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.

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.

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.

Saddling the Truffles

The black elfin saddle Helvella lacunosa, photographed by Fred Stevens.

The subject of today's post is the fungus family Helvellaceae. In the past, the Helvellaceae have been treated as the family including the morels and false morels. False morels and morels are ascomycetes* that produce convoluted fruiting bodies generally supported above ground by a stalk. However, molecular analyses have unanimously indicated the non-monophyly of the morels and false morels relative to the truffles (Percudani et al. 1999), which produce their fruiting bodies underground (while above-ground fungi have their spores generally dispersed by the wind, truffles have spores dispersed by passing through an animal's digestive system after it eats the truffle). The intermingled relationship between truffles and morels had already been indicated by morphologists based on microscopic features of the spores and asci, and so past members of the Helvellaceae have been dispersed among multiple families. At the same time, genera of truffles have been shown to have a relationship with the Helvellaceae, so of the five genera listed in Helvellaceae in the most recent "Outline of Ascomycota" (Lumbsch & Huhndorf 2007) only two (Helvella and Cidaris) are above-ground fruiters, while the other three (Balsamia, Barssia and Picoa) are truffles. This is ignoring the point that the single known species of Cidaris has not seemingly been identified since its original description (Underwood 1896) and its relationship to Helvella would probably require investigation.

*One of the major groups of fungi, ascomycetes produce spores in an ascus, an elongate structure with spores contained in a row within it.

A stem-less Helvella, H. astieri, photographed by Thomas Læssøe.

Members of the genus Helvella are commonly known as 'saddle fungi' or 'elfin saddles' due to the appearance of the fruiting bodies in some species. Other species possess a variety of different fruiting morphologies, some cup-like, some irregularly folded and lumpy. Not all Helvella species produce fruiting bodies supported by a stalk: in some, the fruiting body sits on the ground or remains partially submerged (Kimbrough et al. 1996), and it has been suggested that such forms may provide some indication how the truffles evolved from above-ground forms. All Helvella species fruit on soil (i.e. never on rotting wood or other such substrates) and it seems likely that all members of the Helvellaceae form ectomycorrhizal associations with plant roots (Hansen 2006).

How to spot desert truffles... (from here)

The truffle members of the Helvellaceae have a solid gleba (the spore-bearing inner mass) interspersed with veins or pockets of hymenia (the spore-producing tissues) separated by sterile tissue (Kimbrough et al. 1996). Picoa species grow in association with Helianthemum (rockrose) species and are among the 'desert truffles' collected in arid parts of the Mediterranean. They are eaten, but are not considered commercially significant due to their small size. Among Helvella species, the white saddle Helvella crispa and black saddle Helvella lacunosa have been described as edible, so long as they are cooked properly.

What the picture above may lead you to... Picoa juniperi, from here.

REFERENCES

Hansen, K. 2006. Systematics of the Pezizomycetes—the operculate discomycetes. Mycologia 98 (6): 1029-1040.

Kimbrough, J. W., L.-T. Li & C.-G. Wu. 1996. Ultrastructural evidence for the placement of the truffle Barssia in the Helvellaceae (Pezizales). Mycologia 88 (1): 38-46.

Lumbsch, H. T., & S. M. Huhndorf (eds) 2007. Outline of Ascomycota—2007. Myconet 13: 1-58.

Percudani, R., A. Trevisi, A. Zambonelli & S. Ottonello. 1999. Molecular phylogeny of truffles (Pezizales: Terfeziaceae, Tuberaceae) derived from nuclear rDNA sequence analysis. Molecular Phylogenetics and Evolution 13 (1): 169-180.

Underwood, L. M. 1896. On the distribution of the North American Helvellales. Minnesota Botanical Studies Bulletin 9 (8): 483-500.

Learning to Like Lichen

The lichen Parmelia saxatilis. The red cups at the top of the photo are the lichen's fruiting bodies (apothecia) that produce fungal spores. Photo from here.

We all know what lichens are. They're the standard example of a mutualistic association that we were all presented with in high school, an association of fungus and unicellular alga allowing both to survive long-term in situations that would normally be fatal for them both. More than 15,000 species of lichen have been described—or, rather, species of lichenised fungi, as names applied to lichens technically apply to the fungal member of the association (only a relatively small number of algae form lichen associations). Though these species can all be attributed to the Ascomycetes among the main fungal subdivisions*, they do not form a single clade within the asomycetes. Instead, it appears that the lichen lifestyle has been gained and/or lost on numerous occasions.

*Lichen-like associations are sometimes formed by other fungi such as Basidiomycetes but they lack the integrity of the ascomycetous examples. Lab workers have even been able to induce lichen-like associations between unicellular algae and colonial or hyphal bacteria such as myxobacteria and streptomycetes (Ahmadjian 1965).

Parmelia is a genus of foliose lichens which is found worldwide but has its highest diversity in Asia (Molina et al. 2004). Well over 1000 species have been assigned to the genus over the years but many (though not all) recent authors have tended towards a much more restricted circumscription of about forty species. True Parmelia, in this sense, is distinguished from other genera in the lichen family Parmeliaceae by its linear pseudocyphellae (pore-like structures in the upper-surface of the lichen's cortex) and its particularly small spores and conidia (conidia are reproductive structures like spores but produced asexually rather than sexually) (Elix 1993). ITS rDNA phylogeny is mostly consistent with many of the proposed segregate genera, including the restricted Parmelia, though it provides little information on their higher relationships (Crespo & Cubero 1998).


Another view of Parmelia saxatilis. As well as the spore-producing apothecium, this photo also shows numerous isidia, the small finger-like protrusions covering the thallus. Containing both fungal and algal cells, the isidia can break off to form new lichens. Photo by Stephen Sharnoff.

Parmelia achieves its highest diversity in temperate or boreal regions. The type species, P. saxatilis, is one of the world's most widespread lichen species, found in both the Arctic and the Antarctic, as well as cooler localities in between (Molina et al. 2004). Lichens can reproduce in one of two ways: small pieces of the thallus containing both algal cells and fungal hyphae may break off to grow directly into a new thallus elsewhere, or the lichen can release spores and/or conidia in the manner of other fungi. A germinating lichen spore will grow extremely slowly: even in laboratory cultures on agar, some lichen fungi will only reach a diameter of 1 mm within the course of a year when grown without algal symbionts(Ahmadjian 1965). Formation of the lichen association is dependent on the fungus randomly coming into contact with an alga, and growing lichen fungi will form exploratory hyphae around anything (even grains of sand) that they touch that might turn out to be an alga (Ahmadjian 1960). The low variety of algal species occuring in lichens appears to be dependent not on any direct attraction of the alga for the fungus, but on the alga's ability to resist digestion by the fungus' hyphae. Lichens are famed for their slow growth even after an association is established, and may increase in diameter by only a millimetre a year*, but the limiting factor is probably not so much their inherent growth abilities as that their favoured environments such as exposed on rocks may only allow growth for a minute part of the year.

*If you're thinking that that doesn't sound any greater than the rate for symbiont-less fungi that I cited above, remember that the latter rate applies to growth in the laboratory under theoretically optimal conditions; growth in the natural environment would be much, much slower.

REFERENCES

Ahmadjian, V. 1960. The lichen association. Bryologist 63 (4): 250-254.

Ahmadjian, V. 1965. Lichens. Annual Review of Microbiology 19: 1-20.

Crespo, A., & O. F. Cubero. 1998. A molecular approach to the circumscription and evaluation of some genera segregated from Parmelia s. lat. Lichenologist 30 (4-5): 369-380.

Elix, J. A. 1993. Progress in the generic delimitation of Parmelia sensu lato Lichens (Ascomycotina: Parmeliaceae) and a synoptic key to the Parmeliaceae. Bryologist 96 (3): 359-383.

Molina, M. del C., A. Crespo, O. Blanco, H. T. Lumbsch & D. L. Hawksworth. 2004. Phylogenetic relationships and species concepts in Parmelia s. str. (Parmeliaceae) inferred from nuclear ITS rDNA and β-tubulin sequences. Lichenologist 36 (1): 37-54.

If They Only Wood (Taxon of the Week: Diaporthales)

Perithecia (fruiting bodies) of Cryphonectria cubensis, the cause of eucalyptus canker. Photo by Edward Barnard.

Most people, when they think of fungi, will think of mushrooms. However, the majority of fungi do not produce such large and obvious structures as mushrooms; the majority of fungi are microscopic decomposers, whose minute fruiting bodies would be easily overlooked by those not looking for them. But tiny as these organisms are, they can have a significant effect on your life.

The Diaporthales are one order of these microfungi. They are a well-defined order of ascomycetes with brown or black perithecia (almost entirely enclosed fruiting bodies with only a single pore at one end and the spores produced inside) submerged either within a stroma (mass of hyphal tissue) or in the surrounding substrate on which they are growing (Rossmann et al., 2007). In many Diaporthales, the opening pore of the perithecia is on a long neck that may or may not also be submerged; it is the combination of round perithecium and elongate neck that lead the authors of one recently-described genus to dub it Lollipopaia (Inderbitzin & Berbee, 2001).


Pycnidia of Cryphonectria parasitica protruding from chestnut bark. Pycnidia resemble perithecia, but differ in containing asexually- rather than sexually-produced spores. Photo from here.

Most Diaporthales are decomposers of rotting wood. As such, they rarely come to humanity's attention, though it probably wouldn't take us long to notice if they disappeared. A small but significant number of Diaporthales, however, have earned a great deal of attention from humans because, while they grow on wood just like their relatives, they don't have the courtesy to wait for the tree to die first. The most famous (or notorious, depending on your preferred choice of adjectives) of Diaporthales is undoubtedly Cryphonectria parasitica, the cause of chestnut blight and famed as the bane of the American chestnut, C. dentata. According to Wikipedia, C. dentata may have made up as much as a quarter of the forest in the Appalachian region of eastern North America prior to the arrival of chestnut blight around 1905; by 1940, it was almost extinct. To this day, the position of the American chestnut across most of its original range remains tenuous; complete extinction has been staved off by the chestnut's ability to produce subsidiary shoots from its base, meaning that a number of trees survive despite being reduced to the central boles. However, complete regrowth is likewise prevented by the fungus attacking any new shoots before they achieve significant growth. Meanwhile, attempts to breed blight-resistant strains of American chestnut are hampered by the tree's slow growth rate.


Three views of American chestnut (Castanea dentata). On the left, American chestnut trees as they could still be found in 1910. In the centre, American chestnut as it survives today - an understorey regenerating shrub, prevented from reaching full growth by the inevitable onset of blight. On the right, the intermediary stage in a grown chestnut felled by the fungus. Images from Ellison et al. (2005).

When chestnut blight was recorded in European chestnut trees (Castanea sativa) in Italy in 1938, people expected a repeat of the American experience. And at first, that was almost exactly what happened - chestnut blight spread rapidly through western Europe, slowed only by the more scattered distribution of its host (C. sativa was not originally native to most parts of Europe, but introduced by the Romans; as a result, it does not form continuous forests in Europe as C. dentata did in America, but is largely only found where it has been deliberately planted by humans). However, during the 1950s and 1960s, reports started coming in of stands of chestnuts that appeared to be coping surprisingly well despite the obvious presence of blight (Heiniger & Rigling, 1994), with the damage from the blight extending only a short way into the wood (as it does in the Asian chestnut Castanea crenata, the original host of the fungus). What was more, when fungal hyphae from these wimpier infections were transplanted into further chestnut trees amongst more normal raging infections, the more virulent infections began to heal. The reduced virulence turns out to be due to a virus infecting the fungus - the disease being cured by a disease of its own. The spread of reduced virulence among chestnut blight in Europe has massively reduced the European epidemic. Attempts to implement the same cure in North America, however, have mostly resulted in failure (Milgroom & Cortesi, 2004). Transmission of reduced virulence between fungal colonies is slow and ineffecient, and in most cases seems to require direct human intervention to be truly effective. While this direct intervention is feasible with the more scattered European chestnut, it offers little hope of restoring the prior forests of American chestnut.

Other species of Diaporthales cause diseases in other crop trees and plants (including butternut canker caused by Sirococcus clavigignenti-juglandacearum, which I'm sure is a terrible thing to be afflicted by, even if it does sound like the name of some sort of confectionary). Dogwood anthracnose is caused by Discula destructiva, recently shown to be an anamorphic (asexual) member of the Diaporthales. Cytospora species attack Eucalyptus, while Greeneria uvicola causes bitter rot in grapes. If you feel enticed to explore the systematics and characteristics of the various subgroups of Diaporthales, there's an impressively detailed coverage on the U.S. Department of Agriculture's Diaporthales page, including a big interactive tree where clicking on a clade brings up descriptions and images to help you while away the hours.

REFERENCES

Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliott, C. R. Ford, D. R. Foster, B. D. Kloeppel, J. D. Knoepp, G. M. Lovett, J. Mohan, D. A. Orwig, N. L. Rodenhouse, W. V. Sobczak, K. A. Stinson, J. K. Stone, C. M. Swan, J. Thompson, B. Von Holle & J. R. Webster. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3 (9): 479-486.

Heiniger, U., & D. Rigling. 1994. Biological control of chestnut blight in Europe. Annual Review of Phytopathology 32: 581-599.

Inderbitzin, P., & M. L. Berbee. 2001. Lollipopaia minuta from Thailand, a new genus and species of the Diaporthales (Ascomycetes, Fungi) based on morphological and molecular data. Canadian Journal of Botany 79: 1099-1106.

Milgroom, M. G., & P. Cortesi. 2004. Biological control of chestnut blight with hypovirulence: a critical analysis. Annual Review of Phytopathology 42: 311-338.

Rossmann, A. Y., D. F. Farr & L. A. Castlebury. 2007. A review of the phylogeny and biology of the Diaporthales. Mycoscience 48: 135-144.

Reference Review: The Trials of Anamorphic Taxa

Skovgaard, K., S. Rosendahl, K. O’Donnell & H. I. Nirenberg. 2003. Fusarium commune is a new species identified by morphological and molecular phylogenetic data. Mycologia 95(4): 630-636.

Fusarium is a genus of filamentous soil fungi (shown above in a diagram from here) that is best known as a cause of a selection of nasty diseases of crop plants. It is an anamorphic genus - that is, it includes taxa that reproduce asexually. Fungal taxonomy maintains a complicated system of classifying asexual anamorphs separately from sexual teleomorphs, at least at the generic level (for instance, Fusarium anamorphs are associated with various teleomorphs of the family Nectriaceae - Rossman et al., 1999). In the past, there were separate families and higher for anamorphic taxa, but these have largely been abandoned. This system remains in place despite the fact that some "individual" hyphal masses (inasmuch as one can recognise an individual in fungi) may reproduce both asexually and sexually. In a previous post, I commented that the double taxonomy system was due to a "combination of history, theory and a certain degree of pragmatism". Anamorphs are usually completely different in appearance to teleomorphs, and there is generally no way to tell easily whether a given teleomorph corresponds to a given anamorph (usually, the only way to make a connection is to luck out and find one of the double-dipping hyphae I refered to a moment ago). Even when a connection is made, there is not necessarily a one-to-one relationship between anamorph and teleomorph - one anamorph may correspond to more than one teleomorph. There are even cases known where an anamorphic taxon is found worldwide, but its apparent teleomorph is only known from a very restricted location. A theoretical component can be invoked, too - species concepts are supposed to reflect gene flow, and gene flow is generally not occurring between anamorphic and teleomorphic lines. There are issues with the double taxonomy system, of course - perhaps most significantly, anamorphic taxa seem to be something of the poor cousins of mycology. Despite their being far more abundant in the environment, anamorphs seem to receive only a fraction of the attention given to their more glamorous teleomorphic counterparts.

I think it's worth noting that almost all anamorphic taxa are treated as essentially artificial form-taxa. Thus, while Fusarium seem to all fall within the Nectriaceae, there is no assumed guarantee that taxa with a Fusarium anamorph necessarily form a monophyletic unit. One teleomorphic genus may include members with a number of different anamorphic forms, that each may be shared with members of other teleomorphic genera. Attempts to try to restrict anamorphic genera phylogenetically, such as Sampaio et al. (2003), are relatively few and far between.

With that background explanation dealt with, on to the description of Fusarium commune Skovgaard et al., 2003. One of the big problems with taxonomy of anamorphic is that, well, there's often not that much to work with. All the flashy characters, the colourful mushrooms, the pungent truffles, the wierd-shaped fruiting bodies, are sexually-reproducing structures of teleomorphs. When a fungus is not actively fruiting, one collection of hyphae looks much like another. And conidia, the structures that give off asexually-produced spores in anamorphs, are often not much more than budding extensions of hyphae. As a result, useful morphological characters of anamorphs are few and often somewhat vaguely distinguished.

It should therefore come as no surprise at all that when molecular data was applied to anamorphs, it seemed that the amount of diversity present had been significantly underestimated. Convergence in anamorphs is rampant, and two morphologically near-identical samples may easily turn out to be very distant phylogenetically. So when morphological taxonomy has proven insufficient, in steps the substitute of molecular taxonomy. And that, I'm afraid, is where my hackles start to raise themselves just a little.

The use of molecular data in taxonomy is a much-abused field. Generally speaking, molecular data cannot resolve species. Any analysis of molecular data results in a branching tree, but species identifications are supposed to be about identifying gene flow in networks. There is no magic figure for "x% genetic divergence = different species". A single species with a large, widespread population (say, a wide-ranging bird species) may feature a large amount of genetic divergence without barriers to gene flow. In contrast, a cluster of short-range endemic species (e.g. snails that don't move about much at all) may have very little genetic variation within or even between populations without gene flow occurring between them. So any use of molecular taxonomy should be approached with extreme caution.

I'm glad to say that Skovgaard et al. seem to get it mostly right as far as I can tell. They use 15 different isolates of the new molecular species - a very important step in fending off the spectre of sample contamination. And they also identify some morphological traits supporting the new species. Fusarium commune differs from the closely related F. oxysporum in producing polyphialides and long, slender monophialides when grown in the dark*, while F. oxysporum produces short monophialides only (phialides are the hyphal branches that produce conidia - if I interpret correctly, polyphialides produce spores in multiple axes, while monophialides only have one axis). I am a little mystified as to why there are no samples of F. blasticola, referred to in the article text as very similar to F. commune, included in the molecular analysis. However, Skovgaard et al. do demonstrate the distinction of F. commune from F. blasticola through a pathogenicity test. Fusarium blasticola is a pathogen of Picea (spruces) and Pinus (pines). Despite specimens of these two hosts being grown for five months in soil inoculated with cultures of F. commune, no sign of infection was noticed. Fusarium commune has since been shown to be able to cause infection in Pseudotsuga (the Douglas fir), another commercial conifer (Stewart et al., 2006).

REFERENCES

Rossman, A. Y., G. J. Samuels, C. T. Rogerson & R. Lowen. 1999. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Studies in Mycology 42: 1-248.

Sampaio, J. P., M. Gadanho, R. Bauer & M. Weiss. 2003. Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiella gen. nov. and the new orders Leucosporidiales and Sporidiobolales. Mycological Progress 2(1): 53-68.

Stewart, J. E., M.-S. Kim, R. L. James, J. R. Kasten Dumroese & N. B. Klopfenstein. 2006. Molecular characterization of Fusarium oxysporum and Fusarium commune isolates from a conifer nursery. Phytopathology 96 (10): 1124-1133.

Reference Review: Messing about with Mildews

Before I start, a reminder that I'll be putting up the Boneyard tomorrow evening, so get any posts for it in quick. Don't forget that Saturday comes earlier for us antipodeans than it does for you European and North American sorts!



Hosagoudar, V. B. 2003. Armatellaceae, a new family segregated from the Meliolaceae. Sydowia 55: 162-167.

It seems that this is Fungal Week here at Catalogue of Organisms - I've barely mentioned them in the past, and suddenly two posts on fungi in rapid succession. Not that I'm complaining - fungi are one of my favourite groups of organisms, and few things are more exciting than coming across some bizarre-looking fungus growing from a rotting log in some damp patch of forest. But as with Wednesday's post, today's subjects come from the less obvious but far more numerous sector of fungal diversity.

Black or dark mildews are parasitic fungi found on plants, particularly the leaves. There are a number of largely unrelated families of ascomycetous fungi that cause black mildew (the picture above from here shows a leaf infected by Apiosporum salicinum - I haven't been able to establish if Apiosporium is closely related to the specific family I'm dealing with today, but the general appearance is probably similar). Though parasitic on a number of food species, none of the black mildews is significant enough to have attracted a huge amount of research attention (reading between the lines, I suspect that they are also somewhat overlooked because they are more significant in the tropics than in temperate developed countries). According to Hosagoudar (2003), their growth on leaves raises the temperature in the affected area, increasing respiration and transpiration rates and reducing photosynthetic efficiency and therefore growth.

The greater part of Hosagoudar (2003) is taken up by a whirlwind tour of the taxonomic history of the Meliolaceae, one of the families of black mildews. At the time of Hosagoudar's writing, Meliolaceae was the only family in the order Meliolales, distinguished by the unique combination of features of an ectophytic (living on the surface of leaves) mycelium with lateral appresoria (swollen points on the hyphae that press against the leaf and give rive to hyphae piercing the leaf surface) and phialides (hyphal cells producing successive spherical asexual spores in chains). At the end of the paper, almost as an afterthought, Hosagoudar establishes the family Armatellaceae for a single genus, Armatella, previously included in Meliolaceae, that lacks phialides and also differs from Meliolaceae proper in having 1-septate ascospores as opposed to 3- to 4-septate ascospores.

I have rather a problem with this sort of setup. Armatella is separated from the other Meliolaceae solely on typological grounds, without any sort of detailed analysis to establish whether the remaining Meliolaceae are truly more closely related to each other than to Armatella. The most recent Outline of Ascomycota (Eriksson, 2006) accepts Armatellaceae in Meliolales, but the Notes on ascomycete systematics that first recorded Hosagoudar's publication (Eriksson, 2005) had a much more cautious reaction, noting that another genus, Diporotheca, had previously been isolated in its own family from Meliolaceae on the basis of lacking phialides. While Hosagoudar (2003) did mention Diporotheca in his taxonomic overview, no comparison of Armatella to Diporotheca was recorded. It is worth noting that in a later paper that Hosagoudar himself is an author on, Armatella has managed to quietly reinsert itself back into Meliolaceae (Biju et al., 2005)*.

*Two other possibilities must be acknowledged here, though: (A) Hosagoudar is not primary author on the latter paper, and it may be that the chosen classification represents the views of the primary author and not those of Hosagoudar, and (B) the time difference between 2003 and 2005 is small enough that Hosagoudar's contribution to the 2005 paper may have actually occurred before he wrote the 2003 paper, with a delay in the appearance of the 2005 paper at either the collation or publication stage.

My even bigger issue, however, is to ask what exactly is the point of establishing a monogeneric family. The concept of 'ranking' is, in my opinion, one of the biggest issues in classification today, and I currently have something of a hate-hate relationship with ranks. It is a widely-known secret that all taxonomic ranks (with the probable, but controversial, exception of the 'species') are essentially arbitrary concepts, and there is no real reason why a given taxon should be recognised as an order or a family or whatever beyond how it sits in relation to other related taxa that have previously been recognised as orders or families or whatever. Different historical factors in research on different groups of organisms mean that a family of insects is in no way a comparable unit to a family of birds or plants or fungi. I personally try to avoid referring a taxon to a specific rank, at least in the privacy of my own head. The problem that really makes me grit my teeth, however, is that when it comes to trying to discuss biodiversity to other people, ranks prove so irritatingly convenient! Most people who don't have to deal with the details of classification every day find it relatively easy to grasp the concept that each rank corresponds to a certain level of superficial distinction (at least from our own human-centric viewpoint), and that a genus represents a smaller degree of distinction than a family, which is in turn less distinct than an order. Also, try as I might, there's only so many times I can use a variation on "clade" or "group" without becoming repetitive, confusing or both (and besides, I usually end up having to refer to "clade A" and "subclade B", invoking an even more arbitrary sort of ranking to indicate that B is a section of A, even though there's no actual difference between "clade" and "subclade" and, were I to change my focus slightly, I might end up referring to "clade B" and "subclade C").

However, given that where and what an individual author chooses to recognise as a given rank is essentially subjective, what does separating a genus into its own family really tell us? The prior establishment of the genus already tells us that it is a distinctive unit. There is a certain virtue to establishing a different concept of the taxon "Meliolaceae" from the taxon "Meliolales", rather than the previous set-up where there were two names for the exact same thing, but in establishing the taxon "Armatellaceae" to contain only "Armatella", we again have two names for the exact same thing, and that's just cluttering up the nomenclature.

Postscript: Unless I head them off at the pass now, it is entirely likely that someone will weigh in on the comments with the PhyloCode argument (I'm looking at you, Mike)*. Someday I'm going to be forced to actually say something on the whole PhyloCode question, on which I am an inveterate fence-sitter. For now, let it suffice to say that I'm not convinced that introduction of the PhyloCode principles would particularly improve matters in corners of phylospace such as this one where the vast majority of taxa still have not been phylogenetically investigated to a significant degree, and while yes, PhyloCode may stabilise taxon definition, taxon content here would probably continue to leap about like a drunken grasshopper.

*Some of you may know Mike Keesey as the author of the Dinosauricon, which was one of the first major web resources on Dinosauria, and I came to know his by-line well back in my DML days. The link above takes you to his brand-spanking new blog, so take a look!

REFERENCES

Biju, C. K., V. B. Hosagoudar & T. K. Abraham. 2005. Meliolaceae of Kerala, India - XV. Nova Hedwigia 80 (3-4): 465-502.

Eriksson, O. E. (ed.) 2005. Notes on ascomycete systematics. Nos 3912-4298. Myconet 11: 115-170.

Eriksson, O. E. (ed.) 2006. Outline of Ascomycota - 2006. Myconet 12: 1-82.