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Oomycetes and Their Role in Late Palaeozoic–Early Mesozoic Ecosystems

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Oomycetes and Their Role in Late Palaeozoic–Early Mesozoic Ecosystems 10th New Phytologist Workshop, Natural History Museum, London, 2014 Oomycetes and their role in Late Palaeozoic–Early Mesozoic ecosystems Ben J. Slater1-2, Stephen McLoughlin3, Jason Hilton2 1Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, UK ([email protected]) 2School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham, UK 3Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, S-104 05 Stockholm, Sweden Oomycetes are a diverse group of multicellular eukaryotes that are widespread in terrestrial and aquatic environments. They are important plant, fungal and animal pathogens in modern ecosystems, one species, Phytophthora infestans, famously being responsible for potato late blight, which has significantly impacted human history and agriculture (Dick 2001). Based on estimates from molecular clock data, oomycetes have been viewed as an ancient group that originated between the early Neoproterozoic to Cambrian (1 Gya – 524 Mya; Bhattacharya et al. 2009), but more recent analyses have placed the origins of the clade within the Silurian or Devonian (Matari and Blair 2014). Nevertheless, descriptions of pre-Cretaceous fossil oomycetes are rare, which has restricted the utility of the fossil record in deciphering the history of this group to date (Krings et al. 2011). Recognition of fossil oomycetes is particularly challenging since their broad morphology is convergent with many other filamentous and osmotrophic organisms – the hyphae of oomycetes are especially difficult to distinguish from those of true fungi in fossil material, for example. Robust assignment of any candidate fossil to an oomycete identity therefore typically requires preservation of the delicate but characteristic oogonium–antheridium reproductive complexes. Recent discoveries of fossil oomycetes (alternatively Peronosporomycetes) in association with anatomically preserved plant remains from Devonian–Triassic strata have significantly expanded our otherwise limited knowledge of the fossil record of this group. Well preserved oogonia and subtending hyphae have been identified in association with the anatomically preserved permineralised tissues of lycophytes (Dotzler et al. 2008; McLoughlin et al. In press), ferns (Krings et al. 2010), pteridosperms (Strullu-Derrien et al. 2010) and gymnosperms (Slater et al. 2013) from a range of Devonian–Triassic deposits globally. The majority of these forms have been interpreted as endophytic or saprotrophic (Taylor et al. 2006; Slater et al. 2013), with one example assigned to a parasitic habit (Strullu-Derrien et al. 2010). Additionally, these fossil oomycetes have been found in a diverse array of palaeoenvironments, spanning the palaeotropics (Strullu-Derrien et al. 2010) to high–palaeolatitude temperate mire systems (Schwendemann et al. 2009). One such high- palaeolatitude mire system is preserved in the Toploje member chert, a Permian silicified peat deposit from the Prince Charles Mountains in Antarctica (McLoughlin et al. 2011; Slater et al. 2011, 2012, 2014). Recently, thin sections of these cherts have been shown to reveal a remarkable wealth of fungal and fungal-like forms preserved among permineralised plant tissues, including exquisitely fossilised oomycetes assigned to the Combresomycetales (Slater et al. 2013). The distinctively ornamented Combresomycetales of Late Palaeozoic–Early Mesozoic distribution appear to have been particularly versatile with respect to plant hosts; this coupled with their continuation into the Triassic indicates that Combresomycetales were generalist or opportunistic organisms that were little affected by the 5 million year hiatus of peat forming ecosystems following the Permian–Triassic biotic crisis (Slater at al. 2013). While the fossil record of Late Palaeozoic–Early Mesozoic oomycetes 10th New Phytologist Workshop, Natural History Museum, London, 2014 remains patchy, an increased awareness of the previously overlooked microorganism content preserved in historical slide collections (Taylor et al. 2011) of coal balls and silicified peats promises to further elucidate the history of this group. Acknowledgements This research was supported by a Natural Environment Research Council, U.K., scholarship (NE/H5250381/1), and an EU Synthesys programme grant (SE-TAF-4827) to BJS. References Bhattacharya, D., Yoon, H.S., Hedges, S.B., Hackett, D., 2009. Eukaryotes. In: Hedges, S.B., Kumar, S., editors. The Timetree of Life. New York: Oxford University Press. 116–120. Dick, M.W., 2001. Straminipilous fungi. Systematics of the Peronosporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and similar organisms. Dordrecht, Boston, London: Kluwer Academic Publishers. 670 p. Dotzler, N., Krings, M., Agerer, R., Galtier, J., Taylor, T.N., 2008. Combresomyces cornifer gen. sp. nov., an endophytic peronosporomycete in Lepidodendron from the Carboniferous of central France. Mycological Research, 112, 1107–1114. Krings, M., Taylor, T.N., Galtier, J., Dotzler, N., 2010. A fossil peronosporomycete oogonium with an unusual surface ornament from the Carboniferous of France. Fungal Biology, 114, 446–450. Krings, M., Taylor, T.N., Dotzler, N., 2011. The fossil record of the Peronosporomycetes (Oomycota). Mycologia, 103, 445–457. Matari, N.H. and Blair, J.E., 2014. A multilocus timescale for oomycete evolution estimated under three distinct molecular clock models. BMC evolutionary biology, 14, 1–11. McLoughlin, S., Slater, B., Hilton, J., Prevec, R., 2011. New vistas on animal-plant-fungal interactions in the Permian-Triassic of Gondwana. GFF, 133, 66–67. McLoughlin, S., Drinnan, A.N., Slater, B.J., Hilton, J., 2015. Paurodendron stellatum: a new Permian permineralized herbaceous lycopsid from the Prince Charles Mountains, Antarctica. Review of Palaeobotany and Palynology, In press. Schwendemann, A.B., Taylor, T.N., Taylor, E.L., Krings, M., Dotzler, N., 2009. Combresomyces cornifer from the Triassic of Antarctica: evolutionary stasis in the Peronosporomycetes. Review of Palaeobotany and Palynology, 154, 1–5. Slater, B.J., McLoughlin, S., Hilton, J., 2011. Guadalupian (Middle Permian) megaspores from a permineralised peat in the Bainmedart Coal Measures, Prince Charles Mountains, Antarctica. Review of Palaeobotany and Palynology, 167, 140–155. Slater, B.J., McLoughlin, S., Hilton, J., 2012. Animal–plant interactions in a middle Permian permineralised peat of the Bainmedart Coal Measures, Prince Charles Mountains, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology, 363, 109–126. 10th New Phytologist Workshop, Natural History Museum, London, 2014 Slater, B.J., McLoughlin, S., Hilton, J., 2013. Peronosporomycetes (Oomycota) from a Middle Permian permineralised peat within the Bainmedart Coal Measures, Prince Charles Mountains, Antarctica. PloS one, 8, e70707. Slater, B.J., McLoughlin, S., Hilton, J., 2014. A high-latitude Gondwanan lagerstätte: the Permian permineralised peat biota of the Prince Charles Mountains, Antarctica. Gondwana Research, 27, 1446–1473. Strullu-Derrien, C., Kenrick, P., Rioult, J.P., Strullu, D.G., 2011. Evidence of parasitic Oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern Lyginopteris oldhamia. Proceedings of the Royal Society London B, 278, 675–680. Taylor, T.N., Krings, M., Kerp, H., 2006. Hassiella monospora gen. et sp. nov., a microfungus from the 400 million year old Rhynie Chert. Mycological Research, 110, 628–632. Taylor, T.N., Krings, M., Dotzler, N., Galtier, J., 2011. The advantage of thin section preparations over acetate peels in the study of late Paleozoic fungi and other microorganisms. PALAIOS, 26, 239–244. .
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