@article{doi:10.1139/facets-2017-0020, author = {Sutherland, Ben J.G. and Covello, Jennifer M. and Friend, Sarah E. and Poley, Jordan D. and Koczka, Kim W. and Purcell, Sara L. and MacLeod, Tara L. and Donovan, Bridget R. and Pino, Jorge and González-Vecino, Jose Luis and Gonzalez, Javier and Troncoso, Jose and Koop, Ben F. and Wadsworth, Simon L. and Fast, Mark D.}, title = {Host–parasite transcriptomics during immunostimulant-enhanced rejection of salmon lice (Lepeophtheirus salmonis) by Atlantic salmon (Salmo salar)}, journal = {FACETS}, volume = {2}, number = {}, pages = {477-495}, year = {2017}, doi = {10.1139/facets-2017-0020}, URL = { https://doi.org/10.1139/facets-2017-0020 }, eprint = { https://doi.org/10.1139/facets-2017-0020 } , abstract = { Salmon lice (Lepeophtheirus salmonis) are important ectoparasites of wild and farmed salmonids and cause major losses to the salmon farming industry throughout the Northern Hemisphere. With the emergence of resistance to several commonly used parasiticides, novel control strategies and integration of multiple treatment options are needed, including host immunostimulation. Here, we investigate the effects of a functional feed containing a peptidoglycan and nucleotide formulation on L. salmonis infection of Atlantic salmon (Salmo salar) by characterizing lice infection levels, the expression of several host immune genes, and the parasite transcriptomic response to the immunostimulated host. Although initial infection intensities were low, the low dose (LD) immunostimulant diet reduced the total lice burden by 50\% relative to controls. Immunostimulant fed hosts up-regulated interleukin-1β in the skin and spleen. This gene has been implicated in successful responses of several salmonid species to salmon lice but is typically not observed in Atlantic salmon, suggesting a favorable influence on the immune response. Lice infecting LD immunostimulated salmon overexpressed genes putatively involved in parasite immunity, including carboxylesterases, and underexpressed genes putatively involved in feeding (e.g., proteases). These lice response genes further improve the characterization of the transcriptome of the non-model parasite by identifying genes potentially involved in evading host immunity. } } @article {, author = {Aaen SM}, author = {Helgesen KO}, author = {Bakke MJ}, author = {Kaur K}, author = {Horsberg TE}, title = {Drug resistance in sea lice: a threat to salmonid aquaculture}, journal = {Trends in Parasitology}, volume = {31}, pages = {72}, year = {2015} } @article {, author = {Albert Š}, author = {Gätschenberger H}, author = {Azzami K}, author = {Gimple O}, author = {Grimmer G}, author = {Sumner S}, title = {Evidence of a novel immune responsive protein in the Hymenoptera}, journal = {Insect Biochemistry and Molecular Biology}, volume = {41}, pages = {968}, year = {2011} } @article {, author = {Alvarez-Pellitero P}, title = {Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects}, journal = {Veterinary Immunology and Immunopathology}, volume = {126}, pages = {171}, year = {2008} } @article {, author = {Braden LM}, author = {Barker DE}, author = {Koop BF}, author = {Jones SRM}, title = {Comparative defense-associated responses in salmon skin elicited by the ectoparasite Lepeophtheirus salmonis}, journal = {Comparative Biochemistry and Physiology Part D: Genomics and Proteomics}, volume = {7}, pages = {100}, year = {2012} } @article {, author = {Braden LM}, author = {Koop BF}, author = {Jones SRM}, title = {Signatures of resistance to Lepeophtheirus salmonis include a TH2-type response at the louse-salmon interface}, journal = {Developmental \& Comparative Immunology}, volume = {48}, pages = {178}, year = {2015} } @article {, author = {Braden LM}, author = {Sutherland BJG}, author = {Koop BF}, author = {Jones SRM}, title = {Enhanced transcriptomic responses in the Pacific salmon louse Lepeophtheirus salmonis oncorhynchi to the non-native Atlantic salmon Salmo salar suggests increased parasite fitness}, journal = {BMC Genomics}, volume = {18}, pages = {110}, year = {2017} } @article {, author = {Bricknell I}, author = {Dalmo RA}, title = {The use of immunostimulants in fish larval aquaculture}, journal = {Fish \& Shellfish Immunology}, volume = {19}, pages = {457}, year = {2005} } @article {, author = {Burka JF}, author = {Hammell KL}, author = {Horsberg TE}, author = {Johnson GR}, author = {Rainnie DJ}, author = {Speare DJ}, title = {Drugs in salmonid aquaculture—a review}, journal = {Journal of Veterinary Pharmacology and Therapeutics}, volume = {20}, pages = {333}, year = {1997} } @article {, author = {Burridge L}, author = {Weis JS}, author = {Cabello F}, author = {Pizarro J}, author = {Bostick K}, title = {Chemical use in salmon aquaculture: a review of current practices and possible environmental effects}, journal = {Aquaculture}, volume = {306}, pages = {7}, year = {2010} } @article {, author = {Casadei E}, author = {Bird S}, author = {Vecino JLG}, author = {Wadsworth S}, author = {Secombes CJ}, title = {The effect of peptidoglycan enriched diets on antimicrobial peptide gene expression in rainbow trout (Oncorhynchus mykiss)}, journal = {Fish \& Shellfish Immunology}, volume = {34}, pages = {529}, year = {2013} } @article {, author = {Costello MJ}, title = {The global economic cost of sea lice to the salmonid farming industry}, journal = {Journal of Fish Diseases}, volume = {32}, pages = {115}, year = {2009} } @article {, author = {Covello JM}, author = {Friend SE}, author = {Purcell SL}, author = {Burka JF}, author = {Markham RJF}, author = {Donkin AW}, title = {Effects of orally administered immunostimulants on inflammatory gene expression and sea lice (Lepeophtheirus salmonis) burdens on Atlantic salmon (Salmo salar)}, journal = {Aquaculture}, volume = {366–367}, pages = {9}, year = {2012} } @article {, author = {Du X-Y}, author = {Clemetson KJ}, title = {Snake venom L-amino acid oxidases}, journal = {Toxicon}, volume = {40}, pages = {659}, year = {2002} } @article {, author = {Fast MD}, title = {Fish immune responses to parasitic copepod (namely sea lice) infection}, journal = {Developmental \& Comparative Immunology}, volume = {43}, pages = {300}, year = {2014} } @article {, author = {Fast MD}, author = {Burka JF}, author = {Johnson SC}, author = {Ross NW}, title = {Enzymes released from Lepeophtheirus salmonis in response to mucus from different salmonids}, journal = {Journal of Parasitology}, volume = {89}, pages = {7}, year = {2003} } @article {, author = {Fast MD}, author = {Ross NW}, author = {Craft CA}, author = {Locke SJ}, author = {MacKinnon SL}, author = {Johnson SC}, title = {Lepeophtheirus salmonis: characterization of prostaglandin E2 in secretory products of the salmon louse by RP-HPLC and mass spectrometry}, journal = {Experimental Parasitology}, volume = {107}, pages = {5}, year = {2004} } @article {, author = {Fast MD}, author = {Johnson SC}, author = {Eddy TD}, author = {Pinto D}, author = {Ross NW}, title = {Lepeophtheirus salmonis secretory/excretory products and their effects on Atlantic salmon immune gene regulation}, journal = {Parasite Immunology}, volume = {29}, pages = {179}, year = {2007} } @article {, author = {Francischetti IMB}, author = {Sa-Nunes A}, author = {Mans BJ}, author = {Santos IM}, author = {Ribeiro JMC}, title = {The role of saliva in tick feeding}, journal = {Frontiers in Bioscience}, volume = {14}, pages = {2051}, year = {2009} } @article {, author = {Frost P}, author = {Nilsen F}, title = {Validation of reference genes for transcription profiling in the salmon louse, Lepeophtheirus salmonis, by quantitative real-time PCR}, journal = {Veterinary Parasitology}, volume = {118}, pages = {169}, year = {2003} } @article {, author = {Gharbi K}, author = {Matthews L}, author = {Bron J}, author = {Roberts R}, author = {Tinch A}, author = {Stear M}, title = {The control of sea lice in Atlantic salmon by selective breeding}, journal = {Journal of the Royal Society Interface}, volume = {12}, pages = {20150574}, year = {2015} } @article {, author = {Gjerde B}, author = {Ødegård J}, author = {Thorland I}, title = {Estimates of genetic variation in the susceptibility of Atlantic salmon (Salmo salar) to the salmon louse Lepeophtheirus salmonis}, journal = {Aquaculture}, volume = {314}, pages = {66}, year = {2011} } @article {, author = {Hamre LA}, author = {Eichner C}, author = {Caipang CMA}, author = {Dalvin ST}, author = {Bron JE}, author = {Nilsen F}, title = {The salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae) life cycle has only two chalimus stages}, journal = {PLoS ONE}, volume = {8}, pages = {e73539}, year = {2013} } @article {, author = {Hellemans J}, author = {Mortier G}, author = {De Paepe A}, author = {Speleman F}, author = {Vandesompele J}, title = {qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data}, journal = {Genome Biology}, volume = {8}, pages = {R19}, year = {2007} } @article {, author = {Igboeli OO}, author = {Fast MD}, author = {Heumann J}, author = {Burka JF}, title = {Role of P-glycoprotein in emamectin benzoate (SLICE®) resistance in sea lice, Lepeophtheirus salmonis}, journal = {Aquaculture}, volume = {344–349}, pages = {40}, year = {2012} } @article {, author = {Igboeli OO}, author = {Purcell SL}, author = {Wotton H}, author = {Poley J}, author = {Burka JF}, author = {Fast MD}, title = {Immunostimulation of Salmo salar L., and its effect on Lepeophtheirus salmonis (Krøyer) P-glycoprotein mRNA expression following subsequent emamectin benzoate exposure}, journal = {Journal of Fish Diseases}, volume = {36}, pages = {339}, year = {2013} } @article {, author = {Igboeli OO}, author = {Burka JF}, author = {Fast MD}, title = {Sea lice population and sex differences in P-glycoprotein expression and emamectin benzoate resistance on salmon farms in the Bay of Fundy, New Brunswick, Canada}, journal = {Pest Management Science}, volume = {70}, pages = {905}, year = {2014} } @article {, author = {Iliev DB}, author = {Skjæveland I}, author = {Jørgensen JB}, title = {CpG oligonucleotides bind TLR9 and RRM-containing proteins in Atlantic salmon (Salmo salar)}, journal = {BMC Immunology}, volume = {14}, pages = {12}, year = {2013} } @article {, author = {Jensen LB}, author = {Provan F}, author = {Larssen E}, author = {Bron JE}, author = {Obach A}, title = {Reducing sea lice (Lepeophtheirus salmonis) infestation of farmed Atlantic salmon (Salmo salar L.) through functional feeds}, journal = {Aquaculture Nutrition}, volume = {21}, pages = {983}, year = {2015} } @article {, author = {Johansson KC}, author = {Metzendorf C}, author = {Söderhäll K}, title = {Microarray analysis of immune challenged Drosophila hemocytes}, journal = {Experimental Cell Research}, volume = {305}, pages = {145}, year = {2005} } @article {, author = {Johnson SC}, author = {Albright LJ}, title = {Comparative susceptibility and histopathology of the response of naive Atlantic, chinook and coho salmon to experimental infection with Lepeophtheirus salmonis (Copepoda: Caligidae)}, journal = {Diseases of Aquatic Organisms}, volume = {14}, pages = {179}, year = {1992} } @article {, author = {Jones SRM}, author = {Fast MD}, author = {Johnson SC}, author = {Groman DB}, title = {Differential rejection of salmon lice by pink and chum salmon: disease consequences and expression of proinflammatory genes}, journal = {Diseases of Aquatic Organisms}, volume = {75}, pages = {229}, year = {2007} } @article {, author = {Jones SRM}, author = {Fast MD}, author = {Johnson SC}, title = {Influence of reduced feed ration on Lepeophtheirus salmonis infestation and inflammatory gene expression in juvenile pink salmon}, journal = {Journal of Aquatic Animal Health}, volume = {20}, pages = {103}, year = {2008} } @article {, author = {Jones SRM}, author = {Kim E}, author = {Bennett W}, title = {Early development of resistance to the salmon louse, Lepeophtheirus salmonis (Krøyer), in juvenile pink salmon, Oncorhynchus gorbuscha (Walbaum)}, journal = {Journal of Fish Diseases}, volume = {31}, pages = {591}, year = {2008} } @article {, author = {Kolstad K}, author = {Heuch PA}, author = {Gjerde B}, author = {Gjedrem T}, author = {Salte R}, title = {Genetic variation in resistance of Atlantic salmon (Salmo salar) to the salmon louse Lepeophtheirus salmonis}, journal = {Aquaculture}, volume = {247}, pages = {145}, year = {2005} } @article {, author = {Martens JHA}, author = {Verlaan M}, author = {Kalkhoven E}, author = {Zantema A}, title = {Cascade of distinct histone modifications during collagenase gene activation}, journal = {Molecular and Cellular Biology}, volume = {23}, pages = {1808}, year = {2003} } @article {, author = {McNair CM}, title = {Ectoparasites of medical and veterinary importance: drug resistance and the need for alternative control methods}, journal = {Journal of Pharmacy and Pharmacology}, volume = {67}, pages = {351}, year = {2015} } @article {, author = {Medzhitov R}, title = {Recognition of microorganisms and activation of the immune response}, journal = {Nature}, volume = {449}, pages = {819}, year = {2007} } @article {, author = {Núñez-Acuña G}, author = {Gonçalves AT}, author = {Valenzuela-Muñoz V}, author = {Pino-Marambio J}, author = {Wadsworth S}, author = {Gallardo-Escárate C}, title = {Transcriptome immunomodulation of in-feed additives in Atlantic salmon Salmo salar infested with sea lice Caligus rogercresseyi}, journal = {Fish \& Shellfish Immunology}, volume = {47}, pages = {450}, year = {2015} } @article {, author = {Núñez-Acuña G}, author = {Vera-Bizama F}, author = {Boltaña S}, author = {Hawes C}, author = {Marambio JP}, author = {Wadsworth S}, title = {In-feed additives modulate ionotropic receptor genes from the sea louse Caligus rogercresseyi: a comparative analysis in two host salmonid species}, journal = {Aquaculture}, volume = {451}, pages = {99}, year = {2016} } @article {, author = {Perkins JR}, author = {Dawes JM}, author = {McMahon SB}, author = {Bennett DLH}, author = {Orengo C}, author = {Kohl M}, title = {ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data}, journal = {BMC Genomics}, volume = {13}, pages = {296}, year = {2012} } @article {, author = {Pike AW}, author = {Wadsworth SL}, title = {Sealice on salmonids: their biology and control}, journal = {Advances in Parasitology}, volume = {44}, pages = {233}, year = {1999} } @article {, author = {Poley J}, author = {Purcell SL}, author = {Igboeli OO}, author = {Donkin A}, author = {Wotton H}, author = {Fast MD}, title = {Combinatorial effects of administration of immunostimulatory compounds in feed and follow-up administration of triple-dose SLICE® (emamectin benzoate) on Atlantic salmon, Salmo salar L., infection with Lepeophtheirus salmonis}, journal = {Journal of Fish Diseases}, volume = {36}, pages = {299}, year = {2013} } @article {, author = {Purcell SL}, author = {Friend SE}, author = {Covello JM}, author = {Donkin A}, author = {Groman DB}, author = {Poley J}, title = {CpG inclusion in feed reduces sea lice, Lepeophtheirus salmonis, numbers following re-infection}, journal = {Journal of Fish Diseases}, volume = {36}, pages = {229}, year = {2013} } @article {, author = {Raynard RS}, author = {Bricknell IR}, author = {Billingsley PF}, author = {Nisbet AJ}, author = {Vigneau A}, author = {Sommerville C}, title = {Development of vaccines against sea lice}, journal = {Pest Management Science}, volume = {58}, pages = {569}, year = {2002} } @article {, author = {Ritchie ME}, author = {Silver J}, author = {Oshlack A}, author = {Holmes M}, author = {Diyagama D}, author = {Holloway A}, title = {A comparison of background correction methods for two-colour microarrays}, journal = {Bioinformatics}, volume = {23}, pages = {2700}, year = {2007} } @article {, author = {Skugor S}, author = {Glover KA}, author = {Nilsen F}, author = {Krasonov A}, title = {Local and systemic gene expression responses of Atlantic salmon (Salmo salar L.) to infection with the salmon louse (Lepeophtheirus salmonis)}, journal = {BMC Genomics}, volume = {9}, pages = {498}, year = {2008} } @article {, author = {Smyth GK}, title = {Linear models and empirical Bayes methods for assessing differential expression in microarray experiments}, journal = {Statistical Applications in Genetics and Molecular Biology}, volume = {3}, pages = {1}, year = {2004} } @article {, author = {Smyth GK}, author = {Speed T}, title = {Normalization of cDNA microarray data}, journal = {Methods}, volume = {31}, pages = {265}, year = {2003} } @article {, author = {Sutherland BJG}, author = {Jantzen SG}, author = {Sanderson DS}, author = {Koop BF}, author = {Jones SRM}, title = {Differentiating size-dependent responses of juvenile pink salmon (Oncorhynchus gorbuscha) to sea lice (Lepeophtheirus salmonis) infections}, journal = {Comparative Biochemistry and Physiology Part D: Genomics and Proteomics}, volume = {6}, pages = {213}, year = {2011} } @article {, author = {Sutherland BJG}, author = {Jantzen SG}, author = {Yasuike M}, author = {Sanderson DS}, author = {Koop BF}, author = {Jones SRM}, title = {Transcriptomics of coping strategies in free-swimming Lepeophtheirus salmonis (Copepoda) larvae responding to abiotic stress}, journal = {Molecular Ecology}, volume = {21}, pages = {6000}, year = {2012} } @article {, author = {Sutherland BJG}, author = {Koczka KW}, author = {Yasuike M}, author = {Jantzen SG}, author = {Yazawa R}, author = {Koop BF}, title = {Comparative transcriptomics of Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha during infections with salmon lice Lepeophtheirus salmonis}, journal = {BMC Genomics}, volume = {15}, pages = {200}, year = {2014} } @article {, author = {Sutherland BJG}, author = {Poley JD}, author = {Igboeli OO}, author = {Jantzen JR}, author = {Fast MD}, author = {Koop BF}, title = {Transcriptomic responses to emamectin benzoate in Pacific and Atlantic Canada salmon lice Lepeophtheirus salmonis with differing levels of drug resistance}, journal = {Evolutionary Applications}, volume = {8}, pages = {133}, year = {2015} } @article {, author = {Tadiso TM}, author = {Krasnov A}, author = {Skugor S}, author = {Afanasyev S}, author = {Hordvik I}, author = {Nilsen F}, title = {Gene expression analyses of immune responses in Atlantic salmon during early stages of infection by salmon louse (Lepeophtheirus salmonis) revealed bi-phasic responses coinciding with the copepod-chalimus transition}, journal = {BMC Genomics}, volume = {12}, pages = {141}, year = {2011} } @article {, author = {Tirloni L}, author = {Reck J}, author = {Terra RMS}, author = {Martins JR}, author = {Mulenga A}, author = {Sherman NE}, title = {Proteomic analysis of cattle tick Rhipicephalus (Boophilus) microplus saliva: a comparison between partially and fully engorged females}, journal = {PLoS ONE}, volume = {9}, pages = {e94831}, year = {2014} } @article {, author = {Torrissen O}, author = {Jones SRM}, author = {Asche F}, author = {Guttormsen A}, author = {Skilbrei OT}, author = {Nilsen F}, title = {Salmon lice—impact on wild salmonids and salmon aquaculture}, journal = {Journal of Fish Diseases}, volume = {36}, pages = {171}, year = {2013} } @article {, author = {Vadstein O}, title = {The use of immunostimulation in marine larviculture: possibilities and challenges}, journal = {Aquaculture}, volume = {155}, pages = {401}, year = {1997} } @article {, author = {Vandesompele J}, author = {De Preter K}, author = {Pattyn F}, author = {Poppe B}, author = {Van Roy N}, author = {De Paepe A}, title = {Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes}, journal = {Genome Biology}, volume = {3}, pages = {RESEARCH0034}, year = {2002} } @article {, author = {Veldhoen N}, author = {Ikonomou MG}, author = {Buday C}, author = {Jordan J}, author = {Rehaume V}, author = {Cabecinha M}, title = {Biological effects of the anti-parasitic chemotherapeutant emamectin benzoate on a non-target crustacean, the spot prawn (Pandalus platyceros Brandt, 1851) under laboratory conditions}, journal = {Aquatic Toxicology}, volume = {108}, pages = {94}, year = {2012} } @article {, author = {Wagner GN}, author = {Fast MD}, author = {Johnson SC}, title = {Physiology and immunology of Lepeophtheirus salmonis infections of salmonids}, journal = {Trends in Parasitology}, volume = {24}, pages = {176}, year = {2008} } @article {, author = {Waite JC}, author = {Skokos D}, title = {Th17 response and inflammatory autoimmune diseases}, journal = {International Journal of Inflammation}, volume = {2012}, pages = {819467}, year = {2012} } @article {, author = {Yáñez JM}, author = {Houston RD}, author = {Newman S}, title = {Genetics and genomics of disease resistance in salmonid species}, journal = {Frontiers in Genetics}, volume = {5}, pages = {415}, year = {2014} } @article {, author = {Yasuike M}, author = {Leong J}, author = {Jantzen SG}, author = {von Schalburg KR}, author = {Nilsen F}, author = {Jones SRM}, title = {Genomic resources for sea lice: analysis of ESTs and mitochondrial genomes}, journal = {Marine Biotechnology}, volume = {14}, pages = {155}, year = {2012} }