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MtDNA allows the sensitive detection and haplotyping of the crayfish plague disease agent Aphanomyces astaci showing clues about its origin and migration

Published online by Cambridge University Press:  26 February 2018

Jenny Makkonen*
Affiliation:
Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 1627, FI-70211, Kuopio, Finland
Japo Jussila
Affiliation:
Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 1627, FI-70211, Kuopio, Finland
Jörn Panteleit
Affiliation:
University of Koblenz-Landau, Institute for Environmental Sciences, Fortstrasse 7, D-76829 Landau, Germany
Nina Sophie Keller
Affiliation:
University of Koblenz-Landau, Institute for Environmental Sciences, Fortstrasse 7, D-76829 Landau, Germany Helmholtz-Centre for Environmental Research (UfZ), Department of Isotope Biogeochemistry, Permoserstrasse 15, D-04318 Leipzig, Germany
Anne Schrimpf
Affiliation:
University of Koblenz-Landau, Institute for Environmental Sciences, Fortstrasse 7, D-76829 Landau, Germany
Kathrin Theissinger
Affiliation:
University of Koblenz-Landau, Institute for Environmental Sciences, Fortstrasse 7, D-76829 Landau, Germany
Raine Kortet
Affiliation:
Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 111, FI-80101, Joensuu, Finland
Laura Martín-Torrijos
Affiliation:
Department of Mycology, Real Jardín Botánico CSIC, Plaza de Murillo 2, ES-28014 Madrid, Spain
Jose Vladimir Sandoval-Sierra
Affiliation:
Department of Mycology, Real Jardín Botánico CSIC, Plaza de Murillo 2, ES-28014 Madrid, Spain
Javier Diéguez-Uribeondo
Affiliation:
Department of Mycology, Real Jardín Botánico CSIC, Plaza de Murillo 2, ES-28014 Madrid, Spain
Harri Kokko
Affiliation:
Department of Environmental and Biological Sciences, University of Eastern Finland, P.O. Box 1627, FI-70211, Kuopio, Finland
*
Author for correspondence: Jenny Makkonen, E-mail: [email protected]

Abstract

The oomycete Aphanomyces astaci, the causative agent of crayfish plague, is listed as one of the 100 worst invasive species in the world, destroying the native crayfish populations throughout Eurasia. The aim of this study was to examine the potential of selected mitochondrial (mt) genes to track the diversity of the crayfish plague pathogen A. astaci. Two sets of primers were developed to amplify the mtDNA of ribosomal rnnS and rnnL subunits. We confirmed two main lineages, with four different haplogroups and five haplotypes among 27 studied A. astaci strains. The haplogroups detected were (1) the A-haplogroup with the a-haplotype strains originating from Orconectes sp., Pacifastacus leniusculus and Astacus astacus; (2) the B-haplogroup with the b-haplotype strains originating from the P. leniusculus; (3) the D-haplogroup with the d1 and d2-haplotypes strains originating from Procambarus clarkii; and (4) the E-haplogroup with the e-haplotype strains originating from the Orconectes limosus. The described markers are stable and reliable and the results are easily repeatable in different laboratories. The present method has high applicability as it allows the detection and characterization of the A. astaci haplotype in acute disease outbreaks in the wild, directly from the infected crayfish tissue samples.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Abrahamsson, S (1969) Signal kräftan – erfarenheter från USA och aspekter på dess inplantering i sverige. Fauna och Flora 64, 109116. In Swedish.Google Scholar
Abrahamsson, S, (1972) The crayfish Astacus astacus L. in Sweden and the introduction of the American crayfish Pacifastacus leniusculus. Freshwater Crayfish 1, 2740.Google Scholar
Agerberg, A and Jansson, H (1995) Allozymic comparisons between three subspecies of the freshwater crayfish Pacifastacus leniusculus (Dana), and between populations introduced to Sweden. Hereditas 122(1), 3339.Google Scholar
Alderman, DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Scientific and Technical Review of the Office International des Epizooties (Paris) 15, 603632.Google Scholar
Cerenius, L, Andersson, MG and Söderhäll, K (2009) Aphanomyces astaci and Crustaceans. In Lamour, K and Kamoun, S (eds). Oomycete Genetics and Genomics: Diversity, Interactions, and Research Tools. Hoboken, NJ, USA: John Wiley & Sons, Inc., pp. 425433.Google Scholar
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9(10), 16571660.Google Scholar
Diéguez-Uribeondo, J and Söderhäll, K (1993) Procambarus clarkii Girard as a vector for the crayfish plague fungus, Aphanomyces astaci Schikora. Aquaculture and Fisheries Management 24, 761765.Google Scholar
Diéguez-Uribeondo, J, Huang, TS and Cerenius, L (1995) Physiological adaptation of an Aphanomyces astaci strain isolated from the freshwater crayfish Procambarus clarkii. Mycological Research 99, 574578.Google Scholar
Diéguez-Uribeondo, J, Garcia, MA, Cerenius, L, Kozubíková, E, Ballesteros, I, Windels, C, Weiland, J, Kator, H, Söderhäll, K and Martin, MP (2009) Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (Oomycetes). Fungal Genetics and Biology 46, 365376.Google Scholar
Goldman, CR (1972) Ecology and physiology of the Californian crayfish Pacifastacus leniusculus (Dana) in relation to its suitability for introduction into European waters. Freshwater Crayfish 1, 105120.Google Scholar
Grandjean, F, Vrålstad, T, Diéguez-Uribeondo, J, Jelić, M, Mangombi, J, Delaunay, C, Filipová, L, Rezinciuc, S, Kozubíková-Balcarová, E, Guyonnet, D, Viljamaa-Dirks, S and Petrusek, A (2014) Microsatellite markers for direct genotyping of the crayfish plague pathogen Aphanomyces astaci (oomycetes) from infected host tissues. Veterinary Microbiology 170(3–4), 317324.Google Scholar
Hebert, Paul DN, Ratnasingham, S and Waard, RD (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B, Biological sciences 270(1), 9699.Google Scholar
Holdich, DM 2002. Biology of Freshwater Crayfish. Oxford, UK: Blackwell Science.Google Scholar
Huang, TS, Cerenius, L and Söderhäll, K (1994) Analysis of genetic diversity in the crayfish plague fungus, Aphanomyces astaci, by random amplification of polymorphic DNA. Aquaculture 126, 19.Google Scholar
International Union For Conservation of Nature (IUCN), (2012) The IUCN red list of threatened species. Version 2012.2. Available at http://www.iucnredlist.org (Accessed 11.04.2017).Google Scholar
Jussila, J, Kokko, H, Kortet, R and Makkonen, J (2013) Aphanomyces astaci PsI-genotype isolates from different Finnish signal crayfish stocks show variation in their virulence but still kill fast. Knowledge and Management of Aquatic Ecosystems 411, 10.Google Scholar
Jussila, J, Vrezec, A, Makkonen, J, Kortet, R and Kokko, H (2015) Invasive crayfish and their invasive diseases in Europe with the focus on the virulence evolution of the crayfish plague. In Canning-Clode, J (ed.). Biological Invasions in Changing Ecosystems. Vectors, Ecological Impacts, Management and Predictions. Warsaw, Poland: De Gruyter Ltd, pp. 183211.Google Scholar
Jussila, J, Vrezec, A, Jaklič, T, Kukkonen, H, Makkonen, J and Kokko, H (2017) Virulence of Aphanomyces astaci isolate from latently infected stone crayfish (Austropotamobius torrentium) population. Journal of Invertebrate Pathology 149, 1520.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 16471649.Google Scholar
Keller, NS, Pfeifferm, M, Roessink, I, Schulz, R and Schrimpf, A (2014) First evidence of crayfish plague agent in populations of the marbled crayfish (Procambarus fallax forma virginalis). Knowledge and Management of Aquatic Ecosystems 414, 15.Google Scholar
Kozubíková, E, Viljamaa-Dirks, S, Heinikainen, S and Petrusek, A (2011) Spiny-cheek crayfish Orconectes limosus carry a novel genotype of the crayfish plague pathogen Aphanomyces astaci. Journal of Invertebrate Pathology 108, 214216.Google Scholar
Kozubíková-Balcarová, E, Koukol, O, Martín, MP, Svoboda, J, Petrusek, A and Diéguez-Uribeondo, J (2013) The diversity of oomycetes on crayfish: morphological vs. molecular identification of cultures obtained while isolating the crayfish plague pathogen. Fungal Biology 117(10), 682691.Google Scholar
Larson, ER, Abbot, C, Usio, N, Azuma, N, Wood, K, Herborg, LM and Olden, JD (2012) The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific Northwest range of Pacifastacus leniusculus. Freshwater Biology 57(9), 18231838.Google Scholar
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6(9), 11101116.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Lowe, S, Browne, M, Boudjelas, S and De Poorter, M (2004) 100 of the World's Worst Invasive Alien Species: A Selection From the Global Invasive Species Database. Auckland, New Zealand: The invasive species specialist group (ISSG), a specialist group of the species survival commission (SSC) of the world conservation union (IUCN).Google Scholar
Lyko, F (2017) The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa 4363, 544552.Google Scholar
Maguire, I, Jelić, M, Klobučar, G, Delpy, M, Delaunay, C and Grandjean, F (2016) Prevalence of the pathogen Aphanomyces astaci in freshwater crayfish populations in Croatia. Diseases of Aquatic Organisms 118(1), 4553.Google Scholar
Makkonen, J, Jussila, J, Henttonen, P and Kokko, H (2011) Genetic variation in the ribosomal internal transcribed spacers of Aphanomyces astaci Schikora from Finland. Aquaculture 311, 4853.Google Scholar
Makkonen, J, Jussila, J and Kokko, H (2012a) The diversity of the pathogenic Oomycete (Aphanomyces astaci) chitinase genes within the genotypes indicate adaptation to its hosts. Fungal Genetics and Biology 49, 635642.Google Scholar
Makkonen, J, Jussila, J, Kortet, R, Vainikka, A and Kokko, H (2012b) Differing virulence of Aphanomyces astaci isolates and elevated resistance of noble crayfish Astacus astacus against crayfish plague. Diseases of Aquatic Organisms 102, 129136.Google Scholar
Makkonen, J, Kokko, H, Vainikka, A, Kortet, R and Jussila, J (2014) Dose-dependent mortality of the noble crayfish (Astacus astacus) to different strains of the crayfish plague (Aphanomyces astaci). Journal of Invertebrate Pathology 115(1), 8691.Google Scholar
Makkonen, J, Vesterbacka, A, Martin, F, Jussila, J, Diéguez-Uribeondo, J, Kortet, R and Kokko, H (2016) Mitochondrial genomes and comparative genomics of Aphanomyces astaci and Aphanomyces invadans. Scientific Reports 6, 36089.Google Scholar
Martin, MD, Cappellini, E, Samaniego, JA, Zepeda, ML, Campos, PF, Seguin-Orlando, A, Wales, N, Orlando, L, Ho, SY, Dietrich, FS, Mieczkowski, PA, Heitman, J, Willerslev, E, Krogh, A, Ristaino, JB and Gilbert, MTP (2013) Reconstructing genome evolution in historic samples of the Irish potato famine pathogen. Nature Communications 4, 2172.Google Scholar
Martin, MD, Ho, SYH, Wales, N, Ristaino, JB and Gilbert, TP (2014) Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant new world Phytophthora infestans. Molecular Biology and Evolution 31, 14141420.Google Scholar
Panteleit, J, Keller, NK, Kokko, H, Jussila, J, Makkonen, J, Theissinger, K and Schrimpf, A (2017) Investigation of ornamental crayfish reveals new carrier species of the crayfish plague pathogen (Aphanomyces astaci). Aquatic Invasions 12(1), 7783.Google Scholar
Peiró, df, Almerão, MP, Delaunay, C, Jussila, J, Makkonen, J, Bouchon, D, Araujo, PB and Souty-Grosset, C (2016) First detection of the crayfish plague pathogen Aphanomyces astaci in South America: a high potential risk to native crayfish. Hydrobiologia 781(1), 181190.Google Scholar
Rambaut, A (2012) Figtree_v1.4.0. Available from: http://tree.bio.ed.ac.uk/software/figtree/ [cited 29. September 2017].Google Scholar
Rezinciuc, S, Galindo, J, Montserrat, J and Diéguez-Uribeondo, J (2014) AFLP-PCR and RAPD-PCR evidences of the transmission of the pathogen Aphanomyces astaci (oomycetes) to wild populations of European crayfish from the invasive crayfish species, Procambarus clarkii. Fungal Biology 118(7), 612620.Google Scholar
Rezinciuc, S, Sandoval-Sierra, J, Oidtmann, B and Diéguez-Uribeondo, J (2015) The biology of crayfish plague pathogen Aphanomyces astaci: current answers to most frequent questions. In Kawai, T, Faulkes, Z and Scholtz, G (eds). Freshwater Crayfish. San Diego, USA: CRC Press, pp. 182204Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3), 539542.Google Scholar
Rozen, S and Skaletsky, H (2000) Primer3 on the www for general users and for biologist programmers. Methods in Molecular Biology 132, 365386.Google Scholar
Schrimpf, A, Chucholl, C, Schmidt, T and Schulz, R (2013) Crayfish plague agent detected in populations of the invasive North American crayfish Orconectes immunis (Hagen, 1870) in the Rhine River, Germany. Aquatic Invasions 8(1), 103109.Google Scholar
Scholtz, G, Braband, A, Tolley, L, Reimann, A, Mittmann, B, Lukhaup, C, Steuerwald, F and Vogt, G (2003) Ecology: parthenogenesis in an outsider crayfish. Nature 421, 806.Google Scholar
Silvestro, D and Michalak, I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12, 335337.Google Scholar
Souty-Grosset, C, Holdich, DM, Noël, PY, Reynolds, J and Haffner, P (2006) Atlas of Crayfish in Europe. Paris, France: Muséum National d'Histoire Naturelle.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 13121313.Google Scholar
Söderhäll, K and Cerenius, L (1999) The crayfish plague fungus: history and recent advances. Freshwater Crayfish 12, 1135.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12), 27252729.Google Scholar
Viljamaa-Dirks, S, Heinikainen, S, Torssonen, H, Pursiainen, M, Mattila, J and Pelkonen, S (2013) Distribution and epidemiology of genotypes of the crayfish plague agent Aphanomyces astaci from noble crayfish Astacus astacus in Finland. Diseases of Aquatic Organisms 103(3), 199208.Google Scholar
Vrålstad, T, Knutsen, AK, Tengs, T and Holst-Jensen, A (2009) A quantitative TaqMan(R) MGB real-time polymerase chain reaction based assay for detection of the causative agent of crayfish plague Aphanomyces astaci. Veterinary Microbiology 137, 146155.Google Scholar
Westman, K (1972) The population of the crayfish Astacus astacus L. in Finland and the introduction of the American crayfish Pacifastacus leniusculus Dana. Freshwater Crayfish 1, 4155.Google Scholar
Westman, K (2000) Comparison of the crayfish Pacifastacus leniusculus Dana, a species introduced into Finland, with the native species, Astacus astacus L., in allopatry and sympatry. PhD thesis, University of Helsinki, Helsinki, Finland.Google Scholar
Yoshida, K, Schuenemann, VJ, Cano, LM, Pais, M, Mishra, B, Sharma, R, Lanz, C, Martin, F, Kamoun, S, Krause, J, Thines, M, Weigel, D and Burbano, H (2013) The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2, e00731.Google Scholar
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