Other unidentified fungi

Very often it is impossible to determine the systematic affinities of a parasitic fungus based on fossils. For instance, three morphologically different types of endophytic fungi occur in the prostrate axes of the Rhynie chert land plant Nothia aphylla (Krings et al., 2007b, 2007c). In spite of the exquisite preservation of the fungi, their affinities remain unclear. The association is nevertheless noteworthy because axes heavily infected by one of these fungi show a hypodermal zigzag line composed of secondarily thickened cell walls that appears to represent a specific host response effective in separating infected from uninfected tissues (Fig. 2O). Another fungus in N. aphylla triggers a host response in the form of encasement layers consisting of cell wall material that exclusively form around hyphae of this endophyte.
A truly enigmatic fossil from the Rhynie chert is Triskelia scotlandica, an acritarch-like structure with a prominent surface ornamentation. The form had been initially described as a green algal resting stage (Strullu-Derrien et al., 2021), but the subsequent discovery of specimens that occur in situ in prominent swellings of fungal hyphae provided strong evidence that it was not algal, but rather fungal in nature (Krings, 2021). Moreover, specimens with a discharge tube suggest that T. scotlandica may be a zoosporangium or resting spore stage of an endoparasite (Fig. 2P), perhaps with affinities to holocarpic Oomycota (e.g., Olpidiopsis), Cryptomycota (e.g., Rozella), or zoosporic Fungi (e.g., Olpidium), in which case the hyphal swellings would be either dilatations resulting from the expansion of the parasite inside, or a host response (hypertrophy).
A geologically younger, presumably parasitic fungus of unknown affinity is Cashhickia acuminata, which is preserved in permineralized calamite roots from the Upper Pennsylvanian of central France (~304 Ma) (Taylor et al., 2012). Infected roots contain intracellular hyphae in the outer cortex that arise from a meshwork-like mycelium extending between cortical cells. All intracellular hyphae are oriented towards the root centre. Within the cortical cells are host responses in the form of callosities that indicate the roots were alive at the time of infection (Fig. 2Q). Fossils similar to C. acuminata have been described in roots from the Triassic of the Svalbard archipelago by McLoughlin and Strullu-Derrien (2016). Other evidence of fungal parasitism in Pennsylvanian plants occurs in a Lasiostrobus polysaccii cone from Illinois, USA (~310 Ma) (Stubblefield et al., 1984). On the inner surface of cortical cells containing fungal hyphae are peculiar swellings that appear to represent wall appositions produced by the host in response to the infection.
Septate fungal hyphae present in silicified Agathoxylon (Araucariaceae) wood from the Upper Cretaceous (~84 Ma) of South Africa have been compared with blue-stain fungi colonizing the wood of present-day Pinus strobus (Strullu-Derrien et al., 2022). They represent the first documented evidence of these wood-colonizing Ascomycota in the geological record. Structures interpreted as fungal mycelia of uncertain affinity have also been found in sections of dinosaur egg shells from the Upper Cretaceous (~80 Ma) of central China (Gong et al., 2008). Based on fungal morphology and the areas in the shells in which the fungi occur, it has been hypothesized that the fungi were parasitic and invaded the eggs before they became lithified.

Concluding Remarks

Fungi today master very different levels of interaction with various other organisms. They form lichens, enter into mutualistic relationships with plants and animals, occur as endophytes in virtually all land plants, and negatively affect the functions of other microorganisms, plants, animals, and even humans as parasites and pathogens (Kaishian et al., 2022). Fungi probably had similar roles in the geologic past. Documenting these roles based on fossils is a challenging task, foremost because of the low preservation potential of most fungal life cycle stages, and because the majority of fungal fossils occur dispersed and are fragmented (Taylor et al., 2015a). It is clear from the examples of fossil fungal parasitism presented in the sections above that the key to understanding fungi as constituents of past ecosystems is the extraordinary preservation found in certain rock deposits. While the Rhynie chert of Scotland is perhaps the prime illustration of this, there are other fossil ecosystems that have been preserved in a similar manner, but to date have received less attention (e.g., García Massini et al., 2012; Klymiuk et al., 2012; Harper et al., 2016). As more information is gathered on the fungi preserved in these deposits, and as further rock deposits containing well preserved fungi are unearthed, additional examples of fungal parasitic interactions will be discovered and described. This will provide increasing opportunities to relate fossils to extant analogues to better understand the past diversity, evolutionary history, and past ecological functions of parasitic fungi.

Acknowledgments

C.L. is supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB26000000), the Second Tibetan Plateau Scientific Expedition and Research (2019QZKK0706), and the National Natural Science Foundation of China (42125201, 41688103). D.H. was supported by the Research Foundation – Flanders (FWO Junior Postdoctoral Fellowship 1206620N). M.K.’s research on fossil fungi received funding from the U.S. National Science Foundation (EAR-0542170, EAR-0949947, and DEB-1441604–S1696A-A), the Alexander von Humboldt Foundation (V-3.FLF-DEU/1064359), and the Deutsche Forschungsgemeinschaft (KE584/13-2, KR2125/5-1). M.K. thanks Hans Kerp and Hagen Hass (both Münster, Germany), Nora Dotzler (Munich, Germany), Jean Galtier (Montpellier, France), Carla J. Harper (Dublin, Irleand), Christopher Walker (Gloucester, UK), Edith L. Taylor (Lawrence, KS, USA) and Thomas N. Taylor (†) for fruitful collaboration over many years. The chapter benefited greatly from constructive comments and suggestions by Alexander R. Schmidt (Göttingen, Germany).

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