Sea lampreys elicit strong transcriptomic responses in the lake trout liver during parasitism

Abstract

BackgroundThe sea lamprey (Petromyzon marinus) is a jawless vertebrate that parasitizes fish as an adult and, with overfishing, was responsible for the decline in lake trout (Salvelinus namaycush) populations in the Great Lakes. While laboratory studies have looked at the rates of wounding on various fish hosts, there have been few investigations on the physiological effects of lamprey wounding on the host. In the current study, two morphotypes of lake trout, leans and siscowets, were parasitized in the laboratory by sea lampreys and the liver transcriptomes of parasitized and nonparasitized fish were analyzed by RNA-seq (DESeq2 and edgeR) to determine which genes and gene pathways (Ingenuity Pathway Analysis) were altered by lamprey parasitism.ResultsOverall, genes encoding molecules involved in catalytic (e.g., enzymatic) and binding activities (factors and regulators) predominated the regulated gene lists. In siscowets, the top upregulated gene was growth arrest and DNA-damage-inducible protein and for leans it was interleukin-18-binding protein. In leans, the most significantly downregulated gene was UDP-glucuronosyltransferase 2A2 - DESeq2 or phosphotriesterase related - edgeR. For siscowets, the top downregulated gene was C-C motif chemokine 19 - DESeq2 or GTP-binding protein Rhes - edgeR. Gene pathways associated with inflammatory-related responses or factors (cytokines, chemokines, oxidative stress, apoptosis) were regulated following parasitism in both morphotypes. However, pathways related to energy metabolism (glycolysis, gluconeogenesis, lipolysis, lipogenesis) were also regulated. These pathways or the intensity or direction (up/downregulation) of regulation were different between leans and siscowets. Finally, one of the most significantly downregulated pathways in both leans and siscowets was the kynurenine (tryptophan degradation) pathway.ConclusionsThe results indicate a strong transcriptional response in the lake trout to lamprey parasitism that entails genes involved in the regulation of inflammation and cellular damage. Responses to energy utilization as well as hydromineral balance also occurred indicating an adjustment in the host to energy demands and osmotic imbalances during parasitism. Given the role of the kynurenine pathway in promoting immunotolerance in mammals, the downregulation observed in this pathway during parasitism may signify an attempt by the host to inhibit any feedback suppression of the immune response to the lamprey.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2959-9) contains supplementary material, which is available to authorized users.

Further evidence from common garden rearing experiments of heritable traits separating lean and siscowet lake charr (Salvelinus namaycush) ecotypes

“…These results indicate that many of the same loci which differentiate lake charr ecotypes may be involved with lipid metabolism in both ecotypes. Our results are supported by previous transcriptomic work showing that multiple genes in the liver involved in lipid metabolism and transport were expressed differentially between the ecotypes (Goetz et al, 2010, 2016). Finally, so far studies of wild populations have been unable to identify large effect loci differentiating ecotypes, and instead have hypothesized a polygenic mechanism is involved in phenotypic differences observed among ecotypes (Baillie, Muir, Hansen, et al, 2016; Perreault‐Payette et al, 2017).…”

“…This may suggest that the QTL we located is linked to other growth and energy metabolism traits that covary with lipid content. In prior studies with the parents of the F2s, liver transcripts involved in lipid binding and metabolism were differentially expressed between the ecotypes (Goetz et al, 2010, 2016), but the QTL region and candidate SNPs did not contain markers in any of those specific genes.…”

A chromosome‐anchored genome assembly for Lake Trout (Salvelinus namaycush)

“…Data were deposited in sequence read archives associated with BioProject PRJNA682236. These sequencing reads, along with those from two previous RNAseq experiments for liver and muscle tissue (Goetz et al, 2010 ; Goetz et al, 2016 : SRA Accessions SRS005644 and SRS387865), were used as input for NCBI’s Eukaryotic Genome Annotation Pipeline (Thibaud‐Nissen et al, 2016 ). A collection of 3547 Atlantic Salmon transcripts were also used as input.…”

A chromosome-anchored genome assembly for Lake Trout (Salvelinus namaycush)

“…Data were deposited in sequence read archives associated with BioProject PRJNA682236. These sequencing reads, along with those from two previous RNAseq experiments (Goetz et al 2010;Goetz et al 2016), were used as input for NCBI's Eukaryotic Genome Annotation Pipeline (Thibaud-Nissen et al 2016).…”