and the renaming of Pichia anomala to Wickerhamomyces anomalus. Antonie van Leeuwenhoek 99: 13–23.

Santos, A., M. San Mauro, E. Bravo & D. Marquina. 2009. PMKT2, a new killer toxin from Pichia membranifaciens, and its promising biotechnological properties for control of the spoilage yeast Brettanomyces bruxellensis. Microbiology 155: 624–634.

Black Yeasts, Black Lichens and Rotting Wood: the Chaetothyriomycetidae

Pyrenula cruenta, copyright Gary Perlmutter.

There is no denying that the advent of molecular phylogenetic analysis has been a boon for fungal systematics. It has allowed a much greater resolution of relationships than was previously possible (especially for comparisons between asexually- and sexually-reproducing fungi), and has even lead to the identification of a number of major lineages that probably could have never been recognised from morphological data alone. One such lineage is the Chaetothyriomycetidae, whose members vary from lichens on tropical tree trunks, to saprobes living in the deep sea, to pathogens in the brains of humans.

The Chaetothyriomycetidae (or Chaetothyriomycetes in many older references: the botanical code goes rather all out in the rather irritating practice of changing the endings of names to indicate arbitrary taxonomic ranks) has been divided by Gueidan et al. (2014) into four major lineages. Two of these, the Pyrenulales and Verrucariaceae, are mostly comprised of lichens. Lichenised fungi in the Pyrenulales associate with green algae of the family Trentopohliaceae (which, despite being 'green algae', are generally orange in colour), and are most commonly found on tree bark in tropical forests. Only one lichenised genus, Strigula, is also found growing on leaves; non-lichenised Pyrenulales are found on bark, leaves or wood (Geiser et al. 2006).

Verrucaria maura on coastal rocks, copyright A. J. Silverside.

The Verrucariaceae, in contrast, associate with different symbiotic algae, and prefer to grow on rocks. Lichens of this family are often blackish; their hyphae are darkened by a melanin-like compound which allows them to tolerate quite exposed conditions. Certain species are particularly prominent around the marine shoreline. Gueidan et al. (2014) also identified a small as-yet-unnamed lineage close to Verrucariaceae including rock-dwelling and moss-associated non-lichenised fungi, but support for this grouping requires further testing.

Another somewhat novel lineage identified by Gueidan et al. (2014) was the Celotheliaceae. The type genus, Celothelium, is a lichenised fungus that associates with the alga Trentepohlia in the manner of Pyrenulaceae. Other members of the Celotheliaceae, however, are quite different in ecology, being mostly pathogens of woody plants. Phaeomoniella chlamydospora is a causative agent of grapevine trunk disease, resulting in conditions such as esca, and the rather ominously named 'black goo decline' (so-called because the stems become filled with 'black goo', as the xylem vessels become clogged with fungal hyphae). Dolabra nepheliae causes canker in lychee and rambutan trees. These pathogenic taxa are commonly largely anamorphic (that is, they produce asexual reproductive structures).

Culture of black yeast Exophiala dermatitidis, from here.

The last and most diverse lineage (so far as we know, anyway) is the Chaetothyriales. Like the Verrucariaceae, the Chaetothyriales have melanised hyphae and often grow on exposed substrates such as rocks. Indeed, molecular analyses have supported a closer relationship between Verrucariaceae and Chaetothyriales than the other major lineages. However, members of the Chaetothyriales are not lichenised. Many are saprobic; others, such as the Chaetothyriaceae, grow on plant leaves but in many cases it is unclear whether they are saprobic or parasitic. The mostly saprobic family Herpotrichiellaceae also includes a number of asexually-reproducing forms that grow as yeasts and are opportunistic pathogens, including in humans. Infections by black yeasts (Exophiala) are most commonly cutaneous and relatively superficial, but they can also cause severe and life-threatening infections of deeper organ systems. These infections are most common in patients with pre-existing conditions affecting the immune system, but at least one species, E. dermatitidis, has been recorded causing fatal brain infections in otherwise healthy individuals.

And I referred at the beginning of this post to the deep sea? Well, the Chaetothyriomycetidae samples from there are, I believe, yet to be described. It is possible that this diverse group of fungi still has surprises for us.

REFERENCES

Geiser, D. M., C. Gueidan, J. Miadlikowska, F. Lutzoni, F. Kauff, V. Hofstetter, E. Fraker, C. L. Schoch, L. Tibell, W. A. Untereiner & A. Aptroot. 2006. Eurotiomycetes: Eurotiomycetidae and Chaetothyriomycetidae. Mycologia 98 (6): 1053-1064.

Gueidan, C., A. Aptroot, M. E. da Silva Cáceres, H. Badali & S. Stenroos. 2014. A reappraisal of orders and families within the subclass Chaetothyriomycetidae (Eurotiomycetes, Ascomycota). Mycol. Progress 13: 1027-1039.

The Naked Ascus

Hyphae with poorly-differentiated fruiting bodies of Gymnascella marismortui, from Buchalo et al. (1998).

Three years ago, Christopher and I visited my aunt in Jordan. We spent a week visiting various parts of the country (Petra is amazing), including that most touristy of all activities, swimming in the Dead Sea. Except 'swimming' is not really the right word for what you do in the Dead Sea: with the salt content of the water and hence your own buoyancy so high, normal swimming movements are practically impossible. You can't do much more than bob along on your back*. Standing back up again is equally disconcerting: the extra force required to push your legs back down through the water is such that it is quite startling to discover that the bottom is only about two feet below you. The water has a not-particularly-pleasant greasy feel to it, and at one point I had a drop of it splash onto my lower lip. To my surprise, I could not really describe the taste of that drop as salty. Rather, I would say that what the Dead Sea tastes of is Pain.

*But not too far. One bather had a congregation of guards on the shore suddenly begin yelling at her, evidently because she was swimming too far out and was about to inadvertently invade Israel.

It's hard to believe that anything could live in such conditions, but there is life there. Salt-loving prokaryotes and unicellular dense algae can sometimes form dense blooms, and in 1998 Buchalo et al. described the filamentous fungus Gymnascella marismortui, grown from spores collected in Dead Sea water. Fungal hyphae where observed growing on wood in the Dead Sea in spots where its saltiness had been diluted, such as by the inflow of freshwater springs or rain. Gymnascella marismortui may play a significant role in breaking down wood or other plant material that has been washed into the Sea.

Reproductive structures of Kraurogymnocarpa lenticulospora, from Udagawa & Uchiyama (1999).

Gymnascella marismortui is just one species in a family of microscopic fungi known as the Gymnoascaceae. The prefix gymno- in the name means 'naked', and refers to the fact that these fungi do not have the asci (spore-packets) surrounded by a strongly differentiated fruiting-body wall. Instead, the asci are surrounded by a cluster of hyphae that are little differentiated from the remainder of the fungus, or that form a net-like arrangement called a reticuloperidium (an example of the latter can be seen in the lower left of the figure above). Greif & Currah (2003) suggested that the reticuloperidium may be an adaptation to dispersal by insects, as they became caught on the hairs of flies and were then split open to release the spores when the fly was grooming itself. The ascospores themselves are oblate in shape, with polar depressions or equatorial thickenings. Gymnoascaceae are found in such habitats as soil, rotting vegetation or dung, where they break down substances such as cellulose and keratin (Stchigel & Guarro 2007).

Apart from their largely unsung role as decomposers, Gymnoascaceae have little economic impact on humans. They are relatives of the fungi that cause ringworm and tinea (indeed, these fungi have been included in the Gymnoascaceae in the past), and there have been occasional reports of Gymnoascaceae causing similar infections. However, these infections were probably just incidental: after all, to a fungus, keratin is keratin.

REFERENCES

Buchalo, A. S., E. Nevo, S. P. Wasser, A. Oren & H. P. Molitoris. 1998. Fungal life in the extremely hypersaline water of the Dead Sea: first records. Proceedings of the Royal Society of London Series B 265: 1461-1465.

Greif, M. D., & R. S. Currah. 2003. A functional interpretation of the role of the reticuloperidium in whole-ascoma dispersal by arthropods. Mycological Research 107 (1): 77-81.

Stchigel, A. M., & J. Guarro. 2007. A reassessment of cleistothecia as a taxonomic character. Mycological Research 111 (9): 1100-1115.

Udagawa, S., & S. Uchiyama. 1999. Taxonomic studies on new or critical fungi of non-pathogenic Onygenales 1. Mycoscience 40: 277-290.

This Post Contains Smut

And here's some of that smut, right in your face:

Specimens of the grass Briza minor infected with the smut Jamesdicksonia brizae, from Roger Shivas.

Smuts are a form of plant-parasite fungus that produce large numbers of dusty spores from sori that rupture from the host-plant tissue. The majority of smuts belong to the basidiomycetes clade Ustilaginomycotina (making them distant relatives of the familiar mushroom). The focus of today's post will be the smut order Georgefischeriales, the vast majority of which are parasites of the vegetative tissue of grasses (Bauer et al. 2001). The exceptions include species of the genus Georgefischeria that parasitise species of the plant family Convolvulaceae (the morning-glories) and a small number of species that parasitise sedges. The species Gjaerumia ossifragi parasitises the bog-asphodel Narthecium ossifragum (Bauer et al. 2005). Members of the Georgefischeriales are distinguished from other smuts in that the septa dividing cells within mature sori lack pores. Members of one georgefischerialean family, the Gjaerumiaceae, have septal pores in young hyphae, but by the time they reach maturity the pores have closed over (Bauer et al. 2005). Like other smuts, Georgefischeriales have a life-cycle that alternates between a parasitic and a non-parasitic, saprobic stage, as summarised in this diagram from Bauer et al. (2001):

If a number of the terms on that diagram don't mean much to you: don't worry, you are not alone. The first thing to understand is that, compared to us, fungi kind of do sexual reproduction in reverse. For most of our life-cycle, we are diploid, with two complementary sets of chromosomes in each cell. When we produce sex cells (eggs and sperm), the number of chromosome sets in the cell is reduced to one, making the cell haploid, so that when egg and sperm fuse the resulting offspring is back to being diploid. Fungi resemble us in having two haploid cells fuse into a diploid offspring, but differ in that they then separate the chromosome sets again to produce separate haploid cells. Fungi are therefore haploid rather than diploid for most of their life-cycle. In the diagram above, it is the non-parasitic stage that is the haploid stage.

The parasitic stage of a smut's life-cycle comes about through the fusion of two haploid non-parasitic cells. However, even though the cells fuse, the nuclei in those cells don't. Instead, they form what is called a dikaryon, a chimaeric organism in which each cell contains two separate genomes in separate nuclei. Many fungi have lifestyles featuring dikarya: mushrooms, for instance, are also dikaryotic. The separate nuclei don't actually fuse until they form the reproductive structures, the basidia. In smuts, these basidia become thick-walled and separate from the parent sorus to produce the dispersal structures, the teliospores. The haploid basidiospores that come from the teliospores are what grow into the next non-parasitic generation.

Sori of Gjaerumia ossifragi on Narthecium, from here.

In three of the four families of Georgefischeriales (Georgefischeriaceae, Tilletiariaceae and Gjaerumiaceae), the saprobic stage of the life cycle grows into filamentous hyphae, but the fourth family, the Eballistraceae (containing the single genus Eballistra), produces a budding yeast as its non-parasitic stage instead. Eballistra also differs from other Georgefischeriales in that it does not produce ballistic spores that are flung from the parent sorus, relying instead on more passive dispersal. Eballistra does resemble Georgefischeriaceae and Gjaerumia in producing holobasidia, basidia that are not subdivided by septa. The Tilletariaceae are distinct in that they produce internally-divided phragmobasidia. Tilletiariaceae include three genera: Tilletiaria have spiny spores while those of Phragmotaenium and Tolysporella are smooth. It is worth noting that Tilletiaria is currently known only from laboratory culture and has not been identified in the wild, but it is expected to be a grass parasite like other Tilletiariaceae. Tolysporella produces teliospores that are clustered into spore-balls; those of Phragmotaenium are released individually. In the Georgefischeriaceae, two genera are distinguished by host range and appearance: Georgefischeria produces light-coloured sori on Convolvulaceae while Jamesdicksonia produces dark sori on grasses.

REFERENCES

Bauer, R., D. Begerow, F. Oberwinkler, M. Piepenbring & M. L. Berbee. 2001. Ustilaginomycetes. In: McLaughlin, D. J., E. G. McLaughlin & P. A. Lemke (eds) The Mycota vol. 7. Systematics and Evolution, part B, pp. 57-83. Springer-Verlag: Berlin.

Bauer, R., M. Lutz & F. Oberwinkler. 2005. Gjaerumia, a new genus in the Georgefischeriales (Ustilaginomycetes). Mycological Research 109 (11): 1250-1258.

Prototaxites Revisited

Reconstruction of Prototaxites by Richard Bizley, used with permission.

Richard Bizley has been kind enough to allow me to reproduce the above painting, which he produced in response to the discussion arising from an earlier post at this site. It shows a 'forest' (for want of a better word) of the enigmatic Silurian-Devonian organism Prototaxites reconstructed as a giant fungus. Richard has asked if anyone has any comments to make on the final product. Is this environment plausible? Could Prototaxites have grown in clusters like this, or would nutrient restrictions been such as to prevent such large organisms from persisting in close proximity to each other?

Since I produced my earlier post on the possible re-interpretation of Prototaxites as representing rolled ground-cover mats (Graham et al. 2010a), the proposal has been criticised in print by Boyce and Hotton (2010) and Taylor et al. (2010), and defended by Graham et al. (2010b). Boyce and Hotton regard it as taphonomically implausible that such rolls could form, while Taylor et al. also point out that the major tubes making up Prototaxites are arranged longitudinally down the 'trunk', not radiating outwards. Graham et al. have pointed out how they feel this is not incompatible with their liverwort mat hypothesis.

Colour-enhanced cross-section of Prototaxites specimen, from Graham et al. (2010b). Note that the 'growth rings' are not regularly concentric.

Prototaxites, it should be pointed out, was just one of a number of Silurian-Devonian organisms called nematophytes. Nematophytes are united by their similar internal structure, composed of hypha-like tubes. However, other nematophytes did not have the gigantic columnar form of Prototaxites: Nematothallus, for instance, was an encrusting lichen-like form, while Nematasketum fossils are only a couple of centimetres in size. Edwards and Axe (2012) have recently published a study on Nematasketum and supported comparisons between nematophytes and fungi. In particular, they compare Nematasketum to root-like anchoring and foraging structures called rhizomorphs produced by some large modern basidiomycetes. Hillier et al. (2008) nominated Prototaxites as potentially connected to root-like casts found in the Anglo-Welsh Old Red Sandstone, but admitted that the grounds for connection were slight.

REFERENCES

Boyce, C. K., & C. L. Hotton. 2010. Prototaxites was not a taphonomic artifact. American Journal of Botany 97 (7): 1073.

Edwards, D., & L. Axe. 2012. Evidence for a fungal affinity for Nematasketum, a close ally of Prototaxites. Botanical Journal of the Linnean Society 168: 1-18.

Graham, L. E., M. E. Cook, D. T. Hanson, K. B. Pigg & J. M. Graham. 2010a. Structural, physiological, and stable carbon isotopic evidence that the enigmatic Paleozoic fossil Prototaxites formed from rolled liverwort mats. American Journal of Botany 97 (2): 268-275.

Graham, L. E., M. E. Cook, D. T. Hanson, K. B. Pigg & J. M. Graham. 2010b. Rolled liverwort mats explain major Prototaxites features: response to commentaries. American Journal of Botany 97 (7): 1079-1086.

Hillier, R. D., D. Edwards & L. B. Morrissey. 2008. Sedimentological evidence for rooting structures in the Early Devonian Anglo-Welsh Basin (UK), with speculation on their producers. Palaeogeography, Palaeoclimatology, Palaeoecology 270 (3-4): 366-380.

Taylor, T. N., E. L. Taylor, A.-L. Decombeix, A. Schwendemann, R. Serbet, I. Escapa & M. Krings. 2010. The enigmatic Devonian fossil Prototaxites is not a rolled-up liverwort mat: comment on the paper by Graham et al. (AJB 97: 268–275). American Journal of Botany 97 (7): 1074-1078.