Dual RNA-seq reveals no plastic transcriptional response of the coccidian parasite Eimeria falciformis to host immune defenses

Abstract

BackgroundParasites can either respond to differences in immune defenses that exist between individual hosts plastically or, alternatively, follow a genetically canalized (“hard wired”) program of infection. Assuming that large-scale functional plasticity would be discernible in the parasite transcriptome we have performed a dual RNA-seq study of the lifecycle of Eimeria falciformis using infected mice with different immune status as models for coccidian infections.ResultsWe compared parasite and host transcriptomes (dual transcriptome) between naïve and challenge infected mice, as well as between immune competent and immune deficient ones. Mice with different immune competence show transcriptional differences as well as differences in parasite reproduction (oocyst shedding). Broad gene categories represented by differently abundant host genes indicate enrichments for immune reaction and tissue repair functions. More specifically, TGF-beta, EGF, TNF and IL-1 and IL-6 are examples of functional annotations represented differently depending on host immune status. Much in contrast, parasite transcriptomes were neither different between Coccidia isolated from immune competent and immune deficient mice, nor between those harvested from naïve and challenge infected mice. Instead, parasite transcriptomes have distinct profiles early and late in infection, characterized largely by biosynthesis or motility associated functional gene groups, respectively. Extracellular sporozoite and oocyst stages showed distinct transcriptional profiles and sporozoite transcriptomes were found enriched for species specific genes and likely pathogenicity factors.ConclusionWe propose that the niche and host-specific parasite E. falciformis uses a genetically canalized program of infection. This program is likely fixed in an evolutionary process rather than employing phenotypic plasticity to interact with its host. This in turn might limit the potential of the parasite to adapt to new host species or niches, forcing it to coevolve with its host.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4095-6) contains supplementary material, which is available to authorized users.

Eimeria falciformisBayerHaberkorn1970 and novel wild derived isolates from house mice: differences in parasite lifecycle, pathogenicity and host immune reactions

“…falciformis BayerHaberkorn1970 (Haberkorn, 1970) Between the two E. falciformis isolates BayerHaberkorn1970 and Brandenburg88 we observed only slight differences in the length of the pre-patent period (time until oocyst shedding, starting at 6 vs. 7 dpi). These results are in agreement with previous reports from the same host (NMRI mice) and the BayerHaberkorn1970 isolate (Stange et al, 2012;Schmid et al, 2012Schmid et al, , 2014Ehret et al, 2017). The pre-patent period for the wild derived E. falciformis isolate (7 dpi) corresponds to that reported for the parasite isolate E. falciformis var praghensis (Mesfin et al, 1978;Kasai et al, 1991), but Mahrt and Shi (1988) and Schito et al (1996) demonstrated slightly longer pre-patent periods (7 or 8 dpi) also in other E. falciformis infections.…”

“…The output of oocysts in our study (for all isolates) was similar or only slightly lower than in previous reports (Schmid et al, 2014;Ehret et al, 2017). Our observation regarding the lifecycle progression of E. ferrisi, agree with the initial description of the life cycle in Mus musculus (Ankrom et al, 1975).…”

“…Parasites are propagated under defined and controlled conditions with the aim to provide infective stages for experiments (Lucius et al, 2017). The procedure allows the parasite to evolve due to mutation and genetic drift or adaptation to the passaging host and environment (Ebert, 1998;Burke, 2012).…”

“…The isolate E. falciformis BayerHaberkorn1970 has been isolated in 1960 (Haberkorn 1970) and since has been propagated in laboratories (first at Bayer animal health, Monheim, Germany; then at the institute for molecular parasitology of the Humboldt University, Berlin, Germany). In nearly 60 years since its isolation E. falciformis BayerHaberkorn1970 has likely become the most commonly used laboratory isolate of rodent Eimeria (Mahrt and Shi 1988;Schito et al, 1996;Steinfelder et al, 2005;Pogonka et al, 2010;Stange et al, 2012;Schmid et al, 2014Schmid et al, , 2012Ehret et al, 2017).…”

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

“…Studies of the European eel using RNA-seq to examine gene expression have found that genes involved in an immune response were differentially expressed in the swim bladder (the site of infection) of naturally infected eels (i.e., containing parasites of all stages) (Schneebauer, Dirks, & Pelster, 2017), as well as in the spleen and the head kidney (immune organs) very soon after experimental infection F I G U R E 1 The Japanese eel (Anguilla japonica) is the native host of Anguillicola crassus, a parasitic swim bladder nematode invasive in the European eel (Anguilla anguilla) (3 dpi, i.e., containing only larvae) . Differential regulation of processes associated with both the innate and the adaptive immune system in immune organs and at the site of infection is a common feature in natural and experimental infections in vertebrates (e.g., Alvarez Rojas et al, 2015;Babayan et al, 2018;Huang et al, 2016) and the gradual shift from the regulation of innate to adaptive immune processes can be observed in gene expression studies (Ehret, Spork, Dieterich, Lucius, & Heitlinger, 2017). Additionally, parasite infections cause differential expression of genes not directly related to an immune response, such as those involved in metabolic processes, tissue repair, or organ function and development (Alvarez Rojas et al, 2015;Babayan et al, 2018;Ronza et al, 2016;Zhang et al, 2017) and this has also been observed in the European eel Schneebauer et al, 2017).…”