Host-pathogen coevolution drives innate immune response to Aphanomyces astaci infection in freshwater crayfish: transcriptomic evidence

Abstract

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.

Genotype–environment associations reveal genes potentially linked to avian malaria infection in populations of an endemic island bird

“…Recent transcriptomic studies have uncovered genes that are upregulated or downregulated during infectious disease (e.g. Boštjančić et al., 2022; Chu et al., 2016; Huang et al., 2013; McNew et al., 2022; Rosenblum et al., 2012). Those examining gene expression changes in the host response to malaria have identified genes that were related to a number of functions beyond those strictly within the immune system, including the stress response, cell death regulation, metabolism, cell signalling, transcriptional regulation and telomerase activity (Quin et al., 2017; Videvall et al., 2015, 2020).…”

Dataset of the de novo assembly and annotation of the marbled crayfish and the noble crayfish hepatopancreas transcriptomes

“…During the experiment, individuals of both species were sampled at: 3 dpi, 21 dpi for the analysis of the gene expression patterns in the infected individuals. Results of this study are presented in [ 2 ].…”

“…Freshwater crayfish are keystone species of freshwater habitats [1][2][3]. One of the major contributors to the loss of the European freshwater crayfish biodiversity is the introduction of highly competitive North American invasive crayfish species, carriers of the devastating disease crayfish plague [4].…”

The Crayfish Plague Pathogen Aphanomyces astaci in Ireland

“…astaci infection and these North American crayfish species repress Ap. astaci hyphal growth without killing the parasite, instead acting as mobile vectors of the pathogen [ 7 , 9 , 10 ]. Since its introduction to Europe, the pathogen has spread across the continent, decimating native European crayfish populations, leading to mortality rates of up to 100% at infected sites [ 11 ].…”