Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-06-14T02:54:08.276Z Has data issue: false hasContentIssue false
  • English
  • Français

Virulence, cultivating conditions, and phylogenetic analyses of oomycete parasites in Daphnia

Published online by Cambridge University Press:  10 November 2008

J. WOLINSKA ,
K. C. KING ,
F. VIGNEUX  and
C. M. LIVELY
J. WOLINSKA*
Affiliation:
Indiana University, Department of Biology, 1001 East 3rd Street, Bloomington, Indiana 47405, USA Ludwig-Maximilians-Universität, Department Biologie II, Evolutionsökologie, Großhaderner Strasse 2, D-82152 Planegg-Martinsried, Germany
K. C. KING
Affiliation:
Indiana University, Department of Biology, 1001 East 3rd Street, Bloomington, Indiana 47405, USA
F. VIGNEUX
Affiliation:
Indiana University, Department of Biology, 1001 East 3rd Street, Bloomington, Indiana 47405, USA
C. M. LIVELY
Affiliation:
Indiana University, Department of Biology, 1001 East 3rd Street, Bloomington, Indiana 47405, USA
*
*Corresponding author: Ludwig-Maximilians-Universität, Department Biologie II, Evolutionsökologie, Großhaderner Strasse 2, D-82152 Planegg-Martinsried, Germany. Tel: +49 (0) 89 2180 74 202. Fax: +49 (0) 89 2180 204. E-mail: wolinska@bio.lmu.de
Get access Rights & Permissions [Opens in a new window]

Summary

We describe the infectivity, virulence, cultivating conditions, and phylogenetic positions of naturally occurring oomycete parasites of Daphnia, invertebrates which play a major role in aquatic food webs. Daphnia pulex individuals were found dead and covered by oomycete mycelia when exposed to pond sediments. We were able to extract 4 oomycete isolates from dead Daphnia and successfully cultivate them. Using the ITS and LSU rDNA sequences, we further showed these isolates to be distinct species. The isolates were experimentally demonstrated to be parasitic and not saprobic. After exposure to the parasites, Daphnia mortality was much higher than that reported for Daphnia infected with other known parasite species. Therefore, it is likely that oomycete parasites are important selective pressures in natural Daphnia populations. Moreover, their close phylogenetic relationship to parasites of fish and algae suggests that the stability of aquatic food webs (i.e. fish–Daphnia–algae) might be influenced by the shared parasite communities.

Keywords

DaphniaITSLSU rDNAparasitesoomycetes
Type
Research Article
Information
Parasitology , Volume 135 , Issue 14 , December 2008 , pp. 1667 - 1678
Copyright
Copyright © 2008 Cambridge University Press

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

REFERENCES

Ballesteros, I., Martin, M. P. and Dieguez-Uribeondo, J. (2006). First isolation of Aphanomyces frigidophilus (Saprolegniales) in Europe. Mycotaxon 95, 335–340.Google Scholar
Bangyeekhun, E., Quiniou, S. M. A., Bly, J. E. and Cerenius, L. (2001). Characterisation of Saprolegnia sp. isolates from channel catfish. Diseases of Aquatic Organisms 45, 53–59.CrossRefGoogle ScholarPubMed
Beck, S. J. and Erb, K. (1984). Facultative parasitism of Spirogyra sp. (Chlorophyta) by Saprolegnia asterophora and Pythium gracile (Eumycota, Oomycetes). Journal of Phycology 20, 13–19.CrossRefGoogle Scholar
Burns, C. W. (1985). Fungal parasitism in a freshwater copepod: components of the interaction between Aphanomyces and Boeckella. Journal of Invertebrate Pathology 46, 5–10.CrossRefGoogle Scholar
Decaestecker, E., De Meester, L. and Ebert, D. (2002). In deep trouble: Habitat selection constrained by multiple enemies in zooplankton. Proceedings of the National Academy of Sciences, USA 99, 5481–5485.CrossRefGoogle ScholarPubMed
Decaestecker, E., Lefever, C., De Meester, L. and Ebert, D. (2004). Haunted by the past: Evidence for dormant stage banks of microparasites and epibionts of Daphnia. Limnology and Oceanography 49, 1355–1364.CrossRefGoogle Scholar
Dick, M. W. (1969 a). Morphology and taxonomy of oomycetes, with special reference to Saprolegniaceae, Leptomitaceae and Pythiaceae.1. Sexual reproduction. New Phytologist 68, 751–775.CrossRefGoogle Scholar
Dick, M. W. (1969 b). The Scoliolegnia asterophora aggregate, formerly Saprolegnia asterophora de Bary (Oomycetes). Botanical Journal of the Linnean Society 62, 255–266.CrossRefGoogle 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, The Netherlands.CrossRefGoogle Scholar
Ebert, D. (2005). Ecology, Epidemiology, and Evolution of Parasitism in Daphnia [Internet], Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information.Google Scholar
Ebert, D. (2008). Host-parasite coevolution: insights from the Daphnia-parasite model system. Current Opinion in Microbiology 11, 1–12.CrossRefGoogle ScholarPubMed
Ebert, D., Hottinger, J. W. and Pajunen, V. I. (2001). Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82, 3417–3434.Google Scholar
Ebert, D., Lipsitch, M. and Mangin, K. L. (2000). The effect of parasites on host population density and extinction: Experimental epidemiology with Daphnia and six microparasites. American Naturalist 156, 459–477.CrossRefGoogle ScholarPubMed
Green, J. (1974). Parasites and epibionts of Cladoceran. Transactions of the Zoological Society of London 32, 417–515.CrossRefGoogle Scholar
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282–290.CrossRefGoogle Scholar
Hatai, K. and Hoshiai, G.-I. (1993). Characteristics of two Saprolegnia species isolated from coho salmon with saprolegniosis. Journal of Aquatic Animal Health 5, 115–118.2.3.CO;2>CrossRefGoogle Scholar
Kiesecker, J. M. and Blaustein, A. R. (1999). Pathogen reverses competition between larval amphibians. Ecology 80, 2442–2448.CrossRefGoogle Scholar
Kiesecker, J. M., Blaustein, A. R. and Miller, C. L. (2001). Transfer of a pathogen from fish to amphibians. Conservation Biology 15, 1064–1070.CrossRefGoogle Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kitancharoen, N., Yuasa, K. and Hatai, K. (1996). Effects of pH and temperature on growth of Saprolegnia diclina and S. parasitica isolated from various sources. Mycoscience 37, 385–390.CrossRefGoogle Scholar
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle ScholarPubMed
Lampert, W. and Sommer, U. (1999). Limnoökologie, 2nd Edn. Georg Thieme Verlag, Stuttgart and New York.Google Scholar
Leclerc, M. C., Guillot, J. and Deville, M. (2000). Taxonomic and phylogenetic analysis of Saprolegniaceae (Oomycetes) inferred from LSU rDNA and ITS sequence comparisons. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 77, 369–377.CrossRefGoogle ScholarPubMed
Little, T. J. and Ebert, D. (1999). Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera). Journal of Animal Ecology 68, 134–149.CrossRefGoogle Scholar
Martin, M. P., Raidl, S. and Tellaria, M. T. (2004). Molecular analysis confirms the relationship between Stephanospora caroticolor and Lidtneria trachyspora. Mycotaxon 90, 133–140.Google Scholar
O'Donnell, K. (1993). Fusarium and its near relatives. In The Fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics (ed.Reynolds, D. R. and Taylor, J. W.), pp. 225–233. CAB International, Wallingford, UK.Google Scholar
Prowse, G. A. (1954). Aphanomyces daphniae sp. nov. parasitic on Daphnia hyalina. Transactions of the British Mycological Society 37, 22–28.CrossRefGoogle Scholar
Riethmuller, A., Weiss, M. and Oberwinkler, F. (1999). Phylogenetic studies of Saprolegniomycetidae and related groups based on nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany-Revue Canadienne De Botanique 77, 1790–1800.CrossRefGoogle Scholar
Scott, W. (1961). A monograph of the genus Aphanomyces. Virginia Agricultural Experiment Station. Blacksburg, Virginia. Technical Bulletin 151, 1–95.Google Scholar
Stazi, A. V., Mantovani, A., Fuglieni, F. and Di Delupis, G. L. D. (1994). Observations on fungal infection of the ovary of laboratory-cultured Daphnia magna. Bulletin of Environmental Contamination and Toxicology 53, 699–703.CrossRefGoogle ScholarPubMed
Tellenbach, C., Wolinska, J. and Spaak, P. (2007). Epidemiology of a Daphnia brood parasite and its implications on host life-history traits. Oecologia 154, 369–375.CrossRefGoogle ScholarPubMed
Tompkins, D. M., Greenman, J. V., Robertson, P. A. and Hudson, P. J. (2000). The role of shared parasites in the exclusion of wildlife hosts: Heterakis gallinarum in the ring-necked pheasant and the grey partridge. Journal of Animal Ecology 69, 829–840.CrossRefGoogle ScholarPubMed
Vallin, S. (1951). Plankton mortality in the northern Baltic caused by a parasitic water-mould. Institute of Freshwater Research, Drottningholm, Sweden. Annual Report 32, 139–148.Google Scholar
Wolinska, J., Keller, B., Manca, M. and Spaak, P. (2007). Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection. Journal of Animal Ecology 76, 191–200.CrossRefGoogle ScholarPubMed
Wood, S. E. and Willoughby, L. G. (1986). Ecological observations on the fungal colonization of fish by Saprolegniaceae in Windermere. Journal of Applied Ecology 23, 737–749.CrossRefGoogle Scholar