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Natural distribution and co-infection patterns of microsporidia parasites in the Daphnia longispina complex

Published online by Cambridge University Press:  12 March 2012

S. WEIGL ,
H. KÖRNER ,
A. PETRUSEK ,
J. SEDA  and
J. WOLINSKA
S. WEIGL
Affiliation:
Ludwig-Maximilians-Universität München, Department Biologie II, Großhaderner Strasse 2, 82152 Planegg-Martinsried, Germany
H. KÖRNER
Affiliation:
Department of Neuroimmunology, Institute for Multiple Sclerosis Research, University Medical Center Göttingen and The Hertie Foundation, Göttingen, Germany
A. PETRUSEK
Affiliation:
Charles University in Prague, Faculty of Science, Department of Ecology, Viničná 7, 12844 Prague, Czech Republic
J. SEDA
Affiliation:
Biological Centre AS CR, Institute of Hydrobiology, Na Sádkách 7, 37005 České Budějovice, Czech Republic
J. WOLINSKA*
Affiliation:
Ludwig-Maximilians-Universität München, Department Biologie II, Großhaderner Strasse 2, 82152 Planegg-Martinsried, Germany
*
*Corresponding author: Ludwig-Maximilians-Universität München, Department Biologie II, Großhaderner Strasse 2, 82152 Planegg-Martinsried, Germany. Tel: +49 (0) 89 2180 74 201. Fax: +49 (0) 89 2180 204. E-mail: wolinska@bio.lmu.de
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Summary

Microsporidia are intracellular parasites, frequently infecting the planktonic crustacean Daphnia. Questioning the ability to detect and identify microsporidia with conventional microscopic techniques, we applied molecular methods in order to investigate the distribution and co-infection patterns of this parasite among 8 communities of the Daphnia longispina hybrid complex. Eight microsporidian taxa were detected, including 3 that previously had not been characterized genetically. Microsporidian communities from nearby lakes were found to be more similar to each other, apparently due to short distance dispersal via secondary hosts. Moreover, we detected seasonal (but not interannual) changes in microsporidian community structure. With some microsporidia being host-specific, these changes might have resulted from seasonal changes in host taxon and clonal composition. The 2 dominant and closely related parasite species were found mainly in single infections, whereas another pair of related microsporidians was found predominantly in co-infections; suggesting species-level differences in the ability to colonize infected hosts. By applying molecular methods, we were not only able to unambiguously identify parasite taxa but also to reveal multiple infections that otherwise would have remained undetected. Given the increased level of accuracy and sensitivity, we highly recommend molecular approaches in future parasite surveys of Daphnia infections.

Keywords

co-infectionDaphniamicrosporidiamultiple infectionsparasite distribution
Type
Research Article
Information
Parasitology , Volume 139 , Issue 7 , June 2012 , pp. 870 - 880
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Becnel, J. J. and Andreadis, T. G. (1999). Microsporidia in insects. In The Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 172–195. ASM Press, Washington, USA.Google Scholar
Ben-Ami, F., Rigaud, T. and Ebert, D. (2011). The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. Journal of Evolutionary Biology 24, 1307–1316. doi: 10.1111/j.1420-9101.2011.02264.x.CrossRefGoogle ScholarPubMed
Bengtsson, J. and Ebert, D. (1998). Distributions and impacts of microparasites on Daphnia in a rockpool metapopulation. Oecologia 115, 213–221. doi: 10.1007/s004420050510.CrossRefGoogle Scholar
Brambilla, D. J. (1983). Microsporidiosis in a Daphnia pulex population. Hydrobiologia 99, 175–188. doi: 10.1007/BF00008769.CrossRefGoogle Scholar
Canning, E. U., Barker, R. J., Page, A. M. and Nicholas, J. P. (1985). Transmission of microsporidia, especially Orthosoma operophterae (Canning, 1960) between generations of winter moth Operophtera brumata (Lepidoptera: Geometridae). Parasitology 90, 11–19. doi: 10.1017/S0031182000048976.CrossRefGoogle Scholar
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
de Roode, J. C., Helinski, M. E. H., Anwar, M. A. and Read, A. F. (2005). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. American Naturalist 166, 531–542.CrossRefGoogle ScholarPubMed
Decaestecker, E., Declerck, S., De Meester, L. and Ebert, D. (2005). Ecological implications of parasites in natural Daphnia populations. Oecologia 144, 382–390. doi: 10.1007/s00442-005-0083-7.CrossRefGoogle ScholarPubMed
Ebert, D. (1995). The ecological interactions between a microsporidian parasite and its host Daphnia magna. Journal of Animal Ecology 64, 361–369.CrossRefGoogle Scholar
Ebert, D. (2005). Ecology, Epidemiology, and Evolution of Parasitism in Daphnia. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information. Available from: http://www.ncbi.nlm.nih.gov/books/NBK2036/.Google Scholar
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
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797. doi: 10.1093/nar/gkh340.CrossRefGoogle ScholarPubMed
Franzen, C., Fischer, S., Schroeder, J., Schölmerich, J. and Schneuwly, S. (2005). Morphological and molecular investigations of Tubulinosema ratisbonensis gen. nov., sp. nov. (Microsporidia: Tubulinosematidae fam. nov.), a parasite infecting a laboratory colony of Drosophila melanogaster (Diptera: Drosophilidae). Journal of Eukaryotic Microbiology 52, 141–152. doi: 10.1111/j.1550-7408.2005.04-3324.x.CrossRefGoogle ScholarPubMed
Friedrich, C., Winder, O., Schaffler, K. and Reinthaler, F. F. (1996). Light and electron microscope study on Gurleya daphniae sp. nov. (Microspora, Gurleyidae), a parasite of Daphnia pulex (Crustacea, Phyllopoda). European Journal of Protistology 32, 116–122.CrossRefGoogle Scholar
Green, J. (1974). Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London 32, 417–515.CrossRefGoogle Scholar
Hammer, Ø., Harper, D. A. T. and Ryan, P. D. (2001). PAST paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.Google Scholar
Hirt, R. P., Logsdon, J. M., Healy, B., Dorey, M. W., Doolittle, W. F. and Embley, T. M. (1999). Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proceedings of the National Academy of Sciences, USA 96, 580–585. doi: 10.1073/pnas.96.2.580CrossRefGoogle ScholarPubMed
Hogg, J. C., Ironside, J. E., Sharpe, R. G., Hatcher, M. J., Smith, J. and Dunn, A. M. (2002). Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR. Parasitology 125, 59–63. doi:10.1017/S0031182002001774.CrossRefGoogle ScholarPubMed
Keeling, P. (2009). Five questions about microsporidia. PLoS Pathology 5, e1000489. doi: 10.1371/journal.ppat.1000489.CrossRefGoogle ScholarPubMed
Keeling, P. J. and Fast, N. M. (2002). Microsporidia: Biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56, 93–116. doi:10.1146/annurev.micro.56.012302.160854.CrossRefGoogle ScholarPubMed
Keller, B., Wolinska, J., Tellenbach, C. and Spaak, P. (2007). Reproductive isolation keeps hybridizing Daphnia species distinct. Limnology and Oceanography 52, 984–991.CrossRefGoogle Scholar
Kurtz, J. and Armitage, S. A. O. (2006). Alternative adaptive immunity in invertebrates. Trends in Immunology 27, 493–496. doi: 10.1016/j.it.2006.09.001.CrossRefGoogle ScholarPubMed
Larsson, J. I. R., Ebert, D. and Vávra, J. (1997). Ultrastructural study and description of Ordospora colligata gen. et sp. nov. (Microspora, Ordosporidae fam. nov.), a new microsporidian parasite of Daphnia magna (Crustacea, Cladocera). European Journal of Protistology 33, 432–443.CrossRefGoogle Scholar
Larsson, J. I. R., Ebert, D., Vávra, J. and Voronin, V. N. (1996). Redescription of Pleistophora intestinalis Chatton, 1907, a microsporidian parasite of Daphnia magna and Daphnia pulex, with establishment of the new genus Glugoides (Microspora, Glugeidae). European Journal of Protistology 32, 251–261.CrossRefGoogle Scholar
Lass, S. and Ebert, D. (2006). Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proceedings of the Royal Society of London, B 273, 199–206. doi: 10.1098/rspb.2005.3310.Google ScholarPubMed
Lipsitch, M. and Moxon, E. R. (1997). Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiology 5, 31–37. doi: 10.1016/s0966-842x(97)81772-6.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. doi: 10.1046/j.1365-2656.1999.00271.x.CrossRefGoogle Scholar
Lohr, J., Yin, M. and Wolinska, J. (2010). Prior residency does not always pay off – coinfections in Daphnia. Parasitology 137, 1493–1500.CrossRefGoogle Scholar
McClymont, E. H., Dunn, A. M., Terry, R. S., Rollinson, D., Littlewood, D. T. J. and Smith, J. E. (2005). Molecular data suggest that microsporidian parasites in freshwater snails are diverse. International Journal for Parasitology 35, 1071–1078. doi: 10.1016/j.ijpara.2005.05.008.CrossRefGoogle Scholar
Murphy, T. M., Walochnik, J., Hassl, A., Moriarty, J., Mooney, J., Toolan, D., Sanchez-Miguel, C., O'Loughlin, A. and McAuliffe, A. (2007). Study on the prevalence of Toxoplasma gondii and Neospora caninum and molecular evidence of Encephalitozoon cuniculi and Encephalitozoon (Septata) intestinalis infections in red foxes (Vulpes vulpes) in rural Ireland. Veterinary Parasitology 146, 227–234. doi: 10.1016/j.vetpar.2007.02.017.CrossRefGoogle Scholar
Petney, T. N. and Andrews, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377–393. doi: 10.1016/s0020-7519(97)00189-6.CrossRefGoogle ScholarPubMed
Petrusek, A., Hobaek, A., Nilssen, J. P., Skage, M., Černý, M., Brede, N. and Schwenk, K. (2008 a). A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda). Zoologica Scripta 37, 507–519. doi: 10.1111/j.1463-6409.2008.00336.x.CrossRefGoogle Scholar
Petrusek, A., Seda, J., Macháček, J., Ruthová, Š. and Šmilauer, P. (2008 b). Daphnia hybridization along ecological gradients in pelagic environments: the potential for the presence of hybrid zones in plankton. Philosophical Transactions of the Royal Society, B: Biological Sciences 363, 2931–2941. doi: 10.1098/rstb.2008.0026.CrossRefGoogle ScholarPubMed
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256. doi: 10.1093/molbev/msn083.CrossRefGoogle ScholarPubMed
Refardt, D., Canning, E., Mathis, A., Cheney, S. A., Lafranchi-Tristem, N. J. and Ebert, D. (2002). Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: Cladocera). Parasitology 124, 381–389. doi:10.1017/S0031182001001305.CrossRefGoogle ScholarPubMed
Refardt, D., Decaestecker, E., Johnson, P. T. J. and Vávra, J. (2008). Morphology, molecular phylogeny, and ecology of Binucleata daphniae n. g., n. sp. (Fungi: Microsporidia), a parasite of Daphnia magna Straus, 1820 (Crustacea: Branchiopoda). Journal of Eukaryotic Microbiology 55, 393–408. doi: 10.1111/j.1550-7408.2008.00341.x.CrossRefGoogle Scholar
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574. doi: 10.1093/bioinformatics/btg180.CrossRefGoogle ScholarPubMed
Seda, J., Kolarova, K., Petrusek, A. and Machacek, J. (2007 a). Daphnia galeata in the deep hypolimnion: spatial differentiation of a “typical epilimnetic” species. Hydrobiologia 594, 47–57. doi: 10.1007/s10750-007-9075-4.CrossRefGoogle Scholar
Seda, J., Petrusek, A., Machacek, J. and Smilauer, P. (2007 b). Spatial distribution of the Daphnia longispina species complex and other planktonic crustaceans in the heterogeneous environment of canyon-shaped reservoirs. Journal of Plankton Research 29, 619–628. doi: 10.1093/plankt/fbm044.CrossRefGoogle Scholar
Slothouber Galbreath, J., Smith, J. E., Becnel, J. J., Butlin, R. and Dunn, A. M. (2010). Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Biological Invasions 12, 191–209. doi: 10.1007/s10530-009-9442-3.CrossRefGoogle Scholar
Slothouber Galbreath, J., Smith, J. E., Terry, R. S., Becnel, J. J. and Dunn, A. M. (2003). Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. International Journal for Parasitology 34, 235–244. doi: 10.1016/j.ijpara.2003.10.009.Google Scholar
Sokal, R. R. and Rohlf, F. J. (1995). Biometry: the Principles and Practice of Statistics in Biological Research, 3rd Edn.W.H. Freeman and Co, San Francisco, CA, USA.Google Scholar
Solter, L. F. and Maddox, J. V. (1998). Physiological host specificity of microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71, 207–216. doi: 10.1006/jipa.1997.4740.CrossRefGoogle ScholarPubMed
Spaak, P. (1996). Temporal changes in the genetic structure of the Daphnia species complex in Tjeukemeer, with evidence for backcrossing. Heredity 76, 539–548. doi: 10.1038/hdy.1996.77.CrossRefGoogle Scholar
Stirnadel, H. A. and Ebert, D. (1997). Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. Journal of Animal Ecology 66, 212–222.CrossRefGoogle Scholar
Sweeney, A. W., Hazard, E. I. and Graham, M. F. (1985). Intermediate host for an Amblyospora sp. (Microspora) infecting the mosquito, Culex annulirostris. Journal of Invertebrate Pathology 46, 98–102. doi: 10.1016/0022-2011(85)90133-8.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2000). PAUP*: Phylogenetic Analysis using Parsimony (and Other Methods). Version 4. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739. doi: 10.1093/molbev/msr121.CrossRefGoogle ScholarPubMed
Vávra, J. (1964). A failure to produce artificial infection in cladoceran microsporidia. Journal of Protozoology 11, 35–36.Google Scholar
Vávra, J., Hyliš, M., Oborník, M. and Vossbrinck, C. R. (2005). Microsporidia in aquatic microcrustacea: the copepod microsporidium Marssoniella elegans Lemmermann, 1900 revisited. Folia Parasitologica 52, 163–172.CrossRefGoogle ScholarPubMed
Vávra, J. and Larsson, J. I. R. (1994). Berwaldia schaefernai (Jírovec, 1937) comb. n. (Protozoa, Microsporida), fine-structure, life-cycle, and relationship to Berwaldia singularis Larsson, 1981. European Journal of Protistology 30, 45–54.CrossRefGoogle Scholar
Vidtman, S. S. and Sokolova, Y. Y. (1994). The description of the new genus Larssonia gen. n. based on the ultrastructural analysis of Microsporidium (Pleistophora) obtusa from Daphnia pulex. Parazitologyia 28, 202–213.Google Scholar
Vivarès, C. P. and Méténier, G. (2001). The microsporidian Encephalitozoon. BioEssays 23, 194–202. doi: 10.1002/1521-1878(200102)23:2<194::aid-bies1027>3·0.co;2-d.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Vossbrinck, C. R., Andreadis, T. G., Vávra, J. and Becnel, J. J. (2004). Molecular phylogeny and evolution of mosquito parasitic microsporidia (Microsporidia: Amblyosporidae). Journal of Eukaryotic Microbiology 51, 259–261. doi: 10.1111/j.1550-7408.2004.tb00167.x.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131–142.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R., Maddox, J. V., Friedman, S., Debrunner-Vossbrinck, B. A. and Woese, C. R. (1987). Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature, London 326, 411–414. doi: 10.1038/326411a0.CrossRefGoogle ScholarPubMed
Williams, B. A. P., Hirt, R. P., Lucocq, J. M. and Embley, T. M. (2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature, London 418, 865–869. doi: 10.1038/nature00949.CrossRefGoogle ScholarPubMed
Wolinska, J., Giessler, S. and Koerner, H. (2009). Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Applied and Environmental Microbiology 75, 7051–7059. doi: 10.1128/AEM.01306-09.CrossRefGoogle ScholarPubMed
Wolinska, J., Keller, B., Bittner, K., Lass, S. and Spaak, P. (2004). Do parasites lower Daphnia hybrid fitness? Limnology and Oceanography 49, 1401–1407.CrossRefGoogle 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. doi: 10.1111/j.1365-2656.2006.01177.x.CrossRefGoogle ScholarPubMed
Wolinska, J., Seda, J., Koerner, H., Smilauer, P. and Petrusek, A. (2011a). Spatial variation of Daphnia parasite load within individual waterbodies. Journal of Plankton Research 33, 1284–1294. doi: 10.1093/plankt/fbr016.CrossRefGoogle Scholar
Wolinska, J., Spaak, P., Koerner, H., Petrusek, A., Seda, J. and Giessler, S. (2011b). Transmission mode affects the population genetic structure of Daphnia parasites. Journal of Evolutionary Biology 24, 265–273. doi: 10.1111/j.1420-9101.2010.02163.x.CrossRefGoogle ScholarPubMed
Yan, N. D. and Larsson, J. I. R. (1988). Prevalence and inferred effects of microsporidia of Holopedium gibberum (Crustacea:Cladocera) in a Canadian Shield lake. Journal of Plankton Research 10, 875–886. doi: 10.1093/plankt/10.5.875.CrossRefGoogle Scholar
Yin, M., Wolinska, J. and Gießler, S. (2010). Clonal diversity, clonal persistence and rapid taxon replacement in natural populations of species and hybrids of the Daphnia longispina complex. Molecular Ecology 19, 4168–4178. doi: 10.1111/j.1365-294X.2010.04807.x.CrossRefGoogle ScholarPubMed
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