Dataset Information

The Atlantic salmon (Salmo salar) antimicrobial peptide cathelicidin-2 is a molecular host-associated cue for the salmon louse (Lepeophtheirus salmonis).

ABSTRACT: Chemical signals are a key element of host-parasite interactions. In marine ecosystems, obligate ectoparasites, such as sea lice, use chemical cues and other sensory signals to increase the probability of encountering a host and to identify appropriate hosts on which they depend to complete their life cycle. The chemical compounds that underlie host identification by the sea lice are not fully described or characterized. Here, we report a novel compound - the Atlantic salmon (Salmo salar) antimicrobial peptide cathelicidin-2 (Cath-2) - that acts as an activation cue for the marine parasitic copepod Lepeophtheirus salmonis. L. salmonis were exposed to 0, 7, 70 and 700 ppb of Cath-2 and neural activity, swimming behaviour and gene expression profiles of animals in response to the peptide were evaluated. The neurophysiological, behavioural and transcriptomic results were consistent: L. salmonis detects Cath-2 as a water-soluble peptide released from the skin of salmon, triggering chemosensory neural activity associated with altered swimming behaviour of copepodids exposed to the peptide, and chemosensory-related genes were up-regulated in copepodids exposed to the peptide. L. salmonis are activated by Cath-2, indicating a tight link between this peptide and the salmon louse chemosensory system.

SUBMITTER: Nunez-Acuna G

PROVIDER: S-EPMC6137231 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The Atlantic salmon (Salmo salar) antimicrobial peptide cathelicidin-2 is a molecular host-associated cue for the salmon louse (Lepeophtheirus salmonis).

Núñez-Acuña Gustavo G Gallardo-Escárate Cristian C Fields David M DM Shema Steven S Skiftesvik Anne Berit AB Ormazábal Ignacio I Browman Howard I HI

Scientific reports 20180913 1

Chemical signals are a key element of host-parasite interactions. In marine ecosystems, obligate ectoparasites, such as sea lice, use chemical cues and other sensory signals to increase the probability of encountering a host and to identify appropriate hosts on which they depend to complete their life cycle. The chemical compounds that underlie host identification by the sea lice are not fully described or characterized. Here, we report a novel compound - the Atlantic salmon (Salmo salar) antimi ...[more]

PMID: 30213966

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Project description:BACKGROUND: The salmon louse (SL) is an ectoparasitic caligid crustacean infecting salmonid fishes in the marine environment. SL represents one of the major challenges for farming of salmonids, and veterinary intervention is necessary to combat infection. This study addressed gene expression responses of Atlantic salmon infected with SL, which may account for its high susceptibility. RESULTS: The effects of SL infection on gene expression in Atlantic salmon were studied throughout the infection period from copepodids at 3 days post infection (dpi) to adult lice (33 dpi). Gene expression was analyzed at three developmental stages in damaged and intact skin, spleen, head kidney and liver, using real-time qPCR and a salmonid cDNA microarray (SFA2). Rapid detection of parasites was indicated by the up-regulation of immunoglobulins in the spleen and head kidney and IL-1 receptor type 1, CD4, beta-2-microglobulin, IL-12beta, CD8alpha and arginase 1 in the intact skin of infected fish. Most immune responses decreased at 22 dpi, however, a second activation was observed at 33 dpi. The observed pattern of gene expression in damaged skin suggested the development of inflammation with signs of Th2-like responses. Involvement of T cells in responses to SL was witnessed with up-regulation of CD4, CD8alpha and programmed death ligand 1. Signs of hyporesponsive immune cells were seen. Cellular stress was prevalent in damaged skin as seen by highly significant up-regulation of heat shock proteins, other chaperones and mitochondrial proteins. Induction of the major components of extracellular matrix, TGF-beta and IL-10 was observed only at the adult stage of SL. Taken together with up-regulation of matrix metalloproteinases (MMP), this classifies the wounds afflicted by SL as chronic. Overall, the gene expression changes suggest a combination of chronic stress, impaired healing and immunomodulation. Steady increase of MMP expression in all tissues except liver was a remarkable feature of SL infected fish. CONCLUSION: SL infection in Atlantic salmon is associated with a rapid induction of mixed inflammatory responses, followed by a period of hyporesponsiveness and delayed healing of injuries. Persistent infection may lead to compromised host immunity and tissue self-destruction.

Project description:Outcomes of infections with the salmon louse Lepeophtheirus salmonis vary considerably among its natural hosts (Salmo, Oncorhynchus spp.). Host-parasite interactions range from weak to strong host responses accompanied by high to low parasite abundances, respectively. Parasite behavioral studies indicate that the louse prefers the host Atlantic Salmon (Salmo salar), which is characterized by a weak immune response, and that this results in enhanced parasite reproduction and growth rates. Furthermore, parasite-derived immunosuppressive molecules (e.g., proteases) have been detected at higher amounts in response to the mucus of Atlantic Salmon relative to Coho Salmon (Oncorhynchus kisutch). However, the host-specific responses of the salmon louse have not been well characterized in either of the genetically distinct sub-species that occur in the Atlantic and Pacific Oceans.We assessed and compared the transcriptomic feeding response of the Pacific salmon louse (L. salmonis oncorhynchi,) while parasitizing the highly susceptible Atlantic Salmon and Sockeye Salmon (Oncorhynchus nerka) or the more resistant Coho Salmon (Oncorhynchus kisutch) using a 38 K oligonucleotide microarray. The response of the louse was enhanced both in the number of overexpressed genes and in the magnitude of expression while feeding on the non-native Atlantic Salmon, compared to either Coho or Sockeye Salmon. For example, putative virulence factors (e.g., cathepsin L, trypsin, carboxypeptidase B), metabolic enzymes (e.g., cytochrome B, cytochrome C), protein synthesis enzymes (e.g., ribosomal protein P2, 60S ribosomal protein L7), and reproduction-related genes (e.g., estrogen sulfotransferase) were overexpressed in Atlantic-fed lice, indicating heightened parasite fitness with this host species. In contrast, responses in Coho- or Sockeye-fed lice were more similar to those of parasites deprived of a host. To test for host acclimation by the parasite, we performed a reciprocal host transfer experiment and determined that the exaggerated response to Atlantic Salmon was independent of the initial host species, confirming our conclusion that the Pacific salmon louse exhibits an enhanced response to Atlantic Salmon.This study characterized global transcriptomic responses of Pacific salmon lice during infection of susceptible and resistant hosts. Similar parasite responses during infection of Coho or Sockeye Salmon, despite differences in natural immunity to infection between these host species, indicate that host susceptibility status alone does not drive the parasite response. We identified an enhanced louse response after feeding on Atlantic Salmon, characterized by up-regulation of virulence factors, energy metabolism and reproductive-associated transcripts. In contrast, the responses of lice infecting Coho or Sockeye Salmon were weaker, with reduced expression of virulence factors. These observations indicate that the response of the louse is independent of host susceptibility and suggest that co-evolutionary host-parasite relationships may influence contemporary host-parasite interactions. This research improves our understanding of the susceptibility of Atlantic Salmon and may assist in the development of novel control measures against the salmon louse.

Project description:BACKGROUND: Salmon species vary in susceptibility to infections with the salmon louse (Lepeophtheirus salmonis). Comparing mechanisms underlying responses in susceptible and resistant species is important for estimating impacts of infections on wild salmon, selective breeding of farmed salmon, and expanding our knowledge of fish immune responses to ectoparasites. Herein we report three L. salmonis experimental infection trials of co-habited Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha, profiling hematocrit, blood cortisol concentrations, and transcriptomic responses of the anterior kidney and skin to the infection. RESULTS: In all trials, infection densities (lice per host weight (g)) were consistently highest on chum salmon, followed by Atlantic salmon, and lowest in pink salmon. At 43 days post-exposure, all lice had developed to motile stages, and infection density was uniformly low among species. Hematocrit was reduced in infected Atlantic and chum salmon, and cortisol was elevated in infected chum salmon. Systemic transcriptomic responses were profiled in all species and large differences in response functions were identified between Atlantic and Pacific (chum and pink) salmon. Pink and chum salmon up-regulated acute phase response genes, including complement and coagulation components, and down-regulated antiviral immune genes. The pink salmon response involved the largest and most diverse iron sequestration and homeostasis mechanisms. Pattern recognition receptors were up-regulated in all species but the active components were often species-specific. C-type lectin domain family 4 member M and acidic mammalian chitinase were specifically up-regulated in the resistant pink salmon. CONCLUSIONS: Experimental exposures consistently indicated increased susceptibility in chum and Atlantic salmon, and resistance in pink salmon, with differences in infection density occurring within the first three days of infection. Transcriptomic analysis suggested candidate resistance functions including local inflammation with cytokines, specific innate pattern recognition receptors, and iron homeostasis. Suppressed antiviral immunity in both susceptible and resistant species indicates the importance of future work investigating co-infections of viral pathogens and lice.

Dataset Information

The Atlantic salmon (Salmo salar) antimicrobial peptide cathelicidin-2 is a molecular host-associated cue for the salmon louse (Lepeophtheirus salmonis).

Publications

The Atlantic salmon (Salmo salar) antimicrobial peptide cathelicidin-2 is a molecular host-associated cue for the salmon louse (Lepeophtheirus salmonis).

Similar Datasets

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