Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-28T12:45:15.588Z Has data issue: false hasContentIssue false

Improved method for genotyping the causative agent of crayfish plague (Aphanomyces astaci) based on mitochondrial DNA

Published online by Cambridge University Press:  12 April 2019

Diana Minardi*
Affiliation:
Biosciences, University of Exeter, Stocker Road, EX4 4QD, Exeter, UK Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, DT4 8UB, Weymouth, UK The Centre for Sustainable Aquaculture Futures, UK
David J. Studholme
Affiliation:
Biosciences, University of Exeter, Stocker Road, EX4 4QD, Exeter, UK
Birgit Oidtmann
Affiliation:
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, DT4 8UB, Weymouth, UK
Tobia Pretto
Affiliation:
National Reference Laboratory for Fish, Crustacean and Mollusc Pathologies, Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe), Viale dell'Università, 10, 35020, Legnaro, Padova, Veneto, Italy
Mark van der Giezen
Affiliation:
Biosciences, University of Exeter, Stocker Road, EX4 4QD, Exeter, UK The Centre for Sustainable Aquaculture Futures, UK
*
Author for correspondence: Diana Minardi, E-mail: [email protected]

Abstract

Aphanomyces astaci causes crayfish plague, which is a devastating disease of European freshwater crayfish. The likely first introduction of A. astaci into Europe was in the mid-19th century in Italy, presumably with the introduction of North American crayfish. These crayfish can carry A. astaci in their cuticle as a benign infection. Aphanomyces astaci rapidly spread across Europe causing the decline of the highly susceptible indigenous crayfish species. Random amplified polymorphic DNA-PCR analysis of A. astaci pure cultures characterized five genotype groups (A, B, C, D and E). Current A. astaci genotyping techniques (microsatellites and genotype-specific regions, both targeting nuclear DNA) can be applied directly to DNA extracted from infected cuticles but require high infection levels. Therefore, they are not suitable for genotyping benign infections in North American crayfish (carriers). In the present study, we combine bioinformatics and molecular biology techniques to develop A. astaci genotyping molecular markers that target the mitochondrial DNA, increasing the sensitivity of the genotyping tools. The assays were validated on DNA extracts of A. astaci pure cultures, crayfish tissue extractions from crayfish plague outbreaks and tissue extractions from North American carriers. We demonstrate the presence of A. astaci genotype groups A and B in UK waters.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

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.)

Footnotes

*

Current Address: Future Animal & Public Health, Endemics & Traceability, Animal & Plant Health, Department for Environment, Food and Rural Affairs (Defra), Nobel House, 17 Smith Square, SW1P 3JR, London, UK.

References

Alderman, DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Revue Scientifique et Technique (International Office of Epizootics) 15, 603632.Google Scholar
Alderman, DJ (2003) Aphanomycosis of crayfish: crayfish plague. Research and Development Technical Report W2-064. Cefas, Weymouth.Google Scholar
Alderman, DJ, Polglase, JL, Frayling, M and Hogger, J (1984) Crayfish plague in Britain. Journal of Fish Diseases 7, 401405.Google Scholar
Bankevich, A, Nurk, S, Antipov, D, Gurevich, AA, Dvorkin, M, Kulikov, AS, Lesin, VM, Nikolenko, SI, Pham, S, Prjibelski, AD, Pyshkin, AV, Sirotkin, AV, Vyahhi, N, Tesler, G, Alekseyev, MA and Pevzner, PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19, 455477.Google Scholar
Bennett, A, Ponder, MM and Garcia-Diaz, J (2018) Phoma infections: classification, potential food sources, and their clinical impact. Microorganisms 6, 58.Google Scholar
Chen, X and Sullivan, PF (2003) Single nucleotide polymorphism genotyping: biochemistry, protocol, cost and throughput. Pharmacogenomics Journal 3, 7796.Google Scholar
Clarke, CR, Studholme, DJ, Hayes, B, Runde, B, Weisberg, A, Cai, R, Wroblewski, T, Daunay, M-C, Wicker, E, Castillo, JA and Vinatzer, BA (2015) Genome-enabled phylogeographic investigation of the quarantine pathogen Ralstonia solanacearum race 3 biovar 2 and screening for sources of resistance against its core effectors. Phytopathology 105, 597607.Google Scholar
Czeczuga, B, Kiziewicz, B and Gruszka, P (2004) Pallasea quadrispinosa G.O. Sars specimens as vectors of aquatic zoosporic fungi parasiting on fish. Polish Journal of Environmental Studies 13, 361366.Google Scholar
Czeczuga, B, Godlewska, A, Czeczugasrmeniuk, E, Semeniuk, A and Muszyńska, E (2015) Influence on mycotal species diversity by different stem parts of submerged aquatic plants that inhibit the growth of aquatic organisms. Nova Hedwigia 101, 335345.Google Scholar
Diéguez-Uribeondo, J and Söderhäll, K (1993) Procambarus clarkii Girard as a vector for the crayfish plague fungus Aphanomyces astaci. Aquaculture Research 24, 761775.Google Scholar
Diéguez-Uribeondo, J, Huang, T, Cerenius, L and Söderhäll, K (1995) Physiological adaptation of an Aphanomyces astaci strain isolated from the freshwater crayfish Procambarus clarkii. Mycological Research 99, 574578.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, 317324.Google Scholar
Grandjean, F, Roques, JAC, Delaunay, C, Petrusek, A, Becking, T and Collas, M (2017) Status of Pacifastacus leniusculus and its role in recent crayfish plague outbreaks in France: improving knowledge on distribution and crayfish plague infection patterns. Aquatic Invasions 12, 541549.Google Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Holdich, DM and Reeve, ID (1991) Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquatic Conservation: Marine and Freshwater Ecosystems 1, 139158.Google Scholar
Holdich, DM, Reynolds, JD, Souty-Grosset, C and Sibley, PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems 11, 394395.Google Scholar
Holdich, DM, James, J, Jackson, C and Peay, S (2014) The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain. Ethology Ecology & Evolution 26, 232262.Google Scholar
Huang, T, 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
James, J, Nutbeam-Tuffs, S, Cable, J, Mrugala, A, Viñuela-Rodriguez, N, Petrusek, A and Oidtmann, B (2017) The prevalence of Aphanomyces astaci in invasive signal crayfish from the UK and implications for native crayfish conservation. Parasitology 144, 411418.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. Berlin: De Gruyter Open, pp. 183211.Google Scholar
Kaldre, K, Paaver, T, Hurt, M and Grandjean, F (2017) First records of the non-indigenous signal crayfish (Pacifastacus leniusculus) and its threat to noble crayfish (Astacus astacus) populations in Estonia. Biological Invasions 9, 27712776.Google Scholar
Kokko, H, Harlioglu, MM, Aydin, H, Makkonen, J, Gökmen, G, Aksu, Ö and Jussila, J (2018) Observations of crayfish plague infections in commercially important narrow-clawed crayfish populations in Turkey. Knowledge and Management of Aquatic Ecosystems 419, 10.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, Beran, L, Ďuriš, Z, Fischer, D, Horká, I, Svobodová, J and Petrusek, A (2014) Status and recovery of indigenous crayfish populations after recent crayfish plague outbreaks in the Czech Republic. Ethology Ecology & Evolution 26, 299319.Google Scholar
Leinonen, R, Sugawara, H and Shumway, M and on behalf of the International Nucleotide Sequence Database Collaboration (2011) The Sequence Read Archive. Nucleic Acids Research 39, D19D21.Google Scholar
Li, H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. eprint arXiv:1303.3997v1 [q-GN].Google Scholar
Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G and Durbin, R (2009) The sequence alignment/map format and SAMtools. Bioinformatics (Oxford, England) 25, 20782079.Google Scholar
Lilley, JH, Cerenius, L and Söderhäll, K (1997) RAPD evidence for the origin of crayfish plague outbreaks in Britain. Aquaculture 157, 181185.Google Scholar
Luo, A, Zhang, A, Ho, SYW, Xu, W, Zhang, Y, Shi, W, Cameron, SL and Zhu, C (2011) Potential efficacy of mitochondrial genes for animal DNA barcoding: a case study using eutherian mammals. BMC Genomics 12, 112.Google Scholar
Lymbery, AJ, Morine, M, Kanani, HG, Beatty, SJ and Morgan, DL (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 3, 171177.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, 4553.Google Scholar
Makkonen, J, Jussila, J, Panteleit, J, Keller, NS, Schrimpf, A, Theissinger, K, Kortet, R, Martín-Torrijos, L, Sandoval-Sierra, JV, Diéguez-Uribeondo, J and Kokko, H (2018) MtDNA allows the sensitive detection and haplotyping of the crayfish plague disease agent Aphanomyces astaci showing clues about its origin and migration. Parasitology 145, 12101218.Google Scholar
Martinati, P (1862) Nota sulla malattia dei gamberi che ammorbò le acque del veronese nell'anno 1861. Memorie Dell'accademia D'agricoltura Commercio Ed Arti Di Verona XLI, 215226.Google Scholar
Mazzaglia, A, Studholme, DJ, Taratufolo, MC, Cai, R, Almeida, NF, Goodman, T, Guttman, DS, Vinatzer, BA and Balestra, GM (2012) Pseudomonas syringae pv. actinidiae (PSA) isolates from recent bacterial canker of kiwifruit outbreaks belong to the same genetic lineage. PLoS One 7, e36518.Google Scholar
Minardi, D, Studholme, DJ, van der Giezen, M, Pretto, T and Oidtmann, B (2018) New genotyping method for the causative agent of crayfish plague (Aphanomyces astaci) based on whole genome data. Journal of Invertebrate Pathology 156, 613.Google Scholar
Mrugala, A, Kawai, T, Kozubíková-Balcarová, E and Petrusek, A (2017) Aphanomyces astaci presence in Japan: a threat to the endemic and endangered crayfish species Cambaroides japonicus? Aquatic Conservation: Marine and Freshwater Ecosystems 27, 103114.Google Scholar
Ninni, AP (1865) Sulla mortalita dei gamberi (Astacus fluviatilis L.) nel Veneto e più particolarmente nella provincia trevigiana. Atti Instituto Veneto 10, 12031209.Google Scholar
Oidtmann, B, Schmid, I, Rogers, D and Hoffmann, RW (1999) An improved isolation method for the cultivation of the crayfish plague fungus, Aphanomyces astaci. Freshwater Crayfish 12, 303312.Google Scholar
Oidtmann, B, Geiger, S, Steinbauer, P, Culas, A and Hoffmann, RW (2006) Detection of Aphanomyces astaci in North American crayfish by polymerase chain reaction. Diseases of Aquatic Organisms 72, 5364.Google Scholar
OIE (2018) Infection with Aphanomyces astaci (Crayfish plague). In Manual of Diagnostic Tests for Aquatic Animals. World Organisation for Animal Health. http://www.oie.int/standard-setting/aquatic-manual/access-online/Google Scholar
Panteleit, J, Keller, NK, Diéguez-Uribeondo, J, Makkonen, J, Martín-Torrijos, L, Patrulea, V, Pîrvu, M, Preda, C, Schrimpf, A and Pârvulescu, L (2018) Hidden sites in the distribution of the crayfish plague pathogen Aphanomyces astaci in Eastern Europe: Relicts of genetic groups from older outbreaks? Journal of Invertebrate Pathology 157, 117124.Google Scholar
Peeler, EJ, Oidtmann, BC, Midtlyng, PJ, Miossec, L and Gozlan, RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions 13, 12911303.Google Scholar
Polglase, JL and Alderman, DJ (1984) Crayfish plague threatens UK stock. Fish Farmer 7, 1617.Google Scholar
Pretto, T, Tosi, F, Sandoval-Sierra, JV, Grandjean, F, Manfrin, A and Diéguez-Uribeondo, J (2014) Characterization of Aphanomyces astaci in white-clawed crayfish Austropotamobius pallipes from Northern Italy: considerations regarding a crayfish plague outbreak., in: IAA & CSJ Joint International Conference on Crustacea. Sapporo, Japan.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, 612620.Google Scholar
Rushton, SP, Lurz, PWW, Gurnell, J, Nettleton, P, Bruemmer, C, Shirley, MDF and Sainsbury, AW (2006) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidemiology and Infection 134, 521533.Google Scholar
Strand, DA, Holst-Jensen, A, Viljugrein, H, Edvardsen, B, Klaveness, D, Jussila, J and Vrålstad, T (2011) Detection and quantification of the crayfish plague agent in natural waters: direct monitoring approach for aquatic environments. Diseases of Aquatic Organisms 95, 917.Google Scholar
Svoboda, J, Mrugała, A, Kozubíková-Balcarová, E and Petrusek, A (2017) Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. Journal of Fish Diseases 40, 127140.Google Scholar
Thorvaldsdóttir, H, Robinson, JT and Mesirov, JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 14, 178192.Google Scholar
Unestam, T (1972) On the host range and origin of the crayfish plague fungus. Report of the Institute of Freshwater Research, Drottningholm 52, 192198.Google Scholar
Unestam, T and Weiss, DW (1970) The host-parasite relationship between freshwater crayfish and the crayfish disease fungus Aphanomyces astaci: responses to infection by a susceptible and a resistant species. Journal of general microbiology 60, 7790.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, 199208.Google Scholar
Vrålstad, T, Knutsen, AK, Tengs, T and Holst-Jensen, A (2009) A quantitative TaqMan® 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
Vrålstad, T, Strand, DA, Grandjean, F, Kvellestad, A, Hastein, T, Knutsen, AK, Taugbøl, T and Skaar, I (2014) Molecular detection and genotyping of Aphanomyces astaci directly from preserved crayfish samples uncovers the Norwegian crayfish plague disease history. Veterinary Microbiology 173, 6675.Google Scholar
Waugh, J (2007) DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29, 188197.Google Scholar
Wilson, IG (1997) Inhibition and facilitation of nucleic acid amplification. Applied and Environmental Microbiology 63, 37413751.Google Scholar
Supplementary material: File

Minardi et al. supplementary material

Minardi et al. supplementary material 1

Download Minardi et al. supplementary material(File)
File 1.7 MB