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Probable Proterozoic fungi

Published online by Cambridge University Press:  08 April 2016

Nicholas J. Butterfield
Nicholas J. Butterfield*
Affiliation:
Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom. E-mail: njb1005@esc.cam.ac.uk
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Abstract

A large, morphologically heterogeneous population of acanthomorphic acritarchs from the early Neoproterozoic Wynniatt Formation, Victoria Island, northwestern Canada, is ascribed to two form-genera, Tappania and Germinosphaera, but just a single natural taxon, Tappania. Analysis of Tappania morphology shows it to have been an actively growing, benthic, multicellular organism capable of substantial differentiation. Most notably, its septate, branching, filamentous processes were capable of secondary fusion, a synapomorphy of the “higher fungi.” Combined with phylogenetic, taphonomic and functional morphologic evidence, such “hyphal fusion” identifies Tappania reliably, if not conclusively, as a fungus, probably a sister group to the “higher fungi,” but more derived than the zygomycetes.

The presence of Tappania in the Mesoproterozoic Roper Group of Australia extends the record of putative fungi to 1430 Ma. Along with other Proterozoic acritarchs exhibiting fungus-like characteristics (e.g., Trachyhystrichosphaera, Shuiyousphaeridium, Dictyosphaera, Foliomorpha), there is a case to be made for an extended and relatively diverse record of Proterozoic fungi.

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Articles
Information
Paleobiology , Volume 31 , Issue 1 , Winter 2005 , pp. 165 - 182
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Ahrén, D., Ursing, B. M., and Tunlid, A. 1998. Phylogeny of nematode-trapping fungi based on 18S rDNA sequences. FEMS Microbiology Letters 158:179–184.CrossRefGoogle ScholarPubMed
Asmerom, Y., Jacobsen, S. B., Knoll, A. H., Butterfield, N. J., and Swett, K. 1991. Strontium isotopic variations of Neoproterozoic seawater: implications for crustal evolution. Geochimica et Cosmochimica Acta 55:2883–2894.Google Scholar
Barron, G. L. 1981. Predators and parasites of microscopic animals. Pp. 167–200in Cole, G. T. and Kendrick, B., eds. Biology of conidial fungi, Vol. 2. Academic Press, New York.Google Scholar
Bengtson, S., and Zhao, Y. 1992. Predatorial borings in late Precambrian mineralized exoskeletons. Science 257:367–369.Google Scholar
Blackwell, M. 2000. Terrestrial life—fungal from the start? Science 289:1884–1885.CrossRefGoogle ScholarPubMed
Boyce, C. K., Hotton, C., Fogel, M. L., Cody, G. D., Hazen, R. M., and Knoll, A. H. 2003. Comparative geochemistry suggests Prototaxites was a gigantic fungus. Geological Society of America Abstracts with Programs 35:587.Google Scholar
Budd, G. E., and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75:253–295.CrossRefGoogle ScholarPubMed
Burnett, J. H. 1976. Fundamentals of mycology, 2d ed.Edward Arnold, London.Google Scholar
Burzin, M. B. 1993. Drevneishii khitridiomitset (Mycota, Chytridiomycetes incertae sedis) iz verkhnego Venda Vostochno-Evropeiskoi Platformy. Pp. 21–33in Sokolov, B. S. and Ivanovskii, A. B., eds. Fauna i Ekosistemy Geologicheskogo Proshlogo. Nauka, Moscow.Google Scholar
Butterfield, N. J. 1997. Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23:247–262.Google Scholar
Butterfield, N. J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404.Google Scholar
Butterfield, N. J. 2001. Ecology and evolution of the Cambrian plankton. Pp. 200–216in Zhuravlev, A. Yu. and Riding, R., eds. Ecology of the Cambrian Radiation. Columbia University Press, New York.Google Scholar
Butterfield, N. J. 2003. Exceptional fossil preservation and the Cambrian Explosion. Integrative and Comparative Biology 43:166–177.Google Scholar
Butterfield, N. J. 2004 A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Paleobiology 30:231–252.Google Scholar
Butterfield, N. J., and Chandler, F. W. 1992. Paleoenvironmental distribution of Proterozoic microfossils, with an example from the Agu Bay Formation, Baffin Island. Palaeontology 35:943–957.Google Scholar
Butterfield, N. J., and Rainbird, R. H. 1998. Diverse organic-walled microfossils, including “possible dinoflagellates,” from the early Neoproterozoic of arctic Canada. Geology 26:963–966.Google Scholar
Butterfield, N. J., Knoll, A. H., and Swett, K. 1994. Paleobiology of the Neoproterozoic Svanbergfjellet Formation, Spitsbergen. Fossils and Strata 34:1–84.Google Scholar
Cavalier-Smith, T. 2001. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. International Journal of Systematic and Evolutionary Microbiology 52:7–76.Google Scholar
Cavalier-Smith, T., and Chao, E. E. Y. 2003. Phylogeny of Choanozoa, Apusozoa, and other protozoa and early eukaryote megaevolution. Journal of Molecular Evolution 56:540–563.Google Scholar
Currah, R. S. 1985. Taxonomy of the Onygenales—Arthrodermataceae, Gymnoascaceae, Myxotrichaceae and Onygenaceae. Mycotaxon 24:1–216.Google Scholar
Darby, D. G. 1974. Reproductive modes of Huroniospora micro-reticulata from cherts of the Precambrian Gunflint Iron-Formation. Geological Society of America Bulletin 85:1595–1596.Google Scholar
Evitt, W. R. 1963. A discussion and proposals concerning fossil dinoflagellates, hystrichospheres, and acritarchs. II. Proceedings of the National Academy of Sciences USA 49:298–302.Google Scholar
Fritsch, F. E. 1945. The structure and reproduction of the algae, Vol. 2. Cambridge University Press, London.Google Scholar
Galagan, J. E., and 76 others. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868.Google Scholar
Glass, N. L., Jacobson, D. J., and Shiu, P. K. T. 2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annual Review of Genetics 34:165–186.CrossRefGoogle ScholarPubMed
Gorbushina, A. A., Whitehead, K., Dornieden, T., Niesse, A., Schulte, A., and Hedges, J. I. 2003. Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock-dwelling microcolonial fungi. Canadian Journal of Botany 81:131–138.CrossRefGoogle Scholar
Gregory, P. H. 1984. The fungal mycelium: an historical perspective. Transactions of the British Mycological Society 82:1–11.Google Scholar
Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., and Hedges, S. B. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133.Google Scholar
Hedges, S. B., Blair, J. E., Venturi, M. L., and Shoe, J. L. 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evolutionary Biology doi: 10.1186/1471-2148-4-2.Google Scholar
Heinlein, M. 2002. Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Current Opinion in Plant Biology 5:543–552.Google Scholar
Hermann, T. N. 1979. Nakhodki gribov v Rifee (Discoveries of fungi in the Riphean). Pp. 129–136in Sokolov, B. S., ed. Paleontologiia Dokembriia I Rannego Kembriia. Nauka, Leningrad.Google Scholar
Hickey, P. C., Jacobson, D. J., Read, N. D., and Glass, N. L. 2002. Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genetics and Biology 37:109–119.Google Scholar
Hofmann, H. J., and Rainbird, R. H. 1995. Carbonaceous megafossils from Neoproterozoic Shaler Supergroup, Victoria Island, Arctic Canada. Palaeontology 37:72–731.Google Scholar
Hua, H., Pratt, B. R., and Zhang, L.-Y. 2003. Borings in Cloudina shells: complex predator-prey dynamics in the terminal Proterozoic. Palaios 18:454–459.Google Scholar
Hueber, F. M. 2001. Rotted wood-alga-fungus: the history and life of Prototaxites Dawson 1859. Review of Palaeobotany and Palynology 116:123–158.Google Scholar
Javaux, E. J., Knoll, A. H., and Walter, M. R. 2001. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412:66–69.CrossRefGoogle ScholarPubMed
Javaux, E. J., Knoll, A. H., and Walter, M. R. 2003. Recognizing and interpreting the fossils of early eukaryotes. Origins of Life and Evolution of the Biosphere 33:75–94.Google Scholar
Jones, E. B. G., Johnson, R. G., and Moss, S. T. 1986. Taxonomic studies of the Halosphaeriaceae—philosophy and rationale for the selection of characters in the delineation of genera. Pp. 211–229in Moss, 1986.Google Scholar
Kaufman, A. J., and Xiao, S. 2003. High CO2 levels in the Proterozoic atmosphere estimated from analyses of individual microfossils. Nature 425:279–282.Google Scholar
Kázmierczak, J. 1975. Colonial Volvocales (Chlorophyta) from the Upper Devonian of Poland and their palaeoenvironmental significance. Acta Palaeontologica Polonica 20:73–85.Google Scholar
Knoll, A. H. 1994. Proterozoic and Early Cambrian protists: evidence for accelerating evolutionary tempo. Proceedings of the National Academy of Sciences USA 91:6743–6750.Google Scholar
Knoll, A. H., and Butterfield, N. J. 1989. New window on Proterozoic life. Nature 337:602–603.Google Scholar
Kohlmeyer, J. 1986. Taxonomic studies of the marine Ascomycotina. Pp. 199–210in Moss, 1986.Google Scholar
Kohlmeyer, J., and Volkmann-Kohlmeyer, B. 2003. Marine ascomycetes from algae and animal hosts. Botanica Marina 46:285–306.Google Scholar
Kohlmeyer, J., Spatafora, J. W., and Volkmann-Kohlmeyer, B. 2000. Lulworthiales, a new order of marine Ascomycota. Mycologia 92:453–458.Google Scholar
Kokinos, J. P., and Anderson, D. M. 1995. Morphological development of resting cysts in cultures of the marine dinoflagellate Linglodinium polyedrum (= L. machaerophorum). Palynology 19:143–166.Google Scholar
Kumar, S. 2001. Mesoproterozoic megafossil Chuaria-Tawuia association may represent parts of a multicellular plant, Vindyan Supergroup, Central India. Precambrian Research 106:187–211.Google Scholar
Landvik, S., Eriksson, O. E., and Berbee, M. L. 2001. Neolecta—a fungal dinosaur? Evidence from β-tubulin amino acid sequences. Mycologia 93:1151–1163.Google Scholar
Lentin, J. K., Fensome, R. A., and Williams, G. L. 1994. The stratigraphic importance of species of Sumatradinium, Barssidinium, and Erymnodinium, Neogene dinoflagellate genera from offshore eastern Canada. Canadian Journal of Earth Sciences 31:567–582.Google Scholar
Liu, Y. J., and Hall, B. D. 2004. Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proceedings of the National Academy of Sciences USA 101:4507–4512.Google Scholar
Martin, W., Rotte, C., Hoffmeister, M., Theissen, U., Gelius-Dietrich, G., Ahr, S., and Henze, K. 2003. Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55:193–204.Google Scholar
McCabe, P. M., Gallagher, M. P., and Deacon, J. W. 1999. Microscopic observation of perfect hyphal fusion in Rhizoctonia solani. Mycological Research 103:487–490.CrossRefGoogle Scholar
Medlin, L. K., Kooistra, W. H. C. F., Potter, D., Saunders, G. W., and Andersen, R. A. 1997. Phylogenetic relationships of the ‘golden algae’ (haptophytes, heterokont chromophytes) and their plastids. Plant Systematics and Evolution 11(Suppl.):187–219.Google Scholar
Mendelson, C. V., and Schopf, J. W. 1992. Proterozoic and Early Cambrian acritarchs. Pp. 219–232in Schopf, J. W. and Klein, C., eds. The Proterozoic biosphere. Cambridge University Press, Cambridge.Google Scholar
Mendoza, L., Taylor, J. W., and Ajello, L. 2002. The Class Mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annual Review of Microbiology 56:315–344.Google Scholar
Michod, R. E. 1997. Evolution of the individual. American Naturalist 150:S5–S21.Google Scholar
Moss, S. T., ed. 1986. The biology of marine fungi. Cambridge University Press, Cambridge.Google Scholar
Nakagiri, A., and Tubaki, K. 1986. Ascocarp peridial wall structure in Corollospora and allied genera of Halosphaeriaceae. Pp. 245–251in Moss, 1986.Google Scholar
Pawlowski, J., Holzmann, M., Berney, C., Fahrni, J., Gooday, A. J., Cedhagen, T., Habura, A., and Bowser, S. S. 2003. The evolution of early Foraminifera. Proceedings of the National Academy of Sciences USA 100:11494–11498.Google Scholar
Peterson, K. J., Waggoner, B., and Hagadorn, J. W. 2003. A fungal analog for Newfoundland Ediacaran fossils? Integrative and Comparative Biology 43:127–136.Google Scholar
Porter, S. M., and Knoll, A. H. 2000. Testate amoebae in the Neoproterozoic era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology 26:360–385.Google Scholar
Porter, S. M., Meisterfeld, R., and Knoll, A. H. 2003. Vase-shaped microfossils from the Neoproterozoic Chuar Group, Grand Canyon: a classification guided by modern testate amoebae. Journal of Paleontology 77:409–429.Google Scholar
Rainbird, R. H., Jefferson, C. W., and Young, G. M. 1996. The early Neoproterozoic sedimentary Succession B of northwestern Laurentia: correlations and paleogeographic significance: Geological Society of America Bulletin 108:454–470.Google Scholar
Redecker, D. 2002. New views on fungal evolution based on DNA markers and the fossil record. Research in Microbiology 153:125–130.Google Scholar
Redecker, D., Kodner, R., and Graham, L. E. 2000. Glomalean fungi from the Ordovician. Science 289:1920–1921.Google Scholar
Retallack, G. J. 1994. Were the Ediacaran fossils lichens? Paleobiology 20:523–544.Google Scholar
Samuelsson, J., and Butterfield, N. J. 2001. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambrian Research 107:235–251.Google Scholar
Schatz, S. 1983. The developmental morphology and life history of Phycomelaina laminariae. Mycologia 76:762–772.Google Scholar
Schopf, J. W. 1968. Microflora of the Bitter Springs Formation, late Precambrian, Central Australia. Journal of Paleontology 42:651–688.Google Scholar
Schopf, J. W., and Barghoorn, E. S. 1969. Microorganisms from the late Precambrian of South Australia. Journal of Paleontology 43:111–118.Google Scholar
Sherwood-Pike, M. A., and Gray, J. 1985. Silurian fungal remains: probable records of the Class Ascomycetes. Lethaia 18:1–20.Google Scholar
Spanggaard, B., Huss, H. H., and Brescianni, J. 1995. Morphology of Ichthyophonus hoferi assessed by light and scanning electron microscopy. Journal of Fish Diseases 18:567–577.Google Scholar
Stanley, S. M. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences USA 70:1486–1489.Google Scholar
Talyzina, N. M., Moldowan, J. M., Johannisson, A., and Fago, F. J. 2000. Affinities of Early Cambrian acritarchs studied by using microscopy, fluorescence flow cytometry and biomarkers. Review of Palaeobotany and Palynology 108:37–53.Google Scholar
Taylor, T. N., and Taylor, E. L. 1997. The distribution and interactions of some Paleozoic fungi. Review of Palaeobotany and Palynology 95:83–94.Google Scholar
Taylor, T. N., Hass, H., and Kerp, H. 1999. The oldest fossil ascomycetes. Nature 399:648.Google Scholar
Timoféev, B. V. 1970. Une découverte de Phycomycetes dans le Précambrien. Review of Palaeobotany and Palynology 10:79–81.Google Scholar
Vidal, G., and Moczydlowska-Vidal, M. 1997. Biodiversity, speciation, and extinction trends of Proterozoic and Cambrian phytoplankton. Paleobiology 23:230–246.Google Scholar
Xiang, X., and Morris, N. R. 1999. Hyphal tip growth and nuclear migration. Current Opinion in Microbiology 2:636–640.Google Scholar
Xiao, S., and Knoll, A. H. 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32:219–240.Google Scholar
Xiao, S., and Knoll, A. H. 2000. Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng'an, Guizhou, South China. Journal of Paleontology 74:767–788.Google Scholar
Xiao, S., Knoll, A. H., Kaufman, A. J., Yin, L., and Zhang, Y. 1997. Neoproterozoic fossils in Mesoproterozoic rocks? Chemostratigraphic resolution of a biostratigraphic conundrum from the North China Platform. Precambrian Research 84:197–220.Google Scholar
Yan, Yu-zhong, and Shi-xing, Zhu 1992. Discovery of acanthomorphic acritarchs from the Baicaoping Formation in Yongji, Shanxi and its geological significance. Acta Micropalaeontologica Sinica 9:267–282.Google Scholar
Yin, C., Bengtson, S., and Zhao, Y. 2004. Silicified and phosphatized Tianzhushania, spheroidal microfossils of possible animal origin from the Neoproterozoic of South China. Acta Palaeontologica Polonica 49:1–12.Google Scholar
Yin, L. 1997. Acanthomorphic acritarchs from Meso-Neoproterozoic shales of the Ruyang Group, Shanxi, China. Review of Palaeobotany and Palynology 98:15–25.Google Scholar
Zhang, Y., Yin, L., Xiao, S., and Knoll, A. H. 1998. Permineralized fossils from the Terminal Proterozoic Doushantuo Formation, South China. Paleontological Society Memoir 50 (Journal of Paleontology 72 (4) supplement), 52 pp.Google Scholar
Zhou, Chuanming, Brasier, M. D., and Yaosong, Xue 2001. Three-dimensional phosphatic preservation of giant acritarchs from the terminal Proterozoic Doushantuo Formation in Guizhou and Hubei provinces, South China. Palaeontology 44:1157–1178.Google Scholar