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Fossil Evidence of the Zygomycetous Fungi

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Fossil Evidence of the Zygomycetous Fungi Persoonia 30, 2013: 1–10 www.ingentaconnect.com/content/nhn/pimj REVIEW ARTICLE http://dx.doi.org/10.3767/003158513X664819 Fossil evidence of the zygomycetous fungi M. Krings1,2, T.N. Taylor 2, N. Dotzler1 Key words Abstract Molecular clock data indicate that the first zygomycetous fungi occurred on Earth during the Precambrian, however, fossil evidence of these organisms has been slow to accumulate. In this paper, the fossil record of the Endogonales zygomycetous fungi is compiled, with a focus on structurally preserved Carboniferous and Triassic fossils interpreted fossil record as zygosporangium-gametangia complexes and resembling those of modern Endogonales. Enigmatic microfossils morphology from the Precambrian to Cenozoic that have variously been interpreted as, or compared to, zygomycetous fungi reproductive biology are also discussed. Among these, the spherical structures collectively termed ‘sporocarps’ are especially interesting sporocarp because of their complex investments and abundance in certain Carboniferous and Triassic rocks. Circumstantial zygosporangium-gametangia complex evidence suggests that at least some ‘sporocarp’ types represent mantled zygosporangia. Zygomycetous fungi probably were an important element in terrestrial paleoecosystems at least by the Carboniferous. Article info Received: 10 September 2012; Accepted: 1 January 2013; Published: 18 February 2013. INTRODUCTION group are to date based exclusively on the analysis of extant members (e.g., White et al. 2006, Liu et al. 2009, Petkovits et The zygomycetous fungi (formerly Zygomycota) comprise ~1 % al. 2011). of the true fungi; approximately 900 living species have been The scarcity of fossil evidence of zygomycetous fungi remains described (Kirk et al. 2001). They are an ecologically hetero- perplexing, especially in light of the fact that habitats conducive geneous, para- or polyphyletic assemblage of predominantly to the growth of these organisms, together with depositional terrestrial organisms (White et al. 2006, Liu et al. 2009, Liu & environments conducive to their preservation, were available at Voigt 2010). The vegetative mycelium generally lacks septa least by the Paleozoic (see Krings et al. 2012a). The scarcity of except where reproductive units are produced and in regions reports appears to be related to the nature of the fossil record of old hyphae. Zygomycetous fungi reproduce asexually via of fungi in general that typically results in the preservation of non-motile endospores formed in sporangia, sporangiola, or isolated parts or stages of the life cycle. Another reason may be merosporangia, or by the formation of chlamydospores, arthro- that most zygomycetous fungi are saprotrophs. While biotrophic spores, and yeast cells, and sexually (where documented) by fungi often trigger the formation of host responses, and/or the formation of zygospores following gametangial fusion, or possess specific infection/penetration structures (e.g., appres- azygospores without prior gametangial conjugation (Benjamin soria), along with special features facilitating nutrient extraction 1979, Benny et al. 2001). Most zygomycetous fungi thrive as from the host (e.g., arbuscules, haustoria), saprotrophs do saprotrophs, others as parasites of plants, animals, and other not normally possess special structures that allow for positive fungi (White et al. 2006, Richardson 2009); still others enter recognition as fossils. As a result, far more attention has been into mutualistic associations (mycorrhizae) with plants (Fassi directed to date at biotrophic than at saprotrophic fossil fungi. et al. 1969, Walker 1985). Despite the comments above there is increasing evidence of Molecular clock estimates indicate that the first zygomycetous fossil zygomycetous fungi that indicate an untapped wealth fungi occurred on Earth during the Precambrian, approximately of information and more recently, a new emphasis on their 1.2–1.4 Ga ago (Heckman et al. 2001, Blair 2009); more con- paleodiversity and evolutionary history. This paper compiles servative estimates place the divergence at about 800 Ma the fossil evidence of the zygomycetous fungi, with a focus on (Berbee & Taylor 2001). If these estimates are accurate, zy- structurally preserved remains interpreted as zygosporangium- gomycetous fungi were certainly important elements in ancient gametangia complexes. Moreover, we also report on several terrestrial ecosystems. Nevertheless, documented evidence of enigmatic fossils from chert, coal balls, amber, shales, and fossil zygomycetes continues to be rare. Not even the famous palynological sampling that have variously been referred to the Early Devonian Rhynie chert (~410 Ma), which is the single- zygomyceteous fungi. Of the latter, the so-called ‘sporocarps’ most important source of information on fossil fungi to date are discussed in greater detail because of their interesting relative to paleoecosystem functioning (Taylor et al. 2004), morphology and abundance in certain rocks, especially those has produced conclusive evidence of zygomycetous fungi. As from the Carboniferous. a result, efforts in reconstructing the evolutionary history and phylogeny of the zygomycetous fungi or of lineages within this MODES OF PRESERVATION 1 Department für Geo- und Umweltwissenschaften, Paläontologie und Geo- biologie, Ludwig-Maximilians-Universität, and Bayerische Staatssammlung The success of recognising and documenting fossil fungi relies für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, heavily on the mode of preservation and technique(s) used to Germany; corresponding author e-mail: [email protected]. prepare samples. The most common types of fossil preserva- 2 Department of Ecology and Evolutionary Biology, and Natural History tion (i.e., impressions, compressions, casts and moulds), with Museum and Biodiversity Institute, University of Kansas, Lawrence KS 66045-7534, USA. the exception of compressions with preserved cuticle (e.g., see © 2013 Naturalis Biodiversity Center & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 2 Persoonia – Volume 30, 2013 Fig. 1 Fossil evidence of zygomycetous fungi (references and further explanations in the text). a. Tappania sp., Lower Neoproterozoic shale, Canada (cour- tesy N.J. Butterfield). — b, c. Microfossils resembling mucoralean columellae; Lower Devonian Rhynie chert, Scotland. — d, e. Winfrenatia reticulata, Lower Devonian Rhynie chert, Scotland; d. thallus; e. hyphal net enclosing cyanobacterial unicells. — f–h. Fungal reproductive units interpreted as zygosporangia with apposed gametangia, Lower Pennsylvanian coal ball, Great Britain; f. group of specimens, two of which showing paired gametangia (arrows); g, h. gametangial fusion. — i–k. Fungal reproductive units interpreted as mantled zygosporangia with apposed gametangia, Lower Pennsylvanian coal ball, Great Britain; i. two specimens, one showing paired gametangia (arrows); j. investment; k. gametangia or suspensors in cross section (arrows). — l, m. Halifaxia taylorii, Lower Pennsylvanian coal ball, Great Britain; l. ‘smaller element’ and microgametangial branch (arrow); m. mantled zygosporangium (Z), macrogametangium (MG), and microgametangial branch (mG). — n, o. Protoascon missouriensis, Upper Pennsylvanian coal ball, USA; n. large suspensor (S), ornamented zygosporangium (Z), and putative small suspensor (arrow, S); o. suspensor appendages. — p. Jimwhitea circumtecta, Middle Triassic permineralized peat (chert), Antarctica, zygosporangium (Z) enveloped in hyphal mantle (HM), macrogametangium (MG) and macrosuspensor (MS), microgametangium (mG) and microsuspensor (mS), gleba (G). — q. Fungus No. 4, Middle Triassic permineralized peat (chert), Antarctica, mantled zygosporangium subtended by sac-like gametangium (arrow). — Scale bars: a = 100 µm; b, c, i, l–q = 20 µm; d = 1 mm; e, f = 50 µm; g, h, k = 10 µm; j = 5 µm. M. Krings et al.: Fossil zygomycetous fungi 3 Dilcher 1965, Krings 2001, Hübers et al. 2011), do not normal ly vyrov (2006) describe compressions of irregularly aggregated provide sufficient resolution to detect fungi, let alone to deter- filaments, globules, and what appear to be copulating filaments mine their systematic affinities. To date coal balls and chert from the Lakhanda microbiota (Late Riphean; ~1020–1030 represent the only sources of compelling evidence of fossil Ma) of the Uchur-Maya Region of south-eastern Siberia as zygomycetes. While coal balls are typically concretions of Mucorites ripheicus. The fossils are believed to represent dif- calcium carbonate, chert deposits generally are an extremely ferent life cycle stages of a mucoralean zygomycete, in which dense microcrystalline or cryptocrystalline type of sedimentary gametangial fusion and (a-)zygospore formation are virtually rock. In both
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