Identification of transcripts relating to host-parasite interactions and feeding-associated activities through de novo transcriptome sequencing of branchiuran fish lice, Argulus foliaceus (Linnaeus, 1758) and Argulus coregoni Thorell, 1865

BackgroundThe genus Argulus, whose members are widely known as “fish lice”, comprises a group of obligate ectoparasites that cause argulosis. This parasitic disease affects both wild and cultured fish populations and can lead to significant mortalities. Our previous work confirmed the presence of immunomodulatory or other active products in the secretions of Argulus foliaceus (Linnaeus, 1758) using proteomic analysis conducted on secretory / excretory products (SEPs). Some of the compounds identified have also been described for other host-associated Crustacea, particularly the parasitic copepod Lepeophtheirus salmonis (Krøyer, 1837). The identification and characterisation of such components can contribute to the understanding of the host-parasite relationship for argulids and may also assist in the development of novel control methods, however, due to limitations in existing genomic resources, only 27 proteins could be confirmed in SEPs. In this study, high-throughput sequencing, supported by the use of a range of bioinformatics tools and methodologies were employed on host-associated stages of A. foliaceus and A. coregoni Thorell, 1865 to explore elements of the transcriptome associated with host-parasite interactions and feeding-associated activities.ResultsThe transcriptome data produced in the current study comprises the largest current genomic data set for the genus Argulus, with 84,256,934 reads, assembled into 66,940 contigs for Argulus foliaceus, and 10,840,092 reads, assembled to give 40,954 contigs, representing the first transcript sequences for Argulus coregoni. A pre-existing transcriptome dataset for A. siamensis was also analysed. An overview of the functional roles of the transcripts and their respective proteins for the three Argulus species was performed using GO analysis. A phylogenetic tree was also constructed, using the top 100 shared genes for the four transcriptome datasets available for Argulus. From this analysis, A. coregoni was revealed to be more closely related to A. foliaceus than to A. siamensis. The application of OrthoVenn software to the Argulus spp. transcriptome datasets identified 6,674 shared gene clusters. The transcriptomic analysis in this study, supported by earlier proteome work, has contributed to identifying, for the first time, a range of proteins / genes in Argulus, and more widely for the Branchiura, that have been previously characterised as being important immune mediators for other aquatic and terrestrial blood-feeding arthropods. Data are available via EBI with the project number PRJEB34947.Conclusions In addition to confirming the presence of a range of key immune mediators in Argulus spp. for the first time, this study has provided important genomic tools for researchers seeking to better understand the biology and host interactions of Argulus spp. The created resources unlock the possibility of characterising protein targets relating to host-parasite interactions and feeding-associated activities and can thereby assist the future development of vaccines, veterinary drugs, functional feeds and other tools that might contribute to improved integrated pest management of these globally important parasites.

Host specificity of Argulus coregoni (Crustacea: Branchiura) increases at maturation

SUMMARYWe tested the hypothesis that host specificity in ectoparasites does not depend exclusively on the features of the host but also on surrounding habitats, using 2 fish ectoparasites, Argulus coregoni and A. foliaceus (Crustacea: Branchiura), occurring sympatrically in Finnish lakes. Although these parasites are considered to be of low specificity, we found that the larger of the 2 species, A. coregoni developed a pronounced preference for salmonid hosts at the beginning of maturation (defined by the presence of copulating specimens). Argulus foliaceus infects a much wider range of fish hosts. We showed that specialization of A. coregoni on salmonids does not necessarily result from incompatibility with other fishes, but could instead reflect higher sensitivity of oxygen depletion compared with A. foliaceus. Adult A. coregoni may meet these demands by attaching to salmonids, the typical inhabitants of well-aerated waters. Young parasites of both species showed little host specificity and attached mainly to fishes with higher body reflectivity. In host choice experiments, A. coregoni of 4–5 mm length preferred salmonids (rainbow trout) to cyprinids (roach) irrespective of the type of fish host, on which it had been previously grown in the laboratory. We suggest that such an innate ontogenetic shift in host preference maintains the major part of the parasite population on its principal host, ensuring successful reproduction within suitable habitats.

Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies

The link between climate changes and disease risks from various pathogens has been increasingly recognized. The effect of climatic factors on host–parasite population dynamics is particularly evident in northern latitudes where the occurrence and transmission of parasites are strongly regulated by seasonality-driven changes in environmental temperatures. Shortened winter periods would increase growth potential of many parasite populations. The ways in which climate warming could affect life history dynamics of the directly transmitted crustacean ectoparasite Argulus coregoni and complex life cycle trematode Diplostomum spathaceum, which frequently cause problems in northern fish farming, are discussed. Increased problems for fish farming are predicted in terms of increased infection pressure from these parasites in future. This would increase problems associated with infections and increase the use of expensive management protocols with high environmental impact.

Delayed transmission of a parasite is compensated by accelerated growth

Compensatory or ‘catch-up’ growth following prolonged periods of food shortages is known to exist in many free-living animals. It is generally assumed that growth rates under normal circumstances are below maximum because elevated rates of growth are costly. The present paper gives experimental evidence that such compensatory growth mechanisms also exist in parasitic species. We explored the effect of periodic host unavailability on survival, infectivity and growth of the fish ectoparasiteArgulus coregoni. Survival and infectivity ofA. coregonimetanauplii deprived of a host for selected time periods were age dependent, which indicates that all metanauplii carry similar energy resources for host seeking. Following the periods off-host, metanauplii were allowed to settle on rainbow trout and were length measured until they reached gravidity. During early development on fish, body length of attachedA. coregoniwas negatively correlated with off-host period indicating a mechanism that creates size variance in an attached parasite cohort originally containing equal amounts of resources. However, over time the size differences between parasites became less pronounced and eventually parasites that were kept off-host for longest periods of time reached the length of those individuals that had been allowed to infect a host sooner.A. coregonithus appears to compensate for delayed growth resulting from an extended host searching period by elevated growth rates, although we show that such accelerated growth incurred a cost, through decreased life-expectancy.