Individual cells and culture plate of Cystofilobasidium capitatum, from Marova et al. (2011).

Belongs within: Opisthokonta.
Contains: Exobasidiomycetes, Ustilaginales, Urocystales, Dacrymycetales, Agaricomycetes, Tremellales.

A relict fungus on a relict host
Published 7 November 2008
Ginkgo leaves infected with the fungus Bartheletia paradoxa (above) and individual Bartheletia telia (below), from Scheuer et al. (2008).

Welcome to Fantastic Fungus Friday! Today brought me word of not just one, but two incredible discoveries involving fungi. For the first one, I’ll send you over to Hyphoid Logic to learn about a fungus that not only digests cellulose (that is, wood), but in doing so releases a mix of organic chemicals that might potentially be used as a diesel substitute. Could an unassuming fungus be the saviour of civilisation as we know it?

The second great discovery is perhaps a little more esoteric, but none the less fascinating, and it involves ginkgo trees. Ginkgo biloba is one of the most famous plants to labour under that most unfortunate of labels, the “living fossil”. Species assigned to the genus Ginkgo date back to the Lower Jurassic, and Ginkgo biloba is the sole surviving species of the Ginkgoales, which, together with the cycads, Gnetales, conifers and angiosperms, is regarded as one of the five primary divisions of living seed plants (some authors have suggested that Ginkgoales are a derived subgroup of the conifers, but retention by Ginkgo biloba of some plesiomorphic features absent from conifers such as motile sperm make this unlikely). Remarkably, Ginkgo may be unknown in the truly wild state—by the time any Europeans first encountered it, they did so only as plants cultivated in eastern Asia, while the only known small populations of ‘wild’ Ginkgo have been suggested to be also derived from human cultivation, rather than naturally occurring (Shen et al. 2005).

Despite having only survived to the present by the narrowest of margins, Ginkgo biloba thrives in cultivation, and has been widely planted. Part of the reason that Ginkgo does so well is that almost nothing harms it. Ginkgo leaves are chock-full of toxic compounds, and very little in the way of animals or fungi feeds or grows on them. A paper in the latest edition of Mycological Research (Scheuer et al. 2008) describes an exceptional fungus that does grow on fallen ginkgo leaves—and the fungus is every bit as remarkable as the plant it cleans up after.

SEMs of Bartheletia telia, and of individual basidia (the poppy-head shaped structures) on the telia, from Scheuer et al. (2008).

Bartheletia paradoxa was first recorded in 1954, but Scheuer et al. (2008) represents its first valid publication (botanical nomenclature requires a Latin diagnosis for new taxa, which the 1954 description lacked). It is, to be honest, not a lot to look at macroscopically—just a little black spot of decay on fallen leaves. Microscopically is a different matter. Bartheletia is a basidiomycete—the clade of fungi that includes most familiar mushrooms, as well as plant pathogens such as rusts and smuts. However, Bartheletia bears a number of features unlike any other basidiomycete—most notably, it has a septal structure that is completely unique. In most basidiomycetes, the septa dividing cells within the hyphae are perforated by a large central pore. Bartheletia lacks such a pore, and instead has the septa perforated by a number of narrow perforations that Schuer et al. describe as more like the plasmodesmata connecting plant cells. Phylogenetically, Bartheletia is also remarkable—it belongs to the Hymenomycetes (the clade including mushroom-producing fungi, as well as jelly fungi and wood-ears), but it doesn’t seem to belong to any of the hymenomycete clade Schuer et al. compare it with. The suggestion (which requires more detailed analysis to confirm) is that this is a fungus which has been phylogenetically isolated from all other living fungi for nearly as long as its host has been from all other living plants. The fungal fossil record is not too great, but the presence of a fossil mushroom in Cretaceous amber (Poinar & Brown 2003) indicates that the primary lineages of Hymenomycetes had diverged by at least that date.

Bartheletia seems to be unique to the Ginkgo leaves it holds its monopoly over—attempts by Scheuer et al. to grow it on leaves of other plant species failed miserably. It grew on blueberry leaves, but not on fifty-four other species including five other species in the same family as blueberries (go figure), and infections on blueberry leaves only formed asexual spores. Ginkgo trees lose their leaves rapidly over a couple of days in autumn. How Bartheletia infects fallen leaves is something of a mystery – no sign of it was found on living leaves still attached to the tree, so infection must happen after the leaf is dropped. Scheuer et al. suggest that spores may be transferred from the remains of leaves dropped the previous year. The adhesive spores may also be spread by soil-dwelling invertebrates. The former explanation may also be why Bartheletia seems to be an uncommon fungus, as the clearing of old leaves by cultivators would break the cycle. Once infection does happen, the growth of Bartheletia is extremely rapid. Bartheletia, like many other basal basidiomycetes, has a triphasic lifecycle. When the developing haploid* fungus first erupts through the leaf surface, it produces conidia, asexual spore-producing structures. These are soon replaced by structures called telia that produce much thicker, larger teliospores. The teliospores remain dormant over the following winter and summer, then germinate to produce diploid basidia. When exactly cross-fertilisation occurs has not been observed—it may be between germinating teliospores. Each basidium then undergo meiosis to form four haploid basidiospores that will germinate into new conidia- and telia-producing hyphae. The entire cycle from teliospore germination to teliospore maturity can be over in as little as two weeks—and then its time to wait out the seasons until the next autumn, and the next leaf fall.

*While animals are diploid for most of their life cycle, fungi are haploid for most of theirs.

Systematics of Orthomycotina
    |--Ustilaginomycotina [Hemibasidiomycetia, Ustomycetes]C-S98
    |    |--ExobasidiomycetesAS12
    |    |--Moniliella Stolk & Dakin 1966 [Moniliellaceae, Moniliellales, Moniliellomycetes]AB19
    |    |    `--M. acetoabutansAB19
    |    |--Entorrhizales [Entorrhizaceae, Entorrhizomycetes, Entorrhizomycetidae, Entorrhizomycota]V02
    |    |    |--Talbotiomyces [Talbotiomycetales]AS12
    |    |    `--Entorrhiza Weber 1884 [incl. Schinzia Nägeli 1842 non Dennstätt 1818]KC01
    |    |         |--E. aschersonianaBSB06
    |    |         `--+--E. casparyanaBSB06
    |    |            `--E. fineraniBSB06
    |    `--Ustilaginomycetes [Ustilaginomycetidae]AS12
    |         |--UstilaginalesV02
    |         `--UrocystalesV02
    `--Agaricomycotina (see below for synonymy)C-S98
         |  i. s.: Fibrillaria Sowerby 1803 (n. d.)KC01
         |  `--AgaricomycetesHB02
              |    |--+--‘Cryptococcus’ himalayensisT-HW02
              |    |  `--Filobasidium Olive 1968GT-H04, KC01
              |    |       |--F. capsuligerumGT-H04
              |    |       `--F. globisporumKS01
              |    `--+--‘Cryptococcus’ albidusGT-H04
              |       `--‘Cryptococcus’ vishniaciiGT-H04
              `--Cystofilobasidiaceae [Cystofilobasidiales]AS12
                   |  i. s.: ‘Cryptococcus’ aquaticusGT-H04
                   |--Udeniomyces Nakase & Takem. 1992KC01
                   |--Cystofilobasidium Oberw. & Bandoni 1983KC01
                   |    |--C. bisporidiiKS01
                   |    |--C. capitatumKS01
                   |    `--C. infirmominiatumHTN02
                   |--Mrakia Yamada & Komag. 1987KC01
                   |    |--M. frigidaSL02
                   |    `--M. gelidaGT-H04
                   `--Xanthophyllomyces Golubev 1995 (see below for synonymy)KC01
                        |--X. dendorousBJ03
                        `--‘Phaffia’ rhodozymaSM03

Agaricomycotina [Autobasidii, Gelimycetes, Heterobasidiomycetes, Homobasidiomycetae, Hymenomycetes, Hymenomycetia, Phragmobasidiomycetidae]C-S98

Xanthophyllomyces Golubev 1995 [incl. Phaffia Mill., Yoney. & Soneda 1976, Rhodomyces Wettst. 1885, Rhodozyma Phaff, Mill. et al. 1972]KC01

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[BSB06] Begerow, D., M. Stoll & R. Bauer. 2006. A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98 (6): 906–916.

[BJ03] Berry, A., D. Janssens, M. Hümbelin, J. P. M. Jore, B. Hoste, I. Cleenwerck, M. Vancanneyt, W. Bretzel, A. F. Mayer, R. Lopez-Ulibarri, B. Shanmugam, J. Swings & L. Pasamontes. 2003. Paracoccus zeaxanthinifaciens sp. nov., a zeaxanthin-producing bacterium. International Journal of Systematic and Evolutionary Microbiology 53: 231–238.

[C-S98] Cavalier-Smith, T. 1998. A revised six-kingdom system of life. Biological Reviews 73: 203–266.

[GT-H04] Guffogg, S. P., S. Thomas-Hall, P. Holloway & K. Watson. 2004. A novel psychrotolerant member of hymenomycetous yeasts from Antarctica: Cryptococcus watticus sp. nov. International Journal of Systematic and Evolutionary Microbiology 54: 275–277.

[HTN02] Hamamoto, M., V. N. Thanh & T. Nakase. 2002. Bannoa hahajimensis gen. nov., sp. nov., and three related anamorphs, Sporobolomyces bischofiae sp. nov., Sporobolomyces ogasawarensis sp. nov. and Sporobolomyces syzygii sp. nov., yeasts isolated from plants in Japan. International Journal of Systematic and Evolutionary Microbiology 52: 1023–1032.

[HB02] Hibbett, D. S., & M. Binder. 2002. Evolution of complex fruiting-body morphologies in homobasidiomycetes. Proceedings of the Royal Society of London Series B – Biological Sciences 269: 1963–1969.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[KS01] Kirschner, R., J. P. Sampaio, M. Gadanho, M. Weiß & F. Oberwinkler. 2001. Cuniculitrema polymorpha (Tremellales, gen. nov. and sp. nov.), a heterobasidiomycete vectored by bark beetles, which is the teleomorph of Sterigmatosporidium polymorphum. Antonie van Leeuwenhoek 80: 149–161.

Poinar, G. O., Jr., & A. E. Brown. 2003. A non-gilled hymenomycete in Cretaceous amber. Mycological Research 107 (6): 763–768.

[SM03] Saldarriaga, J. F., M. L. McEwan, N. M. Fast, F. J. R. Taylor & P. J. Keeling. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53: 355–365.

Scheuer, C., R. Bauer, M. Lutz, E. Stabentheiner, V. A. Mel’nik & M. Grube. 2008. Bartheletia paradoxa is a living fossil on Ginkgo leaf litter with a unique septal structure in the Basidiomycota. Mycological Research 112 (11): 1265–1279.

[SL02] Schweigkofler, W., K. Lopandic, O. Molnár & H. Prillinger. 2002. Analysis of phylogenetic relationships among Ascomycota with yeast phases using ribosomal DNA sequences and cell wall sugars. Organisms Diversity & Evolution 2: 1–17.

Shen, L., X.-Y. Chen, X. Zhang, Y.-Y. Li, C.-X. Fu & Y.-X. Qiu. 2005. Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR-RFLPs: inference of glacial refugia. Heredity 94: 396–401.

[T-HW02] Thomas-Hall, S., & K. Watson. 2002. Cryptococcus nyarrowii sp. nov., a basidiomycetous yeast from Antarctica. International Journal of Systematic and Evolutionary Microbiology 52: 1033–1038.

[V02] Vánky, K. 2002. The smut fungi of the world. A survey. Acta Microbiologica et Immunologica Hungarica 49 (2–3): 163–175.

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