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Fungal intruders of enigmatic propagule clusters occurring in microbial mats from the Lower Devonian Rhynie chert

PalZ volume 93, pages 135–149 (2019)Cite this article

Abstract

Microbial mats in the Lower Devonian Rhynie chert represent diverse communities of organisms, which probably not only co-occurred in these structures, but also variously interacted with one another. However, little is known about these interactions. Three different types of fungi interact with clusters of small propagules that frequently occur within the Rhynie microbial mats. One of the fungi occurs in the form of small mycelia and single reproductive units within individual propagules, while the second is characterized by apophysate, epibiotic sporangia and multibranched rhizoidal systems that extend through the clusters and penetrate individual propagules. The third fungus consists of what is interpreted as a distal sporangium or spore from which a long, tubular stalk reaches into the propagule cluster. One specimen of the latter fungus occurs inside a specimen of the second fungus and, moreover, shows evidence suggestive of hyperparasitism in the form of conical callosities. This discovery supports the suggestion that microbial mats in the Rhynie paleoecosystem were complex structures based on the presence of numerous interactions between different organisms within the mats.

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References

  • Barr, D.J.S. 1970. Phlyctochytrium reinboldtae (Chytridiales): morphology and physiology. Canadian Journal of Botany 48: 479–484.

    Article  Google Scholar 

  • Barr, D.J.S. 1978. Taxonomy and phylogeny of chytrids. Biosystems 10: 153–165.

    Article  Google Scholar 

  • Barr, D.J.S. 1980. An outline for the reclassification of the Chytridiales, and for a new order, the Spizellomycetales. Canadian Journal of Botany 58: 2380–2394.

    Article  Google Scholar 

  • Barr, D.J.S. 1984. The classification of Spizellomyces, Gaertneriomyces, Triparticalcar, and Kochiomyces (Spizellomycetales, Chytridiomycetes). Canadian Journal of Botany 62: 1171–1201.

    Article  Google Scholar 

  • Barr, D.J.S., and C.J. Hickman. 1967. Chytrids and algae. I. Host-substrate range, and morphological variation of species of Rhizophydium. Canadian Journal of Botany 45: 423–430.

    Article  Google Scholar 

  • Beakes, G.W., and M. Thines. 2017. Hyphochytriomycota and Oomycota. In Handbook of the Protists, eds. J.M. Archibald, A.G.B. Simpson, C.H. Slamovits, L. Margulis, M. Melkonian, D.J. Chapman, and J.O. Corliss, 435–505. Cham: Springer International.

    Chapter  Google Scholar 

  • Blackwell, W.H., P.M. Letcher, and M.J. Powell. 2006. Thallus development and the systematics of Chytridiomycota: an additional developmental pattern represented by Podochytrium. Mycotaxon 97: 91–109.

    Google Scholar 

  • Błaszkowski, J., G.M. Kovács, and T. Balázs. 2009. Glomus perpusillum, a new arbuscular mycorrhizal fungus. Mycologia 101: 247–255.

    Article  Google Scholar 

  • Błaszkowski, J., G. Chwat, A. Góralska, P. Ryszka, and G.M. Kovács. 2015. Two new genera, Dominikia and Kamienskia, and D. disticha sp. nov. in Glomeromycota. Nova Hedwigia 100: 225–238.

    Article  Google Scholar 

  • Bomfleur, B., H. Kerp, T.N. Taylor, Ø. Moestrup, and E.L. Taylor. 2012. Triassic leech cocoon from Antarctica contains fossil bell animal. Proceedings of the National Academy of Sciences USA 109: 20971–20974.

    Article  Google Scholar 

  • Bracker, C.E., and L.J. Littlefield. 1973. Structural concepts of host-pathogen interfaces. In Fungal Pathogenicity and the Plant’s Response, eds. R.J.W. Byrde and C.V. Cutting, 159–318. London, New York, NY: Academic.

    Chapter  Google Scholar 

  • Brundrett, M.C., C. Walker, C.J. Harper, and M. Krings. 2018. Fossils of arbuscular mycorrhizal fungi give insights into the history of a successful partnership with plants. In Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor, eds. M. Krings, C.J. Harper, N.R. Cúneo, and G.W. Rothwell, 461–480. London: Elsevier/Academic Press.

    Chapter  Google Scholar 

  • Calderón-Urrea, A., B. Vanholme, S. Vangestel, S.M. Kane, A. Bahaji, K. Pha, M. Garcia, A. Snider, and G. Gheysen. 2016. Early development of the root-knot nematode Meloidogyne incognita. BMC Developmental Biology 16: 10.

    Article  Google Scholar 

  • Channing, A., and D. Edwards. 2009a. Silicification of higher plants in geothermally influenced wetlands: Yellowstone as a Lower Devonian Rhynie analog. Palaios 24: 505–521.

    Article  Google Scholar 

  • Channing, A., and D. Edwards. 2009b. Yellowstone hot spring environments and the palaeo-ecophysiology of Rhynie chert plants: towards a synthesis. Plant Ecology & Diversity 2: 111–143.

    Article  Google Scholar 

  • Channing, A., and D. Edwards. 2013. Wetland megabias: ecological and ecophysiological filtering dominates the fossil record of hot spring floras. Palaeontology 56: 523–556.

    Article  Google Scholar 

  • Chen, S.F., and C.Y. Chien. 1995. Some chytrids of Taiwan (I). Botanical Bulletin of Academia Sinica 36: 235–241.

    Google Scholar 

  • Chen, S.F., and C.Y. Chien. 1998. Some chytrids of Taiwan (II). Botanical Bulletin of Academia Sinica 39: 47–56.

    Google Scholar 

  • Chen, S.F., M.L. Hsu, and C.Y. Chien. 2000. Some chytrids of Taiwan (III). Botanical Bulletin of Academia Sinica 41: 73–80.

    Google Scholar 

  • Currah, R.S., R.A. Stockey, and B.A. LePage. 1998. An Eocene tar spot on a fossil palm and its fungal hyperparasite. Mycologia 90: 667–673.

    Article  Google Scholar 

  • Dayal, R. 1997. Chytrids of India. New Delhi: MD.

    Google Scholar 

  • Dogma, I.J. 1969. Additions to the phycomycete flora of the Douglas Lake Region VIII. Chytriomyces annulatus sp. nov. and notes on other zoosporic fungi. Nova Hedwigia 18: 349–365.

    Google Scholar 

  • Dollhofer, V., S. Podmirseg, T. Callaghan, G.W. Griffith, and K. Fliegerová. 2015. Anaerobic fungi and their potential for biogas production. In Biogas Science and Technology, eds. G.M. Guebitz, A. Bauer, G. Bochmann, A. Gronauer, and S. Weiss, 41–61. Cham: Springer International.

    Chapter  Google Scholar 

  • Edwards, D., L. Dolan, and P. Kenrick (eds.) 2018. The Rhynie cherts: our earliest terrestrial ecosystem revisited. Philosophical Transactions of the Royal Society of London B 373: 1–201.

  • Ellis, D.H. 1981. Sporangiospore ornamentation of thermophilic Rhizopus species and some allied genera. Mycologia 73: 511–523.

    Article  Google Scholar 

  • Emmett, R.W., and D.G. Parbery. 1975. Appressoria. Annual Review of Phytopathology 13: 147–165.

    Article  Google Scholar 

  • Franks, J., and J.F. Stolz. 2009. Flat laminated microbial mat communities. Earth-Science Reviews 96: 163–172.

    Article  Google Scholar 

  • Frenken, T., E. Alacid, S.A. Berger, E.C. Bourne, M. Gerphagnon, H.P. Grossart, A.S. Gsell, B.W. Ibelings, M. Kagami, F.C. Küpper, P.M. Letcher, A. Loyau, T. Miki, J.C. Nejstgaard, S. Rasconi, A. Reñé, T. Rohrlack, K. Rojas-Jimenez, D.S. Schmeller, D.B. Van de Waal, S. Van den Wyngaert, E. Van Donk, J. Wolinska, C. Wurzbacher, and R. Agha. 2017. Integrating chytrid fungal parasites into plankton ecology: research gaps and needs. Environmental Microbiology 19: 3802–3822.

    Article  Google Scholar 

  • Gerphagnon, M., J. Colombert, D. Latour, and T. Sime-Ngando. 2017. Spatial and temporal changes of parasitic chytrids of cyanobacteria. Scientific Reports 7: 6056.

    Article  Google Scholar 

  • Grayson, R.L., and M.L. Lacy. 1975. Development and nuclear history of the teliospores of Urocystis colchici. Phytopathology 65: 994–999.

    Article  Google Scholar 

  • Hajek, A.E., J.E. Longcore, D.R. Simmons, K. Peters, and R.A. Humber. 2013. Chytrid mycoparasitism of entomophthoralean azygospores. Journal of Invertebrate Pathology 114: 333–336.

    Article  Google Scholar 

  • Harper, C.J., M. Krings, N. Dotzler, E.L. Taylor, and T.N. Taylor. 2017. Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: morphology and development of vesicle-colonizing microfungi. Geobios 50: 9–22.

    Article  Google Scholar 

  • Hass, H., T.N. Taylor, and W. Remy. 1994. Fungi from the Lower Devonian Rhynie chert: mycoparasitism. American Journal of Botany 81: 29–37.

    Article  Google Scholar 

  • Hoffmann, K., J. Pawłowska, G. Walther, M. Wrzosek, G.S. de Hoog, G.L. Benny, P.M. Kirk, and K. Voigt. 2013. The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia 30: 57–76.

    Article  Google Scholar 

  • Hoysted, G.A., J. Kowal, A. Jacob, W.R. Rimington, J.G. Duckett, S. Pressel, S. Orchard, M.H. Ryan, K.J. Field, and M.I. Bidartondo. 2018. A mycorrhizal revolution. Current Opinion in Plant Biology 44: 1–6.

    Article  Google Scholar 

  • James, T.Y., P.M. Letcher, J.E. Longcore, S.E. Mozley-Standridge, D. Porter, M.J. Powell, G.W. Griffith, and R. Vilgalys. 2006. A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860–871.

    Article  Google Scholar 

  • Jeffries, P., and T.W.K. Young. 1984. Sporangiospore structure and germination in Dimargaritales. Transactions of the British Mycological Society 83: 223–232.

    Article  Google Scholar 

  • Jeffries, P., and T.W.K. Young. 1994. Interfungal Parasitic Relationships. Wallingford: CAB International.

    Google Scholar 

  • Jennessen, J., J. Schnürer, J. Olsson, R.A. Samson, and J. Dijksterhuis. 2008. Morphological characteristics of sporangiospores of the temple fungus Rhizopus oligosporus differentiate it from other taxa of the R. microsporus group. Mycological Research 112: 547–563.

    Article  Google Scholar 

  • Kagami, M., A. de Bruin, B.W. Ibelings, and E. Van Donk. 2007. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologica 578: 113–129.

    Article  Google Scholar 

  • Karakas, M. 2015. Fungi associated with egg masses and females of plant parasitic nematode Meloidogyne incognita (Nematoda: Heteroderidae). Bangladesh Journal of Botany 44: 373–378.

    Article  Google Scholar 

  • Karatygin, I.V., N.S. Snigirevskaya, and S.V. Vikulin. 2009. The most ancient terrestrial lichen Winfrenatia reticulata: a new find and new interpretation. Paleontological Journal 43: 107–114.

    Article  Google Scholar 

  • Karling, J.S. 1932. Studies in the Chytridiales VII. The organization of the chytrid thallus. American Journal of Botany 19: 41–74.

    Article  Google Scholar 

  • Karling, J.S. 1944. Brazilian anisochytrids. American Journal of Botany 31: 391–397.

    Article  Google Scholar 

  • Karling, J.S. 1966/68. Some zoosporic fungi of New Zealand IV. Polyphlyctis gen. nov., Phlyctochytrium and Rhizidium. Sydowia 20: 86–95.

    Google Scholar 

  • Karling, J.S. 1968. Zoosporic fungi of Oceania. IV. Additional monocentric chytrids. Mycopathologia et Mycologia Applicata 36: 165–178.

    Article  Google Scholar 

  • Karling, J.S. 1977. Chytridiomycetarum Iconographia. An Illustrated and Brief Descriptive Guide to the Chytridiomycetous Genera with a Supplement of the Hyphochytridiomycetes. Vaduz: J. Cramer.

    Google Scholar 

  • Kerp, H., and H. Hass. 2004. De Onder-Devonische Rhynie Chert - het oudste en meest compleet bewaard gebleven terrestrische ecosysteem. Grondboor & Hamer 58: 33–50.

    Google Scholar 

  • Koske, R.E. 1984. Spores of VAM fungi inside spores of VAM fungi. Mycologia 76: 853–862.

    Article  Google Scholar 

  • Kidston, R., and W.H. Lang. 1921. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part IV. Restorations of the vascular cryptogams, and discussion of their bearing on the general morphology of the Pteridophyta and the origin of the organisation of land-plants. Transactions of the Royal Society Edinburgh 52: 831–854.

    Article  Google Scholar 

  • Krings, M., and C.J. Harper. 2018. Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: glomoid spores under attack. Geobios 51: 151–160.

    Article  Google Scholar 

  • Krings, M., and T.N. Taylor. 2014a. An unusual fossil microfungus with suggested affinities to the Chytridiomycota from the Lower Devonian Rhynie chert. Nova Hedwigia 99: 403–412.

    Article  Google Scholar 

  • Krings, M., and T.N. Taylor. 2014b. Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: an intricate interaction between two mycelial fungi. Symbiosis 64: 53–61.

    Article  Google Scholar 

  • Krings, M., and T.N. Taylor. 2015. A fungal reproductive unit from the Lower Devonian Rhynie chert (Aberdeenshire, Scotland) that demonstrates an unusual hyphal investment pattern. Scottish Journal of Geology 51: 131–139.

    Article  Google Scholar 

  • Krings, M., H. Kerp, H. Hass, T.N. Taylor, and N. Dotzler. 2007a. A filamentous cyanobacterium showing structured colonial growth from the Early Devonian Rhynie chert. Review of Palaeobotany and Palynology 146: 265–276.

    Article  Google Scholar 

  • Krings, M., T.N. Taylor, H. Hass, H. Kerp, N. Dotzler, and E.J. Hermsen. 2007b. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist 174: 648–657.

    Article  Google Scholar 

  • Krings, M., N. Dotzler, and T.N. Taylor. 2009. Globicultrix nugax nov. gen. et nov. spec. (Chytridiomycota), an intrusive microfungus in fungal spores from the Rhynie chert. Zitteliana A 48/49: 165–170.

    Google Scholar 

  • Krings, M., T.N. Taylor, J. Galtier, and N. Dotzler. 2010a. Microproblematic endophytes and epiphytes of fern pinnules from the Upper Pennsylvanian of France. Geobios 43: 503–510.

    Article  Google Scholar 

  • Krings, M., N. Dotzler, J.E. Longcore, and T.N. Taylor. 2010b. An unusual microfungus in a fungal spore from the Lower Devonian Rhynie chert. Palaeontology 53: 753–759.

    Article  Google Scholar 

  • Krings, M., T.N. Taylor, E.L. Taylor, H. Kerp, H. Hass, N. Dotzler, and C.J. Harper. 2012. Microfossils from the Lower Devonian Rhynie Chert with suggested affinities to the peronosporomycetes. Journal of Paleontology 86: 358–367.

    Article  Google Scholar 

  • Krings, M., T.N. Taylor, N. Dotzler, and C.J. Harper. 2013. Frankbaronia velata nov. sp., a putative peronosporomycete oogonium containing multiple oospores from the Lower Devonian Rhynie chert. Zitteliana A 53: 23–30.

    Google Scholar 

  • Krings, M., T.N. Taylor, H. Kerp, and C. Walker. 2015. Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: sporocarp formation in glomeromycotan spores. Geobios 48: 449–458.

    Article  Google Scholar 

  • Krings, M., T.N. Taylor, and H. Martin. 2016. An enigmatic fossil fungus from the 410 Ma Rhynie chert that resembles Macrochytrium (Chytridiomycota) and Blastocladiella (Blastocladiomycota). Mycologia 108: 303–312.

    Article  Google Scholar 

  • Krings, M., C.J. Harper, and E.L. Taylor. 2017a. Fungi and fungal interactions in the Rhynie chert: A review of the evidence, with the description of Perexiflasca tayloriana gen. et sp. nov. Philosophical Transactions of the Royal Society of London B 373: ID 20160500.

  • Krings, M., H. Kerp, E.L. Taylor, and C.J. Harper. 2017b. Hagenococcus aggregatus nov. gen. et sp., a microscopic, colony-forming alga from the 410-million-yr-old Rhynie chert. Nova Hedwigia 105: 205–217.

    Article  Google Scholar 

  • Krings, M., T.N. Taylor, and C.J. Harper. 2017c. Early fungi: Evidence from the fossil record. In The Fungal Community, Its Organization and Role in the Ecosystem, 4th ed., eds. J. Dighton and J.F. White, 37–52. Boca Raton: CRC Taylor and Francis.

    Chapter  Google Scholar 

  • Krings, M., C.J. Harper, H. Kerp, and E.L. Taylor. 2018. Exceptional preservation of sessile, long-stalked microorganisms in the Lower Devonian Windyfield chert (Scotland). In Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor, eds. M. Krings, C.J. Harper, N.R. Cúneo, and G.W. Rothwell, 519–526. London, San Diego, Cambridge, Oxford: Elsevier/Academic Press.

    Chapter  Google Scholar 

  • Kyle, M., S. Haande, V. Ostermaier, and T. Rohrlack. 2015. The Red Queen race between parasitic chytrids and their host, Planktothrix: a test using a time series reconstructed from sediment DNA. PLoS ONE 10 (3): e0118738.

    Article  Google Scholar 

  • Letcher, P.M., and M.J. Powell. 2002. A taxonomic summary of Chytriomyces (Chytridiomycota). Mycotaxon 84: 447–487.

    Google Scholar 

  • Letcher, P.M., and M.J. Powell. 2012. A Taxonomic Summary and Revision of Rhizophydium (Rhizophydiales, Chytridiomycota). Tuscaloosa: University Printing.

    Google Scholar 

  • Letcher, P.M., J.E. Longcore, and M.J. Powell. 2014. Irineochytrium, a new genus in Chytridiales having zoospores and aplanospores. Mycologia 106: 1188–1198.

    Article  Google Scholar 

  • Longcore, J.E. 1992. Morphology and zoospore ultrastructure of Chytriomyces angularis sp. nov. (Chytridiales). Mycologia 84: 442–451.

    Article  Google Scholar 

  • Mark, D.F., C.M. Rice, A.E. Fallick, N.H. Trewin, M.R. Lee, A. Boyce, and J.K.W. Lee. 2011. 40Ar/39Ar dating of hydrothermal activity, biota and gold mineralization in the Rhynie hot-spring system, Aberdeenshire, Scotland. Geochimica et Cosmochimica Acta 75: 555–569.

    Article  Google Scholar 

  • Mark, D.F., C.M. Rice, and N.H. Trewin. 2013. Discussion on ‘A high-precision U-Pb age constraint on the Rhynie Chert Konservat-Lagerstätte: time scale and other implications’ Journal, Vol. 168, 863–872. Journal of the Geological Society of London 170: 701–703.

    Article  Google Scholar 

  • Parry, S.F., S.R. Noble, Q.G. Crowley, and C.H. Wellman. 2011. A high precision U-Pb age constraint on the Rhynie chert Konservat-Lagerstätte: time scale and other implications. Journal of the Geological Society of London 168: 863–872.

    Article  Google Scholar 

  • Poinar, G.O. 2015. Phylum Nemata. In Thorp and Covich’s Freshwater Invertebrates, Ecology and General Biology, vol. 1, eds. J.H. Thorp and D.C. Rogers, 273–302. London, San Diego, Waltham, Oxford: Academic Press/Elsevier.

    Chapter  Google Scholar 

  • Poinar, G.O., and R. Buckley. 2007. Evidence of mycoparasitism and hypermycoparasitism in Early Cretaceous amber. Mycological Research 111: 503–506.

    Article  Google Scholar 

  • Poinar, G., H. Kerp, and H. Hass. 2008. Palaeonema phyticum gen. n., sp. n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants. Nematology 10: 9–14.

    Article  Google Scholar 

  • Poinar Jr., G.O., and R. Poinar. 2003. Description and development of Gastromermis anisotis sp. n. (Nematoda: Mermithidae), a parasite in a quadritrophic system involving a cyanobacterium, midge and virus. Nematology 5: 325–338.

    Article  Google Scholar 

  • Powell, C.L., N.H. Trewin, and D. Edwards. 2000. Palaeoecology and plant succession in a borehole through the Rhynie cherts, Lower Old Red Sandstone, Scotland. Geological Society of London Special Publication 180: 439–457.

    Article  Google Scholar 

  • Prieto-Barajas, C., E. Valencia-Cantero, and G. Santovo. 2018. Microbial mat ecosystems: structure types, functional diversity, and biotechnological application. Electronic Journal of Biotechnology 31: 48–56.

    Article  Google Scholar 

  • Rabatin, S.C., and L.H. Rhodes. 1982. Acaulospora bireticulata inside orbatid mites. Mycologia 74: 859–861.

    Article  Google Scholar 

  • Remy, W., T.N. Taylor, and H. Hass. 1994. Early Devonian fungi: a blastocladalean fungus with sexual reproduction. American Journal of Botany 81: 690–702.

    Article  Google Scholar 

  • Rice, C.M., N.H. Trewin, and L.I. Anderson. 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: 203–214.

    Article  Google Scholar 

  • Roane, M.K., and R.A. Paterson. 1974. Some aspects of morphology and development in the Chytridiales. Mycologia 66: 147–164.

    Article  Google Scholar 

  • Samson, R.A. 2016. Cellular constitution, water and nutrient needs, and secondary metabolites. In Environmental Mycology in Public Health. Part II. Fungi and Mycotoxins Risk Assessment and Management, eds. C. Viegas, A.C. Pinheiro, R. Sabino, S. Viegas, J. Brandão, and C. Veríssimo, 5–15. Amsterdam, Boston, Heidelberg, London: Elsevier/Academic Press.

    Chapter  Google Scholar 

  • Siddiqui, Z.A., and I. Mahmood. 1996. Biological control of plant parasitic nematodes by fungi: a review. Bioresource Technology 58: 229–239.

    Article  Google Scholar 

  • Sønstebø, J.H., and T. Rohrlack. 2011. Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Applied and Environmental Microbiology 77: 1344–1351.

    Article  Google Scholar 

  • Sparrow, F.K. 1960. Aquatic Phycomycetes, 2nd rev. ed. Ann Arbor: University of Michigan Press.

    Google Scholar 

  • Sparrow, F.K. 1977. A Rhizidiomycopsis on azygospopres of Gigaspora margarita. Mycologia 69: 1053–1058.

    Article  Google Scholar 

  • Sparrow, F.K., and I.J. Dogma. 1973. Zoosporic phycomycetes from Hispaniola. Archiv für Mikrobiologie 89: 177–204.

    Article  Google Scholar 

  • Spatafora, J.W., Y. Chang, G.L. Benny, K. Lazarus, M.E. Smith, M.L. Berbee, G. Bonito, N. Corradi, I. Grigoriev, A. Gryganskyi, T.L. James, K. O’Donnell, R.W. Robertson, T.N. Taylor, J. Uehling, R. Vilgalys, and M.M. White. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108: 1028–1046.

    Article  Google Scholar 

  • Stirling, G.R., and R. Mankau. 1979. Mode of parasitism of Meloidogyne and other nematode eggs by Dactylella oviparasitica. Journal of Nematology 11: 282–288.

    Google Scholar 

  • Strullu-Derrien, C., Z. Wawrzyniak, T. Goral, and P. Kenrick. 2015. Fungal colonization of the rooting system of the early land plant Asteroxylon mackiei from the 407-Myr-old Rhynie chert (Scotland, UK). Botanical Journal of the Linnean Society 179: 201–213.

    Article  Google Scholar 

  • Strullu-Derrien, C., T. Goral, J.E. Longcore, J. Olesen, P. Kenrick, and G.D. Edgecombe. 2016. A new chytridiomycete fungus intermixed with crustacean resting eggs in a 407-Million-year-old continental freshwater environment. PLoS ONE 11 (12): e0167301.

    Article  Google Scholar 

  • Strullu-Derrien, C., A. R.T. Spencer, T. Goral, J. Dee, R. Honegger, P. Kenrick, J.E. Longcore, and M.L. Berbee. 2017. New insights into the evolutionary history of Fungi from a 407 Ma Blastocladiomycota fossil showing a complex hyphal thallus. Philosophical Transactions of the Royal Society of London B 373: ID20160502.

  • Stubblefield, S.P., T.N. Taylor, C.E. Miller, and G.T. Cole. 1984. Studies in Paleozoic fungi. III. Fungal parasitism in a Pennsylvanian gymnosperm. American Journal of Botany 71: 1275–1284.

    Article  Google Scholar 

  • Taber, R.A. 1982. Occurrence of Glomus spores in weed seeds in soil. Mycologia 74: 515–520.

    Article  Google Scholar 

  • Taylor, T.N., and M. Krings. 2015. A colony-forming microorganism with probable affinities to the Chroococcales (Cyanobacteria) from the Lower Devonian Rhynie chert. Review of Palaeobotany and Palynology 219: 147–156.

    Article  Google Scholar 

  • Taylor, T.N., H. Hass, and W. Remy. 1992a. Devonian fungi: interactions with the green alga Palaeonitella. Mycologia 84: 901–910.

    Article  Google Scholar 

  • Taylor, T.N., W. Remy, and H. Hass. 1992b. Fungi from the lower Devonian Rhynie chert: chytridiomycetes. American Journal of Botany 79: 1233–1241.

    Article  Google Scholar 

  • Taylor, T.N., W. Remy, H. Hass, and H. Kerp. 1995. Fossil arbuscular mycorrhiza from the Early Devonian. Mycologia 87: 560–573.

    Article  Google Scholar 

  • Taylor, T.N., H. Hass, and H. Kerp. 1997. A cyanolichen from the Lower Devonian Rhynie chert. American Journal of Botany 84: 992–1004.

    Article  Google Scholar 

  • Taylor, T.N., S.D. Klavins, M. Krings, E.L. Taylor, H. Kerp, and H. Hass. 2004. Fungi from the Rhynie chert: a view from the dark side. Transactions of the Royal Society of Edinburgh, Earth Sciences 94: 457–473.

    Article  Google Scholar 

  • Taylor, T.N., H. Kerp, and H. Hass. 2005. Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences USA 102: 5892–5897.

    Article  Google Scholar 

  • Taylor, T.N., M. Krings, and E.L. Taylor. 2015. Fossil Fungi, 1st ed. Amsterdam, Boston, Heidelberg, London: Elsevier/Academic Press.

    Google Scholar 

  • Trewin, N.H., and S.R. Fayers. 2016. Macro to micro aspects of the plant preservation in the Early Devonian Rhynie cherts, Aberdeenshire, Scotland. Earth and Environmental Sciences Transactions of the Royal Society of Edinburgh 106: 67–80.

    Article  Google Scholar 

  • Trewin, N.H., and H. Kerp. 2017. The Rhynie and Windyfield cherts, Early Devonian, Rhynie, Scotland. In Terrestrial Conservation Lagerstätten: Windows into the Evolution of Life on Land, eds. N.C. Fraser and H.D. Sues, 1–38. Edinburgh: Dunedin Academic.

    Google Scholar 

  • Trewin, N.H., and C.M. Rice. 1992. Stratigraphy and sedimentology of the Devonian Rhynie chert locality. Scottish Journal of Geology 28: 37–47.

    Article  Google Scholar 

  • Trewin, N.H., S.R. Fayers, and R. Kelman. 2003. Subaqueous silicification of the contents of small ponds in an Early Devonian hot spring complex, Rhynie, Scotland. Canadian Journal of Earth Sciences 40: 1697–1712.

    Article  Google Scholar 

  • Van den Wyngaert, S., K. Rojas-Jimenez, K. Seto, M. Kagami, and H.P. Grossart. 2018. Diversity and hidden host specificity of chytrids infecting colonial volvocalean algae. Journal of Eukaryotic Microbiology, in press.

  • Van Geel, B., A. Aptroot, and D. Mauquoy. 2006. Sub-fossil evidence for fungal hyperparasitism (Isthmospora spinosa on Meliola ellisii, on Calluna vulgaris) in a Holocene intermediate ombrotrophic bog in northern-England. Review of Palaeobotany and Palynology 141: 121–126.

    Article  Google Scholar 

  • Walker, C., A. Gollotte, and D. Redecker. 2018a. A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis). Mycorrhiza 28: 213–219.

    Article  Google Scholar 

  • Walker, C., C.J. Harper, M.C. Brundrett, and M. Krings. 2018b. Looking for arbuscular mycorrhizal fungi (AMF) in the fossil record: an illustrated guide. In Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor., eds. M. Krings, C.J. Harper, N.R. Cúneo, and G.W. Rothwell, 481–517. London, San Diego, Cambridge, Oxford: Elsevier/Academic Press.

    Chapter  Google Scholar 

  • Ward, D.M., M.J. Ferris, S.C. Nold, and M.M. Bateson. 1998. A natural view of microbial diversity within hot spring cyanobacterial mat communities. Microbiology and Molecular Biology Reviews 62: 1353–1370.

    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: 167–211.

    Article  Google Scholar 

  • Wellman, C.H., H. Kerp, and H. Hass. 2006. Spores of the Rhynie chert plant Aglaophyton (Rhynia) major (Kidston and Lang) D.S. Edwards, 1986. Review of Palaeobotany and Palynology 142: 229–250.

    Article  Google Scholar 

  • Young, T.W.K. 1985. Ultrastructure of mucoralean sporangiospores. Botanical Journal of the Linnean Society 91: 151–165.

    Article  Google Scholar 

  • Zopf, W. 1884. Zur Kenntniss der Phycomyceten. I. Zur Morphologie und Biologie der Ancyclisteen und Chytridiaceen. Nova Acta Academiae Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosum 47: 143–236.

    Google Scholar 

  • Zycha, H., R. Siepmann, and G. Linnemann. 1969. Mucorales. Eine Beschreibung aller Gattungen und Arten dieser Pilzgruppe. Lehre: J. Cramer.

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Acknowledgements

We acknowledge financial support from the National Science Foundation (DEB-1441604 subcontract S1696A-A to M.K.) and the Alexander von Humboldt-Foundation (3.1-USA/1160852 STP to C.J.H.). We gratefully acknowledge N. Dotzler, H. Martin, and S. Sónyi (all Munich, Germany) for technical assistance, and Charles H. Wellman (Sheffield, UK) and James F. White (New Brunswick, NJ, USA) for insightful comments on the manuscript.

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Authors and Affiliations

  1. SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333, Munich, Germany

    Michael Krings & Carla J. Harper

  2. Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, Richard-Wagner-Straße 10, 80333, Munich, Germany

    Michael Krings

  3. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045-7534, USA

    Michael Krings & Carla J. Harper

  4. KU Biodiversity Institute & Natural History Museum, University of Kansas, Lawrence, KS, 66045-7534, USA

    Michael Krings & Carla J. Harper

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  1. Michael Krings
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Correspondence to Michael Krings.

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Krings, M., Harper, C.J. Fungal intruders of enigmatic propagule clusters occurring in microbial mats from the Lower Devonian Rhynie chert. PalZ 93, 135–149 (2019). https://doi.org/10.1007/s12542-018-0427-3

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  • DOI: https://doi.org/10.1007/s12542-018-0427-3

Keywords

  • Apophysis
  • Chytridiomycota
  • Mucoromycota
  • Nematoda
  • Parasitism
  • Reproductive unit
  • Rhizoidal system
  • Zoosporangium