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Microfossils from the Lower Devonian Rhynie Chert with suggested affinities to the peronosporomycetes

Published online by Cambridge University Press:  20 May 2016

Michael Krings
Affiliation:
Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, and Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, Munich 80333, Germany, ; Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence KS 66045-7534, USA, ; ;
Thomas N. Taylor
Affiliation:
Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence KS 66045-7534, USA, ; ;
Edith L. Taylor
Affiliation:
Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence KS 66045-7534, USA, ; ;
Hans Kerp
Affiliation:
Forschungsstelle für Paläobotanik am Geologisch-Paläontologischen Institut, Westfälische Wilhelms-Universität Münster, Hindenburgplatz 57, Münster 48143, Germany, ;
Hagen Hass
Affiliation:
Forschungsstelle für Paläobotanik am Geologisch-Paläontologischen Institut, Westfälische Wilhelms-Universität Münster, Hindenburgplatz 57, Münster 48143, Germany, ;
Nora Dotzler
Affiliation:
Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, and Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, Munich 80333, Germany, ;
Carla J. Harper
Affiliation:
Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence KS 66045-7534, USA, ; ;

Abstract

A conspicuous silicified microfossil, Frankbaronia polyspora n. gen. n. sp., occurs in plant litter and as an inhabitant of microbial mats from the Lower Devonian Rhynie chert, Aberdeenshire, Scotland. Specimens are elongate-cylindrical, oval, or spherical, thin-walled, and may possess conical or column-like surface projections. Most specimens occur isolated, some are arranged in pairs or short chains. Each specimen contains several small spheres, each in turn with a (sub)centric opaque inclusion. Immature specimens indicate that ontogenesis in this fossil includes the formation of a single centric body of opaque material that subsequently is apportioned among the developing small spheres. Frankbaronia polyspora is quite similar in size and morphology to the oogonia containing oospores seen in certain extant members of the Peronosporomycetes. The Rhynie chert is known to contain the oldest fossil evidence of the Peronosporomycetes but only a single form (Hassiella monospora) has previously been documented. The discovery of a second putative representative of this group of organisms proves that this paleoecosystem is still an important source of new information on the paleodiversity of microbial life.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

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References

Alberghina, J. S., Vélez, C. G., and Vigna, M. S. 2009. The oogonial aperture of Oedogonium decipiens var. decipiens (Oedogoniales, Chlorophyta) and its systematic significance. Plant Systematics and Evolution, 280:99104.CrossRefGoogle Scholar
Baschnagel, R. A. 1966. New fossil algae from the Middle Devonian of New York. Transactions of the American Microscopical Society, 85:297302.Google Scholar
Beakes, G. W. and Gay, J. L. 1978. Light and electron microscopy of oospore maturation in Saprolegnia furcata. Transactions of the British Mycological Society, 71:2535.Google Scholar
Beakes, G. W. and Sekimoto, S. 2009. The evolutionary phylogeny of Oomycetes—insights gained from studies of holocarpic parasites of algae and invertebrates, p. 124. InLamour, K. and Kamoun, S.(eds.), Oomycete Genetics and Genomics: Diversity, Interactions, and Research Tools. John Wiley & Sons, Inc., Hoboken, New Jersey.Google Scholar
Bhattacharya, D., Yoon, H. S., Hedges, S. B., and Hackett, D. 2009. Eukaryotes, p. 116120. InHedges, S. B. and Kumar, S.(eds.), The Timetree of Life. Oxford University Press, Oxford, UK.Google Scholar
Bian, L. and Liu, Z. 1999. Discovery of Late Ordovician algal fossils of Oedogoniales in Jiangxi Province, China. Acta Palaeontologica Sinica, 38:4649. (In Chinese)Google Scholar
Canter, H. M. and Dick, M. W. 1994. Eurychasmopsis multisecunda gen. et sp. nov., a parasite of the suctorian ciliate Podophyra. Mycological Research, 98:105117.Google Scholar
Cavalier-Smith, T. 1986. The kingdom Chromista: origin and systematics, p. 309347. InRound, F. E. and Chapman, D. J.(eds.), Progress in Phycological Research, vol. 4. Biopress Ltd, Bristol.Google Scholar
Coker, W. C. and Hyman, O. W. 1912. Thraustotheca clavata. Mycologia, 4:8790.Google Scholar
Croft, W. N. and George, E. A. 1959. Blue-green algae from the Middle Devonian of Rhynie, Aberdeenshire. Bulletin of the British Museum of Natural History, Geology, 3:341353.Google Scholar
Davis, B. M. 1903. Oogenesis in Saprolegnia. Botanical Gazette, 35:233249, 320–349.Google Scholar
Dick, M. W. 1972. Morphology and taxonomy of the Oomycetes, with special reference to Saprolegniaceae, Leptomitaceae, and Pythiaceae. II. Cytogenetic systems. New Phytologist, 71:11511159.Google Scholar
Dick, M. W. 1986. A new family and a new genus for two taxa previously assigned to Apodachlyella completa (J. E. Humphrey) H. Indoh (Peronosporomycetidae: Leptomitales). Botanical Journal of the Linnean Society, 93:225229.Google Scholar
Dick, M. W. 1995. Sexual reproduction in the Peronosporomycetes (chromistan fungi). Canadian Journal of Botany, 73 (Supplement 1):S712S724.Google Scholar
Dick, M. W. 2001. Straminipilous Fungi: Systematics of the Peronosporomycetes Including Accounts of the Marine Straminipilous Protists, the Plasmodiophorids and Similar Organisms. Kluwer Academic Publishers, Dordrecht, 670 p.Google Scholar
Dotzler, N., Taylor, T. N., and Krings, M. 2007. A prasinophycean alga of the genus Cymatiosphaera in the Early Devonian Rhynie chert. Review of Palaeobotany and Palynology, 147:106111.Google Scholar
Dotzler, N., Krings, M., Agerer, R., Galtier, J., and Taylor, T. N. 2008. Combresomyces cornifer gen. sp. nov., an endophytic peronosporomycete in Lepidodendron from the Carboniferous of central France. Mycological Research, 112:11071114.CrossRefGoogle Scholar
Dotzler, N., Walker, C., Krings, M., Hass, H., Kerp, H., Taylor, T. N., and Agerer, R. 2009. Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycological Progress, 8:918.Google Scholar
Drechsler, C. 1930. Some new species of Pythium. Journal of the Washington Academy of Sciences, 20:398418.Google Scholar
Duncan, J. M. 1977. Germination in vitro of Phythophthora fragariae oospores from infected root tissue. Transactions of the British Mycological Society, 69:391395.Google Scholar
Edwards, D. S. and Lyon, A. G. 1983. Algae from the Rhynie chert. Botanical Journal of the Linnean Society, 86:3755.Google Scholar
Ettl, H. 1988. Über Definitionen und Terminologie der asexuellen Fortpflanzungszellen bei Grünalgen (Chlorophyta). Archiv für Protistenkunde, 135:1734.Google Scholar
Fayers, S. R. and Trewin, N. H. 2004. A review of the palaeoenvironments and biota of the Windyfield chert. Transactions of the Royal Society of Edinburgh, Earth Sciences, 94:395408.Google Scholar
Flanagan, P. W. 1970. Meiosis and mitosis in Saprolegniaceae. Canadian Journal of Botany, 48:20692076.Google Scholar
Fletcher, J. 1978. Timing of events during oospore genesis in Saprolegnia diclina. Transactions of the British Mycological Society, 70:417422.Google Scholar
Graham, L. E. and Wilcox, L. W. 2000. Algae. Prentice Hall, Inc., Upper Saddle River, New Jersey, 640 p.Google Scholar
Hass, H., Taylor, T. N., and Remy, W. 1994. Fungi from the Lower Devonian Rhynie chert: mycoparasitism. American Journal of Botany, 81:2937.Google Scholar
Heath, I. B. and Greenwood, A. D. 1970. Wall formation in the Saprolegniales. II. Formation of cysts by the zoospores of Saprolegnia and Dictyuchus. Archiv für Mikrobiologie, 75:6779.Google Scholar
Hirn, K. E. 1900. Monographie und Iconographie der Oedogoniaceen. Acta Societatis Scientiarum Fennicae, 27:1394.Google Scholar
Howard, K. L. 1971. Oöspore types in the Saprolegniaceae. Mycologia, 63:679686.Google Scholar
Howard, K. L. and Moore, R. T. 1970. Ultrastructure of oogenesis in Saprolegnia terrestris. Botanical Gazette, 131:311336.Google Scholar
Humphrey, J. E. 1893. The Saprolegniaceae of the United States. Transactions of the American Philosophical Society, 17:1148.Google Scholar
Indoh, H. 1939. Studies on the Japanese aquatic fungi. I. On Apodachlyella completa sp. nov. with revision of the Leptomitaceae. Science Reports of the Tokyo Bunrika Daigaku, Section B, 4:4350.Google Scholar
Johnson, T. W. 1949. A new species of Achlya with coiled oogonial stalks. Mycologia, 41:678685.Google Scholar
Johnson, T. W., Seymour, R. L., and Padgett, D. E. 2002. Biology and systematics of the Saprolegniaceae. Published online at:http://dl.uncw.edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book/ (last accessed 10, September 2010).Google Scholar
Kanouse, B. B. 1932. A physiological and morphological study of Saprolegnia parasitica. Mycologia, 24:431452.Google Scholar
Karling, J. S. 1942. A new chytrid with giant zoospores: Septochytrium macrosporum sp. nov. American Journal of Botany, 29:616622.Google Scholar
Karling, J. S. 1977. Chytridiomycetarum Iconographia. An Illustrated and Brief Descriptive Guide to the Chytridiomycetous Genera with a Supplement of the Hyphochytridiomycetes. J. Cramer, Vaduz, viii + 414 p.Google Scholar
Kaźmierczak, J. and Kremer, B. 2009. Spore-like bodies in some early Paleozoic acritarchs: Clues to chlorococcalean affinities. Acta Palaeontologica Polonica, 54:541551.Google Scholar
Kerp, H. and Hass, H. 2004. De Onder-Devonische Rhynie Chert – het oudste en meest compleet bewaard gebleven terrestrische ecosysteem. Grondboor en Hamer, 58:3350.Google Scholar
Kerp, H. and Hass, H. 2009. Ökologie und Reproduktion der frühen Landpflanzen. Berichte der Reinhold-Tüxen-Gesellschaft, 21:111127.Google Scholar
Kidston, R. and Lang, W. H. 1921. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part V. The Thallophyta occurring in the peat-bed; the succession of the plants throughout a vertical section of the bed, and the conditions of accumulation and preservation of the deposit. Transactions of the Royal Society of Edinburgh, 52:855902.Google Scholar
Kitancharoen, N., Yuasa, K., and Hatai, K. 1995. Morphological aspects of Saprolegnia diclina Type 1 isolated from pejerrey, Odonthetes bonariensis. Mycoscience, 36:365368.CrossRefGoogle Scholar
Krings, M., Kerp, H., Hass, H., Taylor, T. N., and Dotzler, N. 2007. A filamentous cyanobacterium showing structured colonial growth from the Early Devonian Rhynie chert. Review of Palaeobotany and Palynology, 146:265276.Google Scholar
Krings, M., Dotzler, N., and Taylor, T. N. 2009a. Globicultrix nugax nov. gen. et nov. spec. (Chytridiomycota), an intrusive microfungus in fungal spores from the Rhynie chert. Zitteliana A, 48/49:165170.Google Scholar
Krings, M., Hass, H., Kerp, H., Taylor, T. N., Agerer, R., and Dotzler, N. 2009b. Endophytic cyanobacteria in a 400-million-yr-old land plant: A scenario for the origin of a symbiosis? Review of Palaeobotany and Palynology, 153:6269.Google Scholar
Krings, M., Dotzler, N., Longcore, J. E., and Taylor, T. N. 2010a. An unusual microfungus in a fungal spore from the Lower Devonian Rhynie chert. Palaeontology, 53:753759.Google Scholar
Krings, M., Taylor, T. N., Galtier, J., and Dotzler, N. 2010b. A fossil peronosporomycete oogonium with an unusual surface ornament from the Carboniferous of France. Fungal Biology, 114:446450.Google Scholar
Krings, M., Taylor, T. N., and Dotzler, N. 2011. The fossil record of the Peronosporomycetes (Oomycota). Mycologia, 103:445457.Google Scholar
Leitgeb, H. 1869. Neue Saprolegnieen. Jahrbücher für wissenschaftliche Botanik, 7:357389.Google Scholar
Lévesque, C. A. 2011. Fifty years of oomycetes – from consolidation to evolutionary and genomic exploration. Fungal Diversity, 50:3546.Google Scholar
Mahato, A. K. 1999. A new species of Oedogonium (Chlorophyllaceae, Oedogoniales) from Bihar, India. Feddes Repertorium, 110:173176.Google Scholar
Middleton, J. T. 1943. The taxonomy, host range and geographic distribution of the genus Pythium. Memoirs of the Torrey Botanical Club, 20:1171.Google Scholar
Nakagiri, A., Okane, I., and Ito, T. 1998. Zoosporangium development, zoospore release and culture properties of Halophytophthora mycoparasitica. Mycoscience, 39:223230.Google Scholar
Nees Von Esenbeck, C. G. 1823. Zusatz. Appended to CARUS, C. G. 1823. Beitrag zur Geschichte der unter Wasser an verwesenden Tierkörpern sich erzeugenden Schimmel- oder Algen-Gattungen. Nova Acta Physico-Medica Academiae Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosum, 11 (2):507522.Google Scholar
Parry, S. F., Noble, S. R., Crowley, Q. G., and Wellman, C. H. 2011. A high-precision U-Pb age constraint on the Rhynie chert Konservat-Lagerstätte: time scale and other implications. Journal of the Geological Society, London, 168:863872.Google Scholar
Paul, B. and Steciow, M. M. 2004. Saprolegnia multispora, a new oomycete isolated from water samples taken in a river in the Burgundian region of France. FEMS Microbiology Letters, 237:393398.Google Scholar
Pieters, A. J. 1915. New species of Achlya and Saprolegnia. Botanical Gazette, 60:483490.Google Scholar
Pirozynski, K. A. 1976. Fossil fungi. Annual Review of Phytopathology, 14:237246.Google Scholar
Prabhuji, S. K. 2010. Sexual reproduction in water molds – I: General aspects related to family Saprolegniaceae. International Journal of Plant Reproductive Biology, 2:1730.Google Scholar
Pringsheim, N. 1858. Beiträge zur Morphologie und Systematik der Algen. 2. Die Saprolegnieen. Jahrbücher für wissenschaftliche Botanik, 1:284306.Google Scholar
Remy, W., Taylor, T. N., and Hass, H. 1994. Early Devonian fungi: a blastocladalean fungus with sexual reproduction. American Journal of Botany, 81:690702.Google Scholar
Rice, C. A. and Ashcroft, W. A. 2004. The geology of the northern half of the Rhynie basin, Aberdeenshire, Scotland. Transactions of the Royal Society of Edinburgh, Earth Sciences, 94:299308.Google Scholar
Rice, C. M., Trewin, N. H., and Anderson, L. I. 2002. Geological setting of the Early Devonian Rhynie cherts, Aberdeenshire, Scotland: An early terrestrial hot spring system. Journal of the Geological Society of London, 159:203214.Google Scholar
Riding, R. and Braga, J. C. 2005. Halysis H⊘eg, 1932 – an Ordovician coralline red alga? Journal of Paleontology, 79:835841.Google Scholar
Seymour, R. L. 1970. The genus Saprolegnia. Nova Hedwigia, 19:1124.Google Scholar
Strullu-Derrien, C., Kenrick, P., Rioult, J. P., and 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, Series B, 278:675680.Google Scholar
Taylor, T. N., Remy, W., and Hass, H. 1992. Fungi from the Lower Devonian Rhynie chert: Chytridiomycetes. American Journal of Botany, 79:12331241.Google Scholar
Taylor, T. N., Remy, W., Hass, H., and Kerp, H. 1995. Fossil arbuscular mycorrhizae from the Early Devonian. Mycologia, 87:560573.Google Scholar
Taylor, T. N., Klavins, S. D., Krings, M., Taylor, E. L., Kerp, H., and Hass, H. 2004. Fungi from the Rhynie chert: A view from the dark side. Transactions: Earth Sciences, 94:457473.Google Scholar
Taylor, T. N., Hass, H., Kerp, H., Krings, M., and Hanlin, R. T. 2005. Perithecial ascomycetes from the 400 million year old Rhynie Chert: An example of ancestral polymorphism. Mycologia, 97:269285.Google Scholar
Taylor, T. N., Krings, M., and Kerp, H. 2006. Hassiella monospora gen. et sp. nov., a microfungus from the 400 million year old Rhynie chert. Mycological Research, 110:628632.Google Scholar
Tiffany, L. H. 1936. The Oedogoniales. Botanical Review, 2:456473.Google Scholar
Trewin, N. H. and Rice, C. M., eds. 2004. The Rhynie hot-spring system: geology, biota and mineralisation. Transactions of the Royal Society of Edinburgh, Earth Sciences, 94:285521.Google Scholar
Van Der Plaats-Niterink, A. J. 1981. Monograph of the genus Pythium. Studies in Mycology, 21:1242.Google Scholar
Wellman, C. H. 2006. Spore assemblages from the Lower Devonian ‘Lower Old Red Sandstone’ deposits of the Rhynie outlier, Scotland. Transactions of the Royal Society of Edinburgh, Earth Sciences, 97:167211.Google Scholar
Wellman, C. H., Kerp, H., and Hass, H. 2006. Spores of the Rhynie chert plant Aglaophyton (Rhynia) major (Kidston and Lang) D.S. Edwards, 1986. Review of Palaeobotany and Palynology, 142:229250.Google Scholar
Weston, W. H. 1918. The development of Thraustotheca, a peculiar water-mould. Annals of Botany, 32 155173.Google Scholar
Ziegler, A. W. 1953. Meiosis in Saprolegniaceae. American Journal of Botany, 40:6066.Google Scholar
Zippi, P. A. 1998. Freshwater algae from the Mattagami Formation (Albian), Ontario: Paleoecology, botanical affinities, and systemjatic taxonomy. Micropaleontology, 44 (Supplement 1):178.Google Scholar