Tracing the origin of the crayfish plague pathogen, Aphanomyces astaci, to the Southeastern United States

AbstractThe oomycete Aphanomyces astaci is an emerging infectious pathogen affecting freshwater crayfish worldwide and is responsible for one of the most severe wildlife pandemics ever reported. The pathogen has caused mass mortalities of freshwater crayfish species in Europe and Asia, and threatens other susceptible species in Madagascar, Oceania and South America. The pathogen naturally coexists with some North American crayfish species that are its chronic carriers. Presumptions that A. astaci originated in North America are based on disease outbreaks that followed translocations of North American crayfish and on the identification of the pathogen mainly in Europe. We studied A. astaci in the southeastern US, a center of freshwater crayfish diversity. In order to decipher the origin of the pathogen, we investigated (1) the distribution and haplotype diversity of A. astaci, and (2) whether there are crayfish species-specificities and/or geographical restrictions for A. astaci haplotypes. A total of 132 individuals, corresponding to 19 crayfish species and one shrimp species from 23 locations, tested positive for A. astaci. Mitochondrial rnnS and rnnL sequences indicated that A. astaci from the southeastern US exhibited the highest genetic diversity so far described for the pathogen (eight haplotypes, six of which we newly describe). Our findings that A. astaci is widely distributed and genetically diverse in the region supports the hypothesis that the pathogen originated in the southeastern US. In contrast to previous assumptions, however, the pathogen exhibited no clear species-specificity or geographical patterns.

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Comparative transcriptome analysis of noble crayfish and marbled crayfish immune response to Aphanomyces astaci challenges

10.1101/2021.05.25.445163 ◽

2021 ◽

Author(s):

Ljudevit Luka Boštjančić ◽

Caterina Francesconi ◽

Christelle Rutz ◽

Lucien Hoffbeck ◽

Laetitia Poidevin ◽

...

Keyword(s):

Invasive Disease ◽

Freshwater Crayfish ◽

Post Challenge ◽

Aphanomyces Astaci ◽

Resistant Species ◽

High Virulence ◽

Noble Crayfish ◽

Immune Related Genes ◽

Marbled Crayfish ◽

Crayfish Species

Introduction of invasive North American crayfish species and their pathogen Aphanomyces astaci has significantly contributed to the decline of European freshwater crayfish populations. In this study, noble crayfish, a susceptible native European species, and marbled crayfish, an invasive disease-resistant species, were challenged with haplogroup A (low virulence) and haplogroup B (high virulence) strain of A. astaci. Hepatopancreatic tissue was isolated 3 and 21 days post-challenge. Our results revealed strong up-regulation in expression levels of the prophenoloxidase cascade immune-related genes in the haplogroup B challenged noble crayfish 3 days post-challenge. In the marbled crayfish, we observed an up-regulation of immune system relevant genes (DSCAM, AP, ALFs, CTLs and hemocyanin) 3 days post-challenge. This response highlights the marbled crayfish capability of building the immune tolerance. Furthermore, we successfully characterised several novel immune related gene groups in both crayfish species, contributing to our current understanding of crayfish immune related genes landscape.

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

Parasitology ◽

10.1017/s0031182019000283 ◽

2019 ◽

Vol 146 (8) ◽

pp. 1022-1029 ◽

Cited By ~ 1

Author(s):

Diana Minardi ◽

David J. Studholme ◽

Birgit Oidtmann ◽

Tobia Pretto ◽

Mark van der Giezen

Keyword(s):

Mitochondrial Dna ◽

North American ◽

Nuclear Dna ◽

Random Amplified Polymorphic Dna ◽

Pcr Analysis ◽

Freshwater Crayfish ◽

Aphanomyces Astaci ◽

High Infection ◽

Pure Cultures ◽

Dna Pcr

AbstractAphanomyces astacicauses crayfish plague, which is a devastating disease of European freshwater crayfish. The likely first introduction ofA. astaciinto Europe was in the mid-19th century in Italy, presumably with the introduction of North American crayfish. These crayfish can carryA. astaciin their cuticle as a benign infection.Aphanomyces astacirapidly spread across Europe causing the decline of the highly susceptible indigenous crayfish species. Random amplified polymorphic DNA-PCR analysis ofA. astacipure cultures characterized five genotype groups (A, B, C, D and E). CurrentA. astacigenotyping 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 developA. astacigenotyping molecular markers that target the mitochondrial DNA, increasing the sensitivity of the genotyping tools. The assays were validated on DNA extracts ofA. astacipure cultures, crayfish tissue extractions from crayfish plague outbreaks and tissue extractions from North American carriers. We demonstrate the presence ofA. astacigenotype groups A and B in UK waters.

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Resistance to the crayfish plague, Aphanomyces astaci (Oomycota) in the endangered freshwater crayfish species, Austropotamobius pallipes

PLoS ONE ◽

10.1371/journal.pone.0181226 ◽

2017 ◽

Vol 12 (7) ◽

pp. e0181226 ◽

Cited By ~ 5

Author(s):

Laura Martín-Torrijos ◽

Miquel Campos Llach ◽

Quim Pou-Rovira ◽

Javier Diéguez-Uribeondo

Keyword(s):

Freshwater Crayfish ◽

Austropotamobius Pallipes ◽

Aphanomyces Astaci ◽

Crayfish Species

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Controlled Infection Experiment With Aphanomyces astaci Provides Additional Evidence for Latent Infections and Resistance in Freshwater Crayfish

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.647037 ◽

2021 ◽

Vol 9 ◽

Author(s):

Caterina Francesconi ◽

Jenny Makkonen ◽

Anne Schrimpf ◽

Japo Jussila ◽

Harri Kokko ◽

...

Keyword(s):

Virulent Strain ◽

Freshwater Crayfish ◽

Infection Experiment ◽

Aphanomyces Astaci ◽

Latently Infected ◽

Noble Crayfish ◽

Disease Agent ◽

Marbled Crayfish ◽

Mass Mortalities ◽

Highly Virulent

For 150 years the crayfish plague disease agent Aphanomyces astaci has been the cause of mass mortalities among native European crayfish populations. However, recently several studies have highlighted the great variability of A. astaci virulence and crayfish resistance toward the disease. The main aim of this study was to compare the response of two crayfish species, the European native noble crayfish (Astacus astacus) and the invasive alien marbled crayfish (Procambarus virginalis), to an A. astaci challenge with a highly virulent strain from haplogroup B and a lowly virulent strain from haplogroup A. In a controlled infection experiment we showed a high resistance of marbled crayfish against an A. astaci infection, with zoospores from the highly virulent haplogroup B strain being able to infect the crayfish, but unable to cause signs of disease. Furthermore, we demonstrated a reduced virulence in the A. astaci strain belonging to haplogroup A, as shown by the light symptoms and the lack of mortality in the generally susceptible noble crayfish. Interestingly, in both marbled crayfish and noble crayfish challenged with this strain, we observed a significant decrease of the detected amount of pathogen’s DNA during the experiment, suggesting that this A. astaci haplogroup A strain has a decreased ability of penetrating into the cuticle of the crayfish. Our results provide additional evidence of how drastically strains belonging to A. astaci haplogroup B and haplogroup A differ in their virulence. This study confirmed the adaptation of one specific A. astaci haplogroup A strain to their novel European hosts, supposedly due to reduced virulence. This feature might be the consequence of A. astaci’s reduced ability to penetrate into the crayfish. Finally, we experimentally showed that marbled crayfish are remarkably resistant against the crayfish plague disease and could potentially be latently infected, acting as carriers of highly virulent A. astaci strains.

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May atyid shrimps act as potential vectors of crayfish plague?

NeoBiota ◽

10.3897/neobiota.51.37718 ◽

2019 ◽

Vol 51 ◽

pp. 65-80 ◽

Cited By ~ 1

Author(s):

Agata Mrugała ◽

Miloš Buřič ◽

Adam Petrusek ◽

Antonín Kouba

Keyword(s):

Procambarus Clarkii ◽

Freshwater Crayfish ◽

Transmission Experiment ◽

Shrimp Species ◽

Aphanomyces Astaci ◽

Freshwater Shrimps ◽

Successful Infection ◽

In The Wild ◽

Species Specific ◽

Crayfish Species

The causative agent of crayfish plague, Aphanomyces astaci Schikora, was long considered to be a specialist pathogen whose host range is limited to freshwater crayfish. Recent studies, however, provided evidence that this parasite does not only grow within the tissues of freshwater-inhabiting crabs but can also be successfully transmitted by them to European crayfish species. The potential to act as alternative A. astaci hosts was also indicated for freshwater shrimps. We experimentally tested resistance of two freshwater atyid shrimps: Atyopsis moluccensis (De Haan, 1849) and Atya gabonensis Giebel, 1875. They were infected with the A. astaci strain associated with the globally widespread North American red swamp crayfish, Procambarus clarkii (Girard, 1852), the typical host of the A. astaci genotype group D. As popular ornamental species, both shrimps may get in contact with infected P. clarkii not only in the wild but also in the aquarium trade. We assessed the potential of shrimps to transmit A. astaci to susceptible crayfish by cohabiting A. gabonensis previously exposed to A. astaci zoospores with the European noble crayfish, Astacus astacus (Linnaeus, 1758). In both experiments, the presence of A. astaci infection was analysed with species-specific quantitative PCR. We detected A. astaci in bodies and exuviae of both shrimp species exposed to A. astaci zoospores, however, the intensity of infection differed between the species and analysed samples; it was higher in A. moluccensis and the exuviae of both species. A. astaci was also detected in one A. astacus individual in the transmission experiment. This finding reveals that freshwater shrimps may be able to transmit A. astaci to crayfish hosts; this is particularly important as even a single successful infection contributes to the spread of the disease. Moreover, our results indicate that the tested shrimp species may be capable of resisting A. astaci infection and reducing its intensity through moulting. Although their potential to act as prominent A. astaci vectors requires further research, it should not be ignored as these freshwater animals may then facilitate A. astaci spread to susceptible crayfish species in aquarium and aquaculture facilities as well as in the wild.

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Money Kills Native Ecosystems: European Crayfish as an Example

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.648495 ◽

2021 ◽

Vol 9 ◽

Author(s):

Japo Jussila ◽

Lennart Edsman ◽

Ivana Maguire ◽

Javier Diéguez-Uribeondo ◽

Kathrin Theissinger

Keyword(s):

Alien Species ◽

Aquatic Ecosystems ◽

Significant Proportion ◽

Suitable Habitat ◽

Freshwater Crayfish ◽

Aphanomyces Astaci ◽

Commercial Activities ◽

Disease Agent ◽

Native Crayfish ◽

Crayfish Species

Native European crayfish conservation was triggered by invasion of crayfish plague disease agent, Aphanomyces astaci, starting 1860s in Northern Italy. Resulting crayfish plague epidemics quickly spread over Continental Europe, then to Finland, Sweden and finally, after running amok around Europe, A. astaci was discovered also in Iberian Peninsula, Norway, Ireland, and United Kingdom in 1970s and 1980s. By that time significant proportion of native crayfish stocks had been lost, and while crayfish plague epidemics were still recorded, also industrialization and waterways construction were causing damage to remaining native crayfish stocks. While alien crayfish introductions, at least Faxonius limosus, already gave rise to first wave of crayfish plague epidemics in late 19th century, later in 1960s it was decided that introductions of alien Pacifastacus leniusculus should be initiated to replace native European crayfish populations. Decisions were based on presumed advantages for fishery, suitable habitat requirements and supposed immunity against A. astaci. Furthermore, conservation of native European crayfish species was sidelined and focus shifted toward alien crayfish stocking routine and consumption. Alien crayfish species introductions resulted in repeated waves of crayfish plague epidemics among remaining native crayfish stocks. It was soon discovered that alien crayfish of North American origin were, as suspected, permanent reservoirs for A. astaci, that some of those alien species were losing their resistance against selected strains of A. astaci and struggled in European aquatic ecosystems. In this article, we introduce numerous motives behind grand mistake of introducing alien crayfish species to Europe and then promoting their stocks instead of focusing on conservation of native crayfish species. We outline how false economical, biological and ecologic assumptions were used to justify a hasty introduction of alien crayfish, which has further devastated native crayfish and also permanently changed European aquatic ecosystems, both with disastrous consequences. Lesson to be learnt is that science-based warnings about alien species damage to native ecosystems and native crayfish must be taken with utmost caution. Protection of native European crayfish should be core issue, not commercial activities. Finally, we summarize main threats and actions needed to protect remaining native freshwater crayfish fauna in Europe.

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Evidence for multiple paternity in two species of Orconectes crayfish

Canadian Journal of Zoology ◽

10.1139/cjz-2014-0132 ◽

2014 ◽

Vol 92 (11) ◽

pp. 985-988 ◽

Cited By ~ 6

Author(s):

A.F. Kahrl ◽

R.H. Laushman ◽

A.J. Roles

Keyword(s):

Genetic Variation ◽

Life History ◽

Multiple Mating ◽

Natural Populations ◽

Multiple Paternity ◽

The Body ◽

Freshwater Crayfish ◽

Decapod Crustaceans ◽

Freshwater Habitats ◽

Crayfish Species

Multiple mating is expected to be common in organisms that produce large clutches as a mechanism by which sexual reproduction can enrich genetic variation. For freshwater crayfish, observation of multiple mating suggests the potential for high rates of multiple paternity, but genetic confirmation is largely lacking from natural populations. We studied paternity within wild-caught broods of two crayfish species in the genus Orconectes (Sanborn’s crayfish (Orconectes sanbornii (Faxon, 1884)) and the Allegheny crayfish (Orconectes obscurus (Hagen, 1870))). Although females have been observed mating with multiple males, this is the first genetic confirmation of multiple paternity in broods of these two species. Berried females were collected in the field and maintained in aquaria until their eggs hatched. We amplified and genotyped extracted DNA from maternal and hatchling tissue for several microsatellite loci. For both species, paternity reconstruction (GERUD 2.0) yielded 2–3 sires per brood and no single paternity clutches. We discuss these results from natural populations in light of the body of work on reproductive ecology of decapod crustaceans and in the context of changes in life history following the transition from marine to freshwater habitats.

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