Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T06:54:33.898Z Has data issue: false hasContentIssue false

Diversity of lichen-associated filamentous fungi preserved in European Paleogene amber

Published online by Cambridge University Press:  28 February 2018

Elina Kettunen
Affiliation:
Department of Biosciences, University of Helsinki, P.O. Box 65, Helsinki, FIN-00014, Finland.
Alexander R. Schmidt*
Affiliation:
Department of Geobiology, University of Göttingen, Goldschmidtstraße 3, D-37077, Göttingen, Germany. Email: [email protected]
Paul Diederich
Affiliation:
National Museum of Natural History, 25 rue Munster, L-2160 Luxembourg, Luxembourg.
Heinrich Grabenhorst
Affiliation:
Amber Study Group, c/o Geological-Palaeontological Institute and Museum of the University of Hamburg, Bundesstraße 55, D-20146, Hamburg, Germany.
Jouko Rikkinen
Affiliation:
Department of Biosciences, University of Helsinki, P.O. Box 65, Helsinki, FIN-00014, Finland. Finnish Museum of Natural History, Botany Unit, PO Box 7, Helsinki, FIN-00014, Finland.
*
*Corresponding author

Abstract

A diversity of filamentous microfungi was discovered from thallus surfaces of epiphytic lichens preserved in Bitterfeld and Baltic amber. We report seven distinct morphologies of dematiaceous hyphomycetes, some of which closely resemble species of the extant genera Sporidesmium, Taeniolella s. lat. and Taeniolina. Both the placement of the fungi on their substrates and the exquisite preservation of delicate structures indicate that the fungi were fully developed before they were engulfed by fresh resin. The lichens probably grew on the trunks of resin producing trees and became embedded in resin flows together with their fungal associates. The findings demonstrate that a wide range of presumably specialised fungi have lived on living and decomposing lichen thalli at least since the Paleogene. The findings add an interesting new component to the as yet poorly known mycota of the ancient European amber forests.

Type
Articles
Copyright
Copyright © The Royal Society of Edinburgh 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

5. References

Alstrup, V. 1991. Sporidesmium bacidiicola sp.n. Graphis Scripta 3, 4445.Google Scholar
Aschenbrenner, I. A., Cardinale, M., Berg, G. & Grube, M. 2014. Microbial Cargo: Do bacteria on symbiotic propagules reinforce the microbiome of lichens? Environmental Microbiology 16, 3743–52.Google Scholar
Aschenbrenner, I. A., Cernava, T., Berg, G. & Grube, M. 2016. Understanding microbial multi-species symbioses. Frontiers in Microbiology 7, 180.Google Scholar
Asplund, J. 2011. Snails avoid the medulla of Lobaria pulmonaria and L. scrobiculata due to presence of secondary compounds. Fungal Ecology 4, 356–58.Google Scholar
Asplund, J. & Wardle, D. A. 2013. The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. Journal of Ecology 101, 689700.Google Scholar
Bates, S. T., Cropsey, G. W. G., Caporaso, J. G., Knight, R. & Fierer, N. 2011. Bacterial communities associated with the lichen symbiosis. Applied and Environmental Microbiology 77, 1309–14.Google Scholar
Blumenstengel, H. 2004. Zur Palynologie und Stratigraphie der Bitterfelder Bernsteinvorkommen (Tertiär). Exkursionsführer und Veröffentlichungen der Deutschen Gesellschaft für Geowissenschaften 224, 17.Google Scholar
Braun, U., Heuchert, B. & Diederich, P. 2009. Two new and another interesting lichenicolous hyphomycete. Herzogia 22, 165–71.Google Scholar
Culberson, C. F. 1969. Chemical and Botanical Guide to Lichen Products. Chapel Hill: University of North Carolina Press. 628 pp.Google Scholar
Culberson, C. F. 1970. Supplement to Chemical and Botanical Guide to Lichen Products. Bryologist 73, 177377.Google Scholar
Culberson, C. F., Culberson, W. L. & Johnson, A. 1977. Second Supplement to Chemical and Botanical Guide to Lichen Products. Missouri Botanical Garden, St. Louis: American Bryological and Lichenologial Society. 400 pp.Google Scholar
Dunlop, J. 2010. Bitterfeld amber. In Penney, D. (ed.) Biodiversity of Fossils in Amber, 5768. Manchester: Siri Scientific Press.Google Scholar
Ellis, M. B. 1976. More dematiaceous Hyphomycetes. Aberystwyth: The Cambrian News Ltd. 507 pp.Google Scholar
Ertz, D, Heuchert, B., Braun, U., Freebury, C. E., Common, R. S. & Diederich, P. 2016. Contribution to the phylogeny and taxonomy of the genus Taeniolella, with a focus on lichenicolous taxa. Fungal Biology 120, 1416–47.Google Scholar
Etayo, J. 2017. Hongos liquenícolas de Ecuador. Opera Lilloana 50, 1535.Google Scholar
Fazio, A. T., Adler, M. T., Bertoni, M. D., Sepùlveda, C. S., Damonte, E. B. & Maier, M. S. 2007. Lichen secondary metabolites from the cultured lichen mycobionts of Teloschistes chrysophthalmus and Ramalina celastri and their antiviral activities. Zeitschrift für Naturforschung 62C, 543–49.Google Scholar
Girlanda, M., Isocrono, D., Bianco, C. & Luppimosca, A. M. 1997. Two foliose lichens as microfungal ecological niches. Mycologia 89, 531–36.Google Scholar
Gray, S. F. 1821. A natural arrangement of British plants. London: Baldwin, Cradock and Joy. 824 pp.Google Scholar
Grube, M., Cardinale, M., de Castro, J. V. Jr., Müller, H. & Berg, G. 2009. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME Journal 3, 1105–15.Google Scholar
Grube, M., Berg, G., Andrésson, Ó. S., Vilhelmsson, O., Dyer, P. S. & Miao, V. P. W. 2014. Lichen genomics: Prospects and progress. In: Martin, F. (ed.) The Ecological Genetics of Fungi, 191212. Hoboken: John Wiley & Sons.Google Scholar
Halama, P. & Van Haluwyn, C. [as ‘Haluwin’] 2004. Antifungal activity of lichen extracts and lichenic acids. Biocontrol 49, 95107.Google Scholar
Haller, A. von. 1768. Historia stirpium indigenarum Helvetiae inchoata. Bern: Sumptibus Societatis Typographicae. 250 pp.Google Scholar
Hartl, C., Schmidt, A. R., Heinrichs, J., Seyfullah, L. J., Schäfer, N., Gröhn, C., Rikkinen, J. & Kaasalainen, U. 2015. Lichen preservation in amber: morphology, ultrastructure, chemofossils, and taphonomic alteration. Fossil Record 18, 127–35.Google Scholar
Hawksworth, D. L. 1979. The Lichenicolous Hyphomycetes. Bulletin of the British Museum for Natural History. 6, 183300.Google Scholar
Hawksworth, D. L. 1982a. Secondary fungi in lichen symbioses: parasites, saprophytes and parasymbionts. Journal of the Hattori Botanical Laboratory 52, 357–66.Google Scholar
Hawksworth, D. L. 1982b. Co-evolution and the detection of ancestry in lichens. Journal of the Hattori Botanical Laboratory 52, 323–29.Google Scholar
Hawksworth, D. L. 2003. The lichenicolous fungi of Great Britain and Ireland: An overview and annotated checklist. Lichenologist 35, 191232.Google Scholar
Hawksworth, D. L. & Cole, M. S. 2002. Intralichen, a new genus for lichenicolous ‘Bispora’ and ‘Trimmatostroma’ species. Fungal Diversity 11, 8797.Google Scholar
Hodkinson, B. P., Gottel, N. R., Schadt, C. W. & Lutzoni, F. 2012. Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environmental Microbiology 14, 147–61.Google Scholar
Hodkinson, B. P. & Lutzoni, F. 2009. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49, 163–80.Google Scholar
Honegger, R., Edwards, D. & Axe, L. 2013. The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytologist 197, 264–75.Google Scholar
Hughes, S. J. 1958. Revisiones Hyphomycetum aliquot cum appendice de nominibus rejiciendis. Canadian Journal of Botany 36, 727836.Google Scholar
Huneck, S. & Yoshimura, I. 1996. Identification of lichen substances. Berlin, Heidelberg: Springer-Verlag. 493 pp.Google Scholar
Iturriaga, T., Hawksworth, D. L. & Crane, J. L. 2008. ‘Sporidesmiumlichenicola sp. nov., a new lichenicolous fungus on Leptogium from Venezuela. Mycologia 100, 392–96.Google Scholar
Kaasalainen, U., Heinrichs, J., Krings, M., Myllys, L., Grabenhorst, H., Rikkinen, J. & Schmidt, A. R. 2015. Alectorioid morphologies in Paleogene lichens: new evidence and re-evaluation of the fossil Alectoria succini Mägdefrau. PLoS ONE 10. e0129526.Google Scholar
Kaasalainen, U., Schmidt, A. R. & Rikkinen, J. 2017. Diversity and ecological adaptations in Palaeogene lichens. Nature Plants 3, 17049.Google Scholar
Karatygin, I. V., Snigirevskaya, N. S. & Vikulin, S. V. 2009. The most ancient terrestrial lichen Winfrenatia reticulata: A new find and new interpretation. Paleontological Journal 43, 107–14.Google Scholar
Kettunen, E., Schmidt, A. R., Diederich, P., Grabenhorst, H. & Rikkinen, J. 2016. Lichen-associated fungi from Paleogene amber. New Phytologist 209, 896–98.Google Scholar
Kirk, P. M. 1981. New or interesting microfungi 1. Dematiaceous hyphomycetes from Devon. Transactions of the British Mycological Society 76, 7187.Google Scholar
Knuth, G., Koch, T., Rappsilber, I. & Volland, L. 2002. Concerning amber in the Bitterfeld region - geologic and genetic aspects. Hallesches Jahrbuch für Geowissenschaften 24, 3546.Google Scholar
Kraichak, E., Divakar, P. K., Crespo, A. & Lumbsch, T. 2015. A tale of two hyper-diversities: Diversification dynamics of the two largest families of lichenized fungi. Scientific Reports 5, 10028.Google Scholar
Lawrey, J. D. 1986. Biological role of lichen substances. Bryologist 89, 111–22.Google Scholar
Lawrey, J. D., Torzilli, A. P. & Chandhoke, V. 1999. Destruction of lichen chemical defenses by a fungal pathogen. American Journal of Botany 86, 184–89.Google Scholar
Lawrey, J. D. & Diederich, P. 2003. Lichenicolous fungi: Interactions, evolution, and biodiversity. Bryologist 106, 80120.Google Scholar
Lawrey, J. D. & Diederich, P. 2016. Lichenicolous fungi – worldwide checklist, including isolated cultures and sequences available. URL: http://www.lichenicolous.net. Accessed 22th June 2016.Google Scholar
Link, H. F. 1809. Observationes in ordines plantarum naturales. Dissertatio I. Magazin der Gesellschaft Naturforschender Freunde Berlin 3, 342.Google Scholar
Link, H. F. 1816. Observationes in ordines plantarum naturales. 2. Magazin der Gesellschaft Naturforschender Freunde Berlin 6, 2545.Google Scholar
Lumbsch, T. 2002. Analysis of phenolic products in lichens for identification and taxonomy. In Kranner, I. C., Beckett, R. P. & Varma, A. K. (eds) Protocols in Lichenology, 281–95. Berlin & Heidelberg: Springer Lab Manuals. 580 pp.Google Scholar
Massalongo, A. B. 1852. Ricerche sull'autonomia dei licheni crostosi. Verona: Dalla tipografia di A. Frizierio. 221 pp.Google Scholar
Millanes, A. M., Truong, C., Westberg, M., Diederich, P. & Wedin, M. 2014. Host switching promotes diversity in host-specialized mycoparasitic fungi: uncoupled evolution in the Biatoropsis-Usnea system. Evolution 68, 1576–93.Google Scholar
Nascimbene, P. & Silverstein, H. 2000. The preparation of fragile Cretaceous ambers for conservation and study of organismal inclusions. In Grimaldi, D. (ed.) Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey, 93102. Leiden: Backhuys Publishers. viii+498 pp.Google Scholar
Nguyen, K. -H., Chollet-Krugler, M., Gouault, N. & Tomasi, S. 2013. UV-protectant metabolites from lichens and their symbiotic partners. Natural Products Reports 30, 1490–508.Google Scholar
Nybakken, L., Helmersen, A., Gauslaa, Y. & Selas, V. 2010. Lichen compounds restrain lichen feeding by bank voles (Myodes glareolus). Journal of Chemical Ecology 36, 298304.Google Scholar
Petrini, O., Hake, U. & Dreyfuss, M. M. 1990. An analysis of fungal communities isolated from fruticose lichens. Mycologia 82, 444–51.Google Scholar
Rambold, G. & Triebel, D. 1992. The inter-lecanoralean associations. Bibliotheca Lichenologica 48, 1201.Google Scholar
Ranković, B. Misić, M. & Sukdolak, S. 2007. Antimicrobial activity of extracts of the lichens Cladonia furcata, Parmelia caperata, Parmelia pertusa, Hypogymnia physodes and Umbilicaria polyphylla. British Journal of Biomedical Science 64, 143–48.Google Scholar
Rikkinen, J. 1995. What's behind the pretty colours? A study on the phytobiology of lichens. Bryobrothera 4, 1239.Google Scholar
Rikkinen, J. 2003a. Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34, 99110.Google Scholar
Rikkinen, J. 2003b. Calicioid lichens from European Tertiary amber. Mycologia 95, 1032–36.Google Scholar
Rikkinen, J., Dörfelt, H., Schmidt, A. R. & Wunderlich, J. 2003. Sooty moulds from European Tertiary amber, with notes on the systematic position of Rosaria (‘Cyanobacteria’). Mycological Research 107, 251–56.Google Scholar
Rikkinen, J. & Poinar, G. O. 2002. Fossilised Anzia (Lecanorales, lichen-forming Ascomycota) from European Tertiary amber. Mycological Research 106, 984–90.Google Scholar
Rikkinen, J. & Poinar, G. O. Jr. 2008. A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens. Journal of Experimental Botany 59, 1007–11.Google Scholar
Schmidt, A. R., Jancke, S., Lindquist, E. E., Ragazzi, E., Roghi, G., Nascimbene, P. C., Schmidt, K., Wappler, T. & Grimaldi, D. A. 2012. Arthropods in amber from the Triassic Period. Proceedings of the National Academy of Sciences of the United States of America 109, 14796–801.Google Scholar
Schmidt, A. R., Dörfelt, H., Grabenhorst, H., Tuovila, H. & Rikkinen, J. 2013. Fungi of the Bitterfeld amber forest. In Rascher, J., Rappsilber, I. & Wimmer, R. (eds) Bitterfelder Bernstein und andere fossile Harze aus Mitteldeutschland. Exkursionsführer und Veröffentlichungen der Deutschen Gesellschaft für Geowissenschaften 249, 5460. Hannover: DGG Publications. 138 pp.Google Scholar
Schmidt, A. R., Beimforde, C., Seyfullah, L. J., Wege, S., Dörfelt, H., Girard, V., Grabenhorst, H., Gube, M., Heinrichs, J., Nel, A., Nel, P., Perrichot, V., Reitner, J. & Rikkinen, J. 2014. Amber fossils of sooty moulds. Review of Palaeobotany and Palynology 200, 5364.Google Scholar
Seifert, K. A., Morgan-Jones, G., Gams, W. & Kendrick, B. 2011. The Genera of Hyphomycetes. Utrecht: CBS Biodiversity Series 9, CBS-KNAW Fungal Biodiversity Centre. 997 pp.Google Scholar
Shenoy, B. D., Jeewon, R., Wu, W. P., Bhat, D. J. & Hyde, K. D. 2006. Ribosomal and RPB2 DNA sequence analyses suggest that Sporidesmium and morphologically similar genera are polyphyletic. Mycological Research 110, 916–28.Google Scholar
Sigurbjörnsdóttir, M. A., Heiðmarsson, S., Jónsdóttir, A. R. & Vilhelmsson, O. 2014. Novel bacteria associated with Arctic seashore lichens have potential roles in nutrient scavenging. Canadian Journal of Microbiology 60, 307–17.Google Scholar
Solhaug, K. A., Gauslaa, Y., Nybakken, L. & Bilger, W. 2003. UV-induction of sun-screening pigments in lichens. New Phytologist 158, 91100.Google Scholar
Standke, G. 2008. Bitterfelder Bernstein gleich Baltischer Bernstein? – Eine geologische Raum-Zeit-Betrachtung und genetische Schlußfolgerungen. In Rascher, J., Wimmer, R., Krumbiegel, G. & Schmiedel, S. (eds) Bitterfelder Bernstein versus Baltischer Bernstein – Hypothesen, Fakten, Fragen. Exkursionsführer und Veröffentlichungen der Deutschen Gesellschaft für Geowissenschaften 236, 1133. Hannover: DGG Publications. 168 pp.Google Scholar
Subramanian, C. V. 1992. A reassessment of Sporidesmium (Hyphomycetes) and some related taxa. Proceedings of the Indian Academy of Sciences 58, 179–90.Google Scholar
Taylor, T. N., Hass, H. & Kerp, H. 1997. A cyanolichen from the Lower Devonian Rhynie chert. American Journal of Botany 84, 9921004.Google Scholar
Torzilli, A. P., Mikelson, P. A. & Lawrey, J. D. 1999. Physiological effect of lichen secondary metabolites on the lichen parasite Marchandiomyces corallinus. Lichenologist 31, 307–14.Google Scholar
U'Ren, J. M., Lutzoni, F., Miadlikowska, J., Laetsch, A. D. & Arnold, A. E. 2012. Host- and geographic structure of endophytic and endolichenic fungi at a continental scale. American Journal of Botany 99, 898914.Google Scholar
Weitschat, W. 1997. Bitterfelder Bernstein - ein eozäner Bernstein auf miozäner Lagerstätte. Metalla 66, 7184.Google Scholar
Werth, S., Millanes, A. M., Wedin, M. & Scheidegger, C. 2013. Lichenicolous fungi show population subdivision by host species but do not share population history with their hosts. Fungal Biology 117, 7184.Google Scholar
Whitton, S. R., McKenzie, E. H. C. & Hyde, K. D. 1999. Microfungi on the Pandanaceae: Troposporopsis gen. nov. Fungal Diversity 3, 173–77.Google Scholar