Comparative transcriptomics of stickleback immune gene responses upon infection by two helminth parasites, Diplostomum pseudospathaceum and Schistocephalus solidus

Abstract

Immune systems of vertebrates are much more diverse than previously thought, in particular at the base of the vertebrate clade. RNA-seq was used to describe in detail the transcriptomic response of stickleback hosts to infection by two helminth parasites, the trematode Diplostomum pseudospathaceum (2 genotypes plus a genotype mix) and the cestode Schistocephalus solidus. Based on a global transcription profiling, we present immune genes that are active during chronic or multiple repeated infection. We found that the transcription profiles of D. pseudospathaceum genotypes were as divergent as those of the two parasite species. When comparing the host immune response, only 5 immune genes were consistently upregulated upon infection by both species. These genes indicated a role for enhanced toll like receptor (TLR) activity (CTSK, CYP27B1) and an associated positive regulation of macrophages (CYP27B1, THBS1) for general helminth defense. We interpret the largely differentiated gene expression response among parasite species as general redundancy of the vertebrate immune system, which was also visible in genotype-specific responses among the different D. pseudospathaceum infections. The present study provides the first evidence that IL4-mediated activation of T-helper lymphocyte cells is also important in anti-helminthic immune responses of teleost fish.

Gene expression response to a nematode parasite in novel and native eel hosts

“…RNA‐seq studies of infection experiments on a range of species indicate that the number of affected processes, the magnitude of change, and the specific genes involved differ considerably among host species‐parasite species systems (e.g., Alvarez Rojas et al, ; Haase et al, ; Kumar, Abd‐Elfattah, & El‐Matbouli, ; Zhang et al, ). Infections with invasive parasites have consistently induced a more pronounced response in susceptible hosts compared with resistant hosts.…”

Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host

“…The absence of SsRV1 in stickleback intestines indicates that the virus is excreted while the parasite develops to sexual maturity in the body cavity [62]. The fish liver, spleen, and head kidneys are involved in many biological processes in sticklebacks, such as immune response to infection by S. solidus, metabolism, and energy storage [63][64][65][66][67][68][69]. The excretion of SsRV1 by S. solidus is likely to stimulate the host immune response, but a putative virus replication in hematopoietic organs could prevent it.…”

Hook, Line and Infection

“…The phagocytic activity of granulocytes and monocytes has also been cited as inhibiting Diplostomum migration into the eye (Erasmus, 1959;Ratanarat-Brockelman, 1974). Despite this apparent bias towards the innate response against this parasite, a recent transcriptomic study identified antibody-mediated responses and increased MHC and il-4r expression (a gene in mammals associated with adaptive helminth resistance) in response to infection (Haase et al, 2016). Such results support the notion that the innate and adaptive immune systems cannot be considered in isolation but must be viewed as a fluid and versatile network (Magnad ottir, 2006).…”

“…Sticklebacks can be infected individually in w1 L water containing freshly emerged cercariae; typical exposure doses range from 20 to 220 cercariae per fish (Brassard et al, 1982;Lyholt and Buchmann, 1996;Kalbe and Kurtz, 2006;Scharsack and Kalbe, 2014;Haase et al, 2016) to 5000e 10,000 for other fish species (Sweeting, 1974;Rintam€ aki-Kinnunen et al, 2004). Whilst the parasite rapidly reaches the ocular tissues (within 24 h postinfection; Chappell et al, 1994), D. pseudospathaceum metacercariae establishment is best assessed after 1 week, since low numbers of early infections may be overlooked (Rauch et al, 2006).…”