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Introduced into Europe from North America 150 years ago alongside its native crayfish hosts, the invasive pathogen Aphanomyces astaci is considered one of the main causes of European crayfish population decline. For the past two centuries, this oomycete pathogen has been extensively studied, with the more recent efforts focused on containing and monitoring its spread across the continent. However, after the recent introduction of new strains, the newly-discovered diversity of A. astaci in North America and several years of coevolution with its European host, a new assessment of the traits linked to the pathogen's virulence is much needed. To fill this gap, we investigated the presence of phenotypic patterns (i.e., in vitro growth and sporulation rates) possibly associated with the pathogen's virulence (i.e., induced mortality in crayfish) in a collection of 14 A. astaci strains isolated both in North America and in Europe. The results highlighted a high variability in virulence, growth rate and motile spore production among the different strains, while the total-sporulation rate was more similar across strains. Surprisingly, growth and sporulation rates were not significantly correlated with virulence. Furthermore, none of the analysed parameters, including virulence, was significantly different among the major A. astaci haplogroups. These results indicate that each strain is defined by a characteristic combination of pathogenic features, specifically assembled for the environment and host faced by each strain. Thus, canonical mitochondrial markers, often used to infer the pathogen's virulence, are not accurate tools to deduce the phenotype of A. astaci strains. As the diversity of A. astaci strains in Europe is bound to increase due to translocations of new carrier crayfish species from North America, there is an urgent need to deepen our understanding of A. astaci's virulence variability and its ability to adapt to new hosts and environments.
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BACKGROUND: For over a century, scientists have studied host-pathogen interactions between the crayfish plague disease agent Aphanomyces astaci and freshwater crayfish. It has been hypothesised that North American crayfish hosts are disease-resistant due to the long-lasting coevolution with the pathogen. Similarly, the increasing number of latent infections reported in the historically sensitive European crayfish hosts seems to indicate that similar coevolutionary processes are occurring between European crayfish and A. astaci. Our current understanding of these host-pathogen interactions is largely focused on the innate immunity processes in the crayfish haemolymph and cuticle, but the molecular basis of the observed disease-resistance and susceptibility remain unclear. To understand how coevolution is shaping the host's molecular response to the pathogen, susceptible native European noble crayfish and invasive disease-resistant marbled crayfish were challenged with two A. astaci strains of different origin: a haplogroup A strain (introduced to Europe at least 50 years ago, low virulence) and a haplogroup B strain (signal crayfish in lake Tahoe, USA, high virulence). Here, we compare the gene expression profiles of the hepatopancreas, an integrated organ of crayfish immunity and metabolism. RESULTS: We characterised several novel innate immune-related gene groups in both crayfish species. Across all challenge groups, we detected 412 differentially expressed genes (DEGs) in the noble crayfish, and 257 DEGs in the marbled crayfish. In the noble crayfish, a clear immune response was detected to the haplogroup B strain, but not to the haplogroup A strain. In contrast, in the marbled crayfish we detected an immune response to the haplogroup A strain, but not to the haplogroup B strain. CONCLUSIONS: We highlight the hepatopancreas as an important hub for the synthesis of immune molecules in the response to A. astaci. A clear distinction between the innate immune response in the marbled crayfish and the noble crayfish is the capability of the marbled crayfish to mobilise a higher variety of innate immune response effectors. With this study we outline that the type and strength of the host immune response to the pathogen is strongly influenced by the coevolutionary history of the crayfish with specific A. astaci strains.
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Aphanomyces , Animales , Aphanomyces/genética , Astacoidea/genética , Resistencia a la Enfermedad , Lagos , TranscriptomaRESUMEN
BACKGROUND: Biodiversity in freshwater ecosystems is declining due to an increased anthropogenic footprint. Freshwater crayfish are keystone species in freshwater ecosystems and play a crucial role in shaping the structure and function of their habitats. The Idle Crayfish Austropotamobius bihariensis is a native European species with a narrow distribution range, endemic to the Apuseni Mountains (Romania). Although its area is small, the populations are anthropogenically fragmented. In this context, the assessment of its conservation status is timely. RESULTS: Using a reduced representation sequencing approach, we identified 4875 genomic SNPs from individuals belonging to 13 populations across the species distribution range. Subsequent population genomic analyses highlighted low heterozygosity levels, low number of private alleles and small effective population size. Our structuring analyses revealed that the genomic similarity of the populations is conserved within the river basins. CONCLUSION: Genomic SNPs represented excellent tools to gain insights into intraspecific genomic diversity and population structure of the Idle Crayfish. Our study highlighted that the analysed populations are at risk due to their limited genetic diversity, which makes them extremely vulnerable to environmental alterations. Thus, our results emphasize the need for conservation measures and can be used as a baseline to establish species management programs.
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Astacoidea , Conservación de los Recursos Naturales , Polimorfismo de Nucleótido Simple , Animales , Astacoidea/genética , Variación Genética/genética , Genómica/métodosRESUMEN
Transcription factors (TFs) have an important role in the regulation of the gene expression network. The role of TFs in the immune response of freshwater crayfish is poorly understood, but leveraging the regulatory mechanisms of immune response could augment the resistance against the invasive oomycete pathogen, Aphanomyces astaci. Previous studies indicated that the TFs CCAAT/enhancer-binding protein (C/EBP) and putative Krüppel homolog-1 protein (Kr-h1) might play a role in immune and stress response of the noble crayfish (Astacus astacus). Here, we aimed to further characterise these two gene products to gain a better understanding of their evolutionary origin, domain organisation and expression patterns across different crayfish tissues. Furthermore, we conducted an immune stimulation experiment to observe the potential changes in the gene expression of C/EBP and Kr-h1 under immune challenge in different crayfish tissues. Our results showed that both C/EBP and Kr-h1 are closely related to other C/EBPs and Kr-h1s in Malacostraca. Gene expression analysis revealed that both TFs are present in all analysed tissues, with higher expression of C/EBP in the gills and Kr-h1 in the abdominal muscle. Immune stimulation with laminarin (mimicking ß-1-3-glucan in the oomycete cell wall) showed an activation of the crayfish immune system, with an overall increase in the total haemocyte count (THC) compared to untreated control and crayfish buffered saline (CBS) treatment. On the gene expression level, an up-regulation of the C/EBP gene was detected in the laminarin treated group in hepatopancreas and heart, while no changes were observed for the Kr-h1 gene. Our results indicate an early change in C/EBP expression in multiple tissues during immune stimulation and suggest its involvement in the immune response of the noble crayfish.
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Repetitive elements are a major component of DNA sequences due to their ability to propagate through the genome. Characterization of Metazoan repetitive profiles is improving; however, current pipelines fail to identify a significant proportion of divergent repeats in non-model organisms. The Decapoda order, for which repeat content analyses are largely lacking, is characterized by extremely variable genome sizes that suggest an important presence of repetitive elements. Here, we developed a new standardized pipeline to annotate repetitive elements in non-model organisms, which we applied to twenty Decapoda and six other Crustacea genomes. Using this new tool, we identified 10% more repetitive elements than standard pipelines. Repetitive elements were more abundant in Decapoda species than in other Crustacea, with a very large number of highly repeated satellite DNA families. Moreover, we demonstrated a high correlation between assembly size and transposable elements and different repeat dynamics between Dendrobranchiata and Reptantia. The patterns of repetitive elements largely reflect the phylogenetic relationships of Decapoda and the distinct evolutionary trajectories within Crustacea. In summary, our results highlight the impact of repetitive elements on genome evolution in Decapoda and the value of our novel annotation pipeline, which will provide a baseline for future comparative analyses.
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Elementos Transponibles de ADN , Decápodos , Animales , Filogenia , Elementos Transponibles de ADN/genética , ADN SatéliteRESUMEN
Soil invertebrates are among the least understood metazoans on Earth. Thus far, the lack of taxonomically broad and dense genomic resources has made it hard to thoroughly investigate their evolution and ecology. With MetaInvert we provide draft genome assemblies for 232 soil invertebrate species, representing 14 common groups and 94 families. We show that this data substantially extends the taxonomic scope of DNA- or RNA-based taxonomic identification. Moreover, we confirm that theories of genome evolution cannot be generalised across evolutionarily distinct invertebrate groups. The soil invertebrate genomes presented here will support the management of soil biodiversity through molecular monitoring of community composition and function, and the discovery of evolutionary adaptations to the challenges of soil conditions.
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Invertebrados , Suelo , Humanos , Animales , Invertebrados/genética , Biodiversidad , Ecología , GenómicaRESUMEN
OBJECTIVES: Crayfish plague disease, caused by the oomycete pathogen Aphanomyces astaci represents one of the greatest risks for the biodiversity of the freshwater crayfish. This data article covers the de novo transcriptome assembly and annotation data of the noble crayfish and the marbled crayfish challenged with Ap. astaci. Following the controlled infection experiment (Francesconi et al. in Front Ecol Evol, 2021, https://doi.org/10.3389/fevo.2021.647037 ), we conducted a differential gene expression analysis described in (Bostjancic et al. in BMC Genom, 2022, https://doi.org/10.1186/s12864-022-08571-z ) DATA DESCRIPTION: In total, 25 noble crayfish and 30 marbled crayfish were selected. Hepatopancreas tissue was isolated, followed by RNA sequencing using the Illumina NovaSeq 6000 platform. Raw data was checked for quality with FastQC, adapter and quality trimming were conducted using Trimmomatic followed by de novo assembly with Trinity. Assembly quality was assessed with BUSCO, at 93.30% and 93.98% completeness for the noble crayfish and the marbled crayfish, respectively. Transcripts were annotated using the Dammit! pipeline and assigned to KEGG pathways. Respective transcriptome and raw datasets may be reused as the reference transcriptome assemblies for future expression studies.