Europe; Microscopy; Oomycetes; Oomycetes: genetics; Oomycetes: isolation purification; Phaeophyta; Phaeophyta: microbiology; Plant Diseases; Plant Diseases: microbiology; Polymerase Chain Reaction; Polymerase Chain Reaction: methods; Sensitivity and Specificity; South America; Water Microbiology
Abstract :
[en] In the marine environment, a growing body of evidence points to parasites as key players in the control of population dynamics and overall ecosystem structure. However, their prevalence and impact on marine macroalgal communities remain virtually unknown. Indeed, infectious diseases of seaweeds are largely underdocumented, partly because of the expertise required to diagnose them with a microscope. Over the last few years, however, real-time quantitative PCR (qPCR) has emerged as a rapid and reliable alternative to visual symptom scoring for monitoring pathogens. Thus, we present here a qPCR assay suitable for the detection and quantification of the intracellular oomycete pathogen Eurychasma dicksonii in its ectocarpalean and laminarialean brown algal hosts. qPCR and microscopic observations made of laboratory-controlled cultures revealed that clonal brown algal strains exhibit different levels of resistance against Eurychasma, ranging from high susceptibility to complete absence of symptoms. This observation strongly argues for the existence of a genetic determinism for disease resistance in brown algae, which would have broad implications for the dynamics and genetic structure of natural populations. We also used qPCR for the rapid detection of Eurychasma in filamentous brown algae collected in Northern Europe and South America and found that the assay is specific, robust, and widely applicable to field samples. Hence, this study opens the perspective of combining large-scale disease monitoring in the field with laboratory-controlled experiments on the genome model seaweed Ectocarpus siliculosus to improve our understanding of brown algal diseases.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Gachon, Claire M. M.
Strittmatter, Martina
Müller, Dieter G.
Kleinteich, Julia ; Université de Liège - ULiège > Département des sciences de la vie > Physiologie et génétique bactériennes
Küpper, Frithjof C.
Language :
English
Title :
Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal.
Publication date :
2009
Journal title :
Applied and Environmental Microbiology
ISSN :
0099-2240
eISSN :
1098-5336
Publisher :
American Society for Microbiology, Washington, United States - District of Columbia
Aleem, A. 1955. Marine fungi from the west-coast of Sweden. Ark. Bot. 3:1-33.
Allen, R., P. D. Bittner-Eddy, L. J. Grenville-Briggs, J. Meitz, A. Rehmany, L. Rose, and J. L. Beynon. 2004. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306:1957-1960.
Bouarab, K., B. Kloareg, P. Potin, and J. A. Correa. 2001. Ecological and biochemical aspects in algal infectious diseases. Cah. Biol. Mar. 42:91-100.
Canter, H. M., and G. Jaworski. 1979. The occurrence of a hypersensitive reaction in the planktonic diatom Asterionella formosa Hassall parasitized by the chytrid Rhizophydium planktonicum Canter emend., in culture. New Phytol. 82:187-206.
Carey, C. 2000. Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environ. Health Perspect. 108:143-150.
Charrier, B., S. M. Coelho, A. Le Bail, T. Tonon, G. Michel, P. Potin, B. Kloareg, C. Boyen, A. F. Peters, and J. M. Cock. 2008. Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol. 177:319-332.
De Bruin, A., B. W. Ibelings, M. Rijkeboer, M. Brehm, and E. van Donk. 2004. Genetic variation in Asterionella formosa (Bacillariophyceae): is it linked to frequent epidemics of host-specific parasitic fungi? J. Phycol. 40:823-830.
Duffy, M. A., and L. Sivars-Becker. 2007. Rapid evolution and ecological host-parasite dynamics. Ecol. Lett. 10:44-53.
Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548.
Gachon, C. M. M., J. G. Day, C. N. Campbell, T. Pröschold, R. J. Saxon, and F. C. Küpper. 2007. The Culture Collection of Algae and Protozoa (CCAP): a biological resource for protistan genomics. Gene doi:10.1016/j.gene.2007.05.018.
Gachon, C. M. M., A. Mingam, and B. Charrier. 2004. Real-time PCR: what relevance to plant studies? J. Exp. Bot. 55:1445-1454.
Gachon, C. M. M., and P. Saindrenan. 2004. Real-time PCR monitoring of fungal development in Arabidopsis thaliana infected by Alternaria brassicicola and Botrytis cinerea. Plant Physiol. Biochem. 42:367-371.
Grahame, E. S. 1976. The occurrence of Lagenisma coscinodisci in Palmeria hardmania from Kingston harbour, Jamaica. Br. Phycol. J. 11:57-61.
Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
Harvell, C. D., K. Kim, J. M. Burkholder, R. R. Colwell, P. R. Epstein, D. J. Grimes, E. E. Hofmann, E. K. Lipp, A. Osterhaus, R. M. Overstreet, J. W. Porter, G. W. Smith, and G. R. Vasta. 1999. Review: marine ecology - emerging marine diseases - climate links and anthropogenic factors. Science 285:1505-1510.
Hoarau, G., J. A. Coyer, W. T. Stam, and J. L. Olsen. 2007. A fast and inexpensive DNA extraction/purification protocol for brown macroalgae. Mol. Ecol. Notes 7:191-193.
Holfeld, H. 1998. Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol. 138:507-517.
Holub, E. B. 2007. Natural variation in innate immunity of a pioneer species. Curr. Opin. Plant Biol. 10:415-424.
Hughes, T. P. 1994. Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265:1547-1551.
Jones, K. E., N. G. Patel, M. A. Levy, A. Storeygard, D. Balk, J. L. Gittleman, and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature 451:990-993.
Küpper, F. C., I. Maier, D. G. Müller, S. L.-D. Goer, and L. Guillou. 2006. Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Cohn. Cryptogam. Algol. 27:165-184.
Küpper, F. C., and D. G. Müller. 1999. Massive occurrence of the heterokont and fungal parasites Anisolpidium, Eurychasma and Chytridium in Pylaiella littoralis (Ectocarpales, Phaeophyceae). Nova Hedwigia 69:381-389.
Marin, B., A. Palm, M. Klingberg, and M. Melkonian. 2003. Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154:99-145.
Martínez Martínez, J., D. C. Schroeder, A. Larsen, G. Bratbak, and W. H. Wilson. 2007. Molecular dynamics of Emiliania huxleyi and co-occurring viruses during two separate mesocosm studies. Appl. Environ. Microbiol. 73:554-562.
Muhling, M., N. J. Fuller, A. Millard, P. J. Somerfield, D. Marie, W. H. Wilson, D. J. Scanlan, A. F. Post, I. Joint, and N. H. Mann. 2005. Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ. Microbiol. 7:499-508.
Müller, D. G., F. C. Küpper, and H. Küpper. 1999. Infection experiments reveal broad host ranges of Eurychasma dicksonii (Oomycota) and Chytridium polysiphoniae (Chytridiomycota), two eukaryotic parasites of marine brown algae (Phaeophyceae). Phycol. Res. 47:217-223.
Peters, A., D. Marie, D. Scornet, B. Kloareg, and J. M. Cock. 2004. Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetics and genomics. J. Phycol. 40:1079-1088.
Potin, P., K. Bouarab, J.-P. Salaün, G. Pohnert, and B. Kloareg. 2002. Biotic interactions of marine algae. Curr. Opin. Plant Biol. 5:308-317.
Rose, L., P. D. Bittner-Eddy, C. H. Langley, E. B. Holub, R. W. Michelmore, and J. Beynon. 2004. The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517-1527.
Sekimoto, S., G. W. Beakes, C. M. M. Gachon, D. G. Müller, F. C. Küpper, and D. Honda. 2008. The development, ultrastructural cytology, and molecular phylogeny of the basal oomycete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis. Protist 159:299-318.
Sekimoto, S., K. Yokoo, Y. Kawamura, and D. Honda. 2008. Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, straminipiles), a unicellular obligate endoparasite of Bangia and Porphyra spp. (Bangiales, Rhodophyta). Mycol. Res. 112:361-374.
Sparrow, F. J. 1960. Aquatic phycomycetes, 2nd ed., vol. XV. The University of Michigan Press, Ann Arbor.
Starr, R., and J. Zeikus. 1993. UTEX - the culture collection of algae at the University of Texas at Austin 1993: list of cultures. J. Phycol. 29:S1-S106.
Strittmatter, M., C. M. M. Gachon, and F. C. Küpper. Ecology of lower oomycetes. In K. Lamour and S. Kamoun (ed.), Oomycete genetics and genomics: diversity, plant and animal interactions, and toolbox, in press. John Wiley and Sons, Hoboken, NJ.
Suttle, C. A. 2005. Viruses in the sea. Nature 437:356-361.
Tillmann, U., K. J. Hesse, and A. Tillmann. 1999. Large-scale parasitic infection of diatoms in the Northfrisian Wadden Sea. J. Sea Res. 42:255-261.
West, J. A., T. A. Klochkova, G. H. Kim, and S. Loiseaux-de Goer. 2006. Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: host species susceptibility. Phycol. Res. 54:72-85.
Wilce, R. T., C. W. Schneider, A. V. Quinlan, and K. V. Bosch. 1982. The life history and morphology of free-living Pilayella littoralis (L) Kjellm (Ectocarpaceae, Ectocarpales) in Nahant Bay, Massachusetts. Phycologia 21:336-354.