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The invasive ergot Claviceps purpurea var. spartinae recently established in the European Wadden Sea on common cord grass is genetically homogeneous and the sclerotia contain high amounts of ergot alkaloids

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Abstract

A well-established population of Claviceps purpurea var. spartinae R.A. Duncan & J.F. White was found on the invasive common cord-grass Spartina anglica C.E. Hubbard at two localities on the German North Sea coast. Additionally, 25 populations of S. anglica with an average air-line distance of 50 km between them along the coastline, starting from the Netherlands via the German coastline up to Denmark, were investigated. All S. anglica populations were heavily infected with C. purpurea var. spartinae (lineage G3). Genetic characterization of the C. purpurea DNA using Amplified Fragment Length Polymorphism (AFLP) and Internal Transcribed Spacer (ITS) analysis clearly indicated that all populations collected at the Wadden Sea were grouped in the same epidemic clade. Comparisons with reference strains indicated that the isolates along the Wadden Sea belonged to the clade also found in Ireland and Wales. The ergot alkaloid pattern is very similar in all genotypes. Ergocristine, α-ergocryptine and their epimers were identified in the samples in high amounts comparable to average values in sclerotia found on rye. The sclerotia of C. purpurea var. spartinae are able to float on the water for several months and could thereby be distributed over large distances by seawater. The sclerotia found in the drift lines still contain the equally high contents of ergot alkaloids as those collected directly from the plants. Current data form the basis for risk assessments and predictions about further spreading of C. purpurea var. spartinae on S. anglica.

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References

  • Adsersen, H., Randløv, M. S., Nielsson, N., Larsen, R. S., Francke, M. S., & Boesgaard, K. (2010). Invasion history of Spartina anglica in Denmark. Svensk Botanisk Tidskrift, 104(6), 393–404.

    Google Scholar 

  • Agrios, G. N. (2005). Plant Pathology. Waltham: Academic.

    Google Scholar 

  • Bakker, L., van der Wal, R., Esselink, P., & Siepel, A. (1999). Exploitation of a new staging area in the Dutch Wadden Sea by Greylag Geese Anser anser: the importance of food-plant dynamics. Ardea, 87(1), 1–13.

    Google Scholar 

  • Blaney, B. J., Molloy, J. B., & Brock, I. J. (2009). Alkaloids in Australian rye ergot (Claviceps purpurea) sclerotia: implications for food and stockfeed regulations. Animal Production Science, 49, 975–982.

    Article  CAS  Google Scholar 

  • Dice, L. R. (1945). Measures of the amount of ecologic association between species. Ecology, 26, 297–302.

    Article  Google Scholar 

  • Douhan, G. W., Smith, M. E., Huyrn, K. L., Westbrook, A., Beerli, P., & Fisher, A. J. (2008). Multigene analysis suggests ecological speciation in the fungal pathogen Claviceps purpurea. Molecular Ecology, 17(9), 2276–2286.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duncan, R. A., Sullivan, R., Alderman, S. C., Spatafora, J. W., & White, J. F. (2002). Claviceps purpurea var. spartinae var. nov.: An ergot adapted to the aquatic environment. Mycotaxon, 81, 11–25.

    Google Scholar 

  • Eleuterius, L. N., & Meyers, S. P. (1977). Alkaloids of Claviceps from Spartina. Mycologia, 69(4), 838–840.

    Article  CAS  PubMed  Google Scholar 

  • Engeland, I. V., Andresen, O., Ropstad, H., Kindahl, H., Waldeland, A., Daskin, A., & Eik, L. O. (1998). Effect of fungal alkaloids on the development of pregnancy and endocrine foetal-placental function in the goat. Animal Reproduction Science, 52(4), 289–302.

    Article  Google Scholar 

  • European Food Safety Authority. (2005). Opinion of the scientific panel on contaminants in food chain on a request from the commission related to ergot as undesirable substance in animal feed. The EFSA Journal, 225, 1–27.

    Google Scholar 

  • Fisher, A. J., DiTomaso, J. M., & Gordon, T. R. (2005). Intraspecific groups of Claviceps purpurea associated with grass species in Willapa Bay, Washington, and the prospects for biological control of invasive Spartina alterniflora. Biological Control, 34(2), 170–179.

    Article  Google Scholar 

  • Gardes, M., & Brunes, T. D. (1993). ITS primers with enhanced specificity for Basidiomycetes – application to the identification of mycorrhiza and rusts. Molecular Ecology, 2, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Hampl, V., Pavlicek, A., & Flegr, J. (2001). Construction and bootstrap analysis of DNA fingerprinting based phylogenetic trees with the freeware program FreeTree: application to Trichomonad parasites. International Journal of Systematic and Evolutionary Microbiology, 51, 731–735.

    Article  CAS  PubMed  Google Scholar 

  • Komarova, E. L., & Tolkachev, O. N. (2001). The chemistry of peptide ergot alkaloids. Part 1. Classification and chemistry of ergot peptides. Pharmaceutical Chemistry Journal, 35(9), 504–513.

    Article  CAS  Google Scholar 

  • Krska, R., Stubbings, G., MacArthur, R., & Crews, C. (2008). Simultaneous determination of six major ergot alkaloids and their epimers in cereals and foodstuffs by LC-MS-MS. Analytical and Bioanalytical Chemistry, 391, 563–576.

    Article  CAS  PubMed  Google Scholar 

  • Mainka, S., Danicke, S., Bohme, H., Überschar, K. H., & Liebert, F. (2007). On the composition of ergot and the effects of feeding two different ergot sources on piglets. Animal Feed Science and Technology, 139, 52–68.

    Article  CAS  Google Scholar 

  • Mulac, D., & Humpf, H. U. (2011). Cytotoxicity and accumulation of ergot alkaloids in human primary cells. Toxicology, 282, 112–121.

    Article  CAS  PubMed  Google Scholar 

  • Müller, C., Kemmlein, S., Klaffke, H., Krauthause, W., Preiss-Weigert, A., & Wittkowski, R. (2009). A basic tool for risk assessment: a new method for the analysis of ergot alkaloids in rye and selected rye products. Molecular Nutrition and Food Research, 53(4), 500–507.

    Article  PubMed  Google Scholar 

  • Nehring, S., & Hesse, K. J. (2008). Invasive alien plants in marine protected areas: the Spartina anglica affair in the European Wadden Sea. Biological Invasions, 10, 937–950.

    Article  Google Scholar 

  • Nehring, S., Boestfleisch, C., Buhmann, A., & Papenbrock, J. (2012). The North American toxic fungal pathogen G3 Claviceps purpurea (Fries) Tulasne is established in the German Wadden Sea. BioInvasions Records, 1, 5–10.

    Article  Google Scholar 

  • Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America, 76(10), 5269–5273.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson, E. C. (2000). Sea beans and nickar nuts. A handbook of exotic seeds and fruits stranded on beaches in north-western Europe. London: BSBI Handbook.

    Google Scholar 

  • Oresanya, T. F., Patience, J. F., Zijistra, R. T., Beaulieu, A. D., Middleton, D. M., Blakley, B. R., & Gillis, D. A. (2003). Defining the tolerable level of ergot in the diet of weaned pigs. Canadian Journal of Animal Science, 83(3), 493–500.

    Article  CAS  Google Scholar 

  • Otto, L., & van Aken, H. M. (1996). Surface circulation in the northeast Atlantic as observed with drifters. Deep-sea research Part I, Oceanographic research papers, 43(4), 467–499.

    Article  Google Scholar 

  • Pažoutová, S. (2002). Evolutionary strategy of Claviceps. In J. F. White, C. W. Bacon, & N. L. Hywel-Jones (Eds.), Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol and Cultural Impacts (pp. 329–354). New York: Marcel Dekker.

    Google Scholar 

  • Pažoutová, S., Olšovská, J., Linka, M., Kolínská, R., & Flieger, M. (2000). Chemoraces and habitat specialization of Claviceps purpurea populations. Applied and Environmental Microbiology, 66(12), 5419–5425.

    Article  PubMed Central  PubMed  Google Scholar 

  • Pažoutová, S., Raybould, A. F., Honzátko, A., & Kolínská, R. (2002). Specialized populations of Claviceps purpurea from salt marsh Spartina species. Mycological Research, 106, 210–214.

    Article  Google Scholar 

  • Rohlf, F. J. (2005). NTSYSpc: Numerical Taxonomy System, ver. 2.11X. Setauket: Exeter Publishing, Ltd.

    Google Scholar 

  • Scott, P. M. (2009). Ergot alkaloids: extent of human and animal exposure. World Mycotoxin Journal, 2(2), 141–149.

    Article  CAS  Google Scholar 

  • Smith, D. J., & Shappell, N. W. (2002). Technical note: epimerization of ergopeptine alkaloids in organic and aqueous solvents. Journal of Animal Science, 80(6), 1616–1622.

    CAS  PubMed  Google Scholar 

  • Strickland, J. R., Looper, M. L., Matthews, J. C., Rosenkrans, C. F., Jr., Flythe, M. D., & Brown, K. R. (2011). Board-invited review: St. Anthony’s Fire in livestock: causes, mechanisms, and potential solutions. Journal of Animal Science, 89(5), 1603–1626.

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson, J. D. (1991). The biology of an invasive plant. What makes Spartina anglica so successful? Bioscience, 41(6), 393–401.

    Article  Google Scholar 

  • Uhlig, S., Vikoren, T., Ivanova, L., & Handeland, K. (2007). Ergot alkaloids in Norwegian wild grasses: a mass spectrometric approach. Rapid Communications in Mass Spectrometry, 21(10), 1651–1660.

    Article  CAS  PubMed  Google Scholar 

  • Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M., & Zabeau, M. (1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research, 23(21), 4407–4414.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols: A Guide to Methods and Applications (pp. 315–322). New York: Academic.

    Chapter  Google Scholar 

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Acknowledgments

We greatly acknowledge Mrs. Anne Buhmann and Mrs. Yvonne Leye for initial sampling and Mrs. Jutta Barras-Akhnoukh for technical assistance in toxin analysis. We would like to thank Nationalparkverwaltung Niedersächsisches Wattenmeer and Landesbetrieb für Küstenschutz, Nationalpark und Meeresschutz, Schleswig-Holstein, Germany, for the permission to take samples. We would also like to acknowledge the Naturschutzbund Deutschland e.V. (NABU), especially the NABU Stations in Wangerooge, Borkum and Westerspätinge for cooperation. We are grateful to Prof. Dr. R. Cox, Hannover, Germany, for correcting the English language and Dr. M. Kolarik, Prague, Czech Republic, for valuable suggestions concerning the taxonomy of C. purpurea.

Culture deposition

Claviceps purpurea var. spartinae isolate from Caeciliengroden is available under serial number DSM 26190 at the Leibniz-Institut DSMZ, Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstraße 7B, D-38124 Braunschweig, Germany.

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Authors and Affiliations

  1. Institute of Botany, Leibniz University Hannover, Herrenhäuser Straße 2, 30419, Hannover, Germany

    Christian Boestfleisch & Jutta Papenbrock

  2. Institute of Food Toxicology and Analytical Chemistry, Department of Analytical Chemistry, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, 30173, Hannover, Germany

    Astrid M. Drotleff & Waldemar Ternes

  3. Federal Agency for Nature Conservation, Konstantinstraße 110, 53179, Bonn, Germany

    Stefan Nehring

  4. Laboratory of the Genetics and Metabolism of Fungi, Institute of Microbiology CAS, Vídeňská 1083, 142 20, Prague 4, Czech Republic

    Sylvie Pažoutová

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  1. Christian Boestfleisch
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  2. Astrid M. Drotleff
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  3. Waldemar Ternes
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  4. Stefan Nehring
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  5. Sylvie Pažoutová
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  6. Jutta Papenbrock
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Correspondence to Jutta Papenbrock.

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Sylvie Pažoutová sadly passed away on 6 September 2013.

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Boestfleisch, C., Drotleff, A.M., Ternes, W. et al. The invasive ergot Claviceps purpurea var. spartinae recently established in the European Wadden Sea on common cord grass is genetically homogeneous and the sclerotia contain high amounts of ergot alkaloids. Eur J Plant Pathol 141, 445–461 (2015). https://doi.org/10.1007/s10658-014-0555-x

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