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

Abstract

Invasive parasites are involved in population declines of new host species worldwide. The high susceptibilities observed in many novel hosts have been attributed to the lack of protective immunity to the parasites which native hosts acquired during their shared evolution. We experimentally infected Japanese eels (Anguilla japonica) and European eels (Anguilla anguilla) with Anguillicola crassus, a nematode parasite that is native to the Japanese eel and invasive in the European eel. We inferred gene expression changes in head kidney tissue from both species, using RNA‐seq data to determine the responses at two time points during the early stages of infection (3 and 23 days postinfection). At both time points, the novel host modified the expression of a larger and functionally more diverse set of genes than the native host. Strikingly, the native host regulated immune gene expression only at the earlier time point and to a small extent while the novel host regulated these genes at both time points. A low number of differentially expressed immune genes, especially in the native host, suggest that a systemic immune response was of minor importance during the early stages of infection. Transcript abundance of genes involved in cell respiration was reduced in the novel host which may affect its ability to cope with harsh conditions and energetically demanding activities. The observed gene expression changes in response to a novel parasite that we observed in a fish follow a general pattern observed in amphibians and mammals, and suggest that the disruption of physiological processes, rather than the absence of an immediate immune response, is responsible for the higher susceptibility of the novel host.

Encapsulation of Anguillicola crassus reduces the abundance of adult parasite stages in the European eel (Anguilla anguilla)

“…We hypothesized that encapsulation in a natural population may trigger an immune response and lead to increased expression of mhc II genes. Cox1 expression was reduced in European eels experimentally infected with A. crassus (Bracamonte, Johnston, Monaghan, et al., 2019). We hypothesized that the disruption of the energy balance would be mitigated by encapsulation, resulting in higher expression of cox1 .…”

“…Consistent with higher oxygen demand with infection severity, the expression of the haemoglobin α gene was correlated with parasite biomass in experimental infections (Fazio et al., 2009). Down‐regulation of several cytochrome genes of the cell respiration pathway indicated that energy provision may be compromised in experimentally infected European eels, which may be due to alteration of resource allocation in infected individuals (Bracamonte, Johnston, Monaghan, et al., 2019).…”

“…Genes were selected based on differential expression in transcriptome‐wide expression studies on European eels and Japanese eels experimentally infected with A. crassus . Mhc IIA and mhc IIB both had altered expression profiles in experimentally infected European eels (Bracamonte, Johnston, Knopf, et al., 2019; Bracamonte, Johnston, Monaghan, et al., 2019). We hypothesized that encapsulation in a natural population may trigger an immune response and lead to increased expression of mhc II genes.…”

“…We hypothesized that the disruption of the energy balance would be mitigated by encapsulation, resulting in higher expression of cox1 . The expression of epor was increased in Japanese eels following A. crassus infections (Bracamonte, Johnston, Monaghan, et al., 2019). We expected increased expression in more heavily infected European eels, especially in the presence of blood‐feeding adults.…”

Assembly-free rapid differential gene expression analysis in non-model organisms using DNA-protein alignment

“…On the other hand, driven by declining costs, RNA-seq is becoming increasingly accessible to labs with modest resources; and as a result, it is being employed on an everexpanding catalog of non-model organisms, pervading the fields of agriculture, aquaculture, ecology, and environment. A very short list of recent studies include: environmental stress response in sea-trout [3], coral [4], ryegrass [5], pigeonpea [6], tiger barb [7]; immune response to parasites and pathogens in guppy [8], eel [9], silkworm [10], peanut [11], sunflower [12]; mechanisms of phenotypic divergence in hares [13], bats [14], grass carps [15]; effect of diet in the growth and development in shrimp [16], yellow perch [17], mandarin fish [18], grenadier anchovy [19], catfish [20], tilapia [21], bass [22]. It is only likely that RNA-seq will continue to rapidly proliferate while high-quality reference databases grow at a slow pace.…”