Dataset Information

Outcome of within-host competition demonstrates that parasite virulence doesn't equal success in a myxozoan model system.

ABSTRACT: Within-host competition can affect outcomes of infections when parasites occupy the same niche. We investigated within-host competition and infection outcomes in Chinook salmon exposed to two genotypes of Ceratonova shasta (myxozoan parasite). We assessed i) virulence (host mortality, median days to death), ii) within-host competition (abundance in host), and iii) success (spore production, proportion of myxospore-producing hosts) following concurrent and sequential exposures to single or mixed-genotype treatments. In single treatments, genotype-I replicated faster, and caused higher and earlier host mortality (higher virulence) but genotype-II produced more myxospores (higher success). In mixed treatments, costs of competition were observed for both genotypes evidenced by reduced replication or myxospore production following concurrent exposures, but only the less-virulent genotype suffered costs of competition when hosts were exposed to genotypes sequentially. To understand potential host effects on competition outcomes, we characterized systemic (spleen) and local (intestine) cytokine and immunoglobulin expression in single and mixed infections. We observed delayed systemic and immunosuppressive responses to the virulent genotype (I), rapid, localized and non-suppressive responses to the less-virulent genotype (II), and a combination of responses to mixed-genotypes. Thus, competition outcomes favoring the virulent genotype may be partially explained by the localized response to genotype-II that facilitates myxospore production (success) offsetting the systemic response to genotype-I that results in early inflammation and immunosuppression (that increases onset of mortality). This evidence for different but simultaneous responses to each genotype suggests selection should favor the exclusion of the weaker competitor and the evolution of increased virulence in the stronger competitor because the outcome was generally more costly for the less-virulent genotype. With caveats, our results are relevant for understanding infection outcomes in commercially and ecologically important salmonids in C. shasta endemic regions where mixed infections are commonplace.

SUBMITTER: Hurst CN

PROVIDER: S-EPMC6441732 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Outcome of within-host competition demonstrates that parasite virulence doesn't equal success in a myxozoan model system.

Hurst C N CN Alexander J D JD Dolan B P BP Jia L L Bartholomew J L JL

International journal for parasitology. Parasites and wildlife 20190318

Within-host competition can affect outcomes of infections when parasites occupy the same niche. We investigated within-host competition and infection outcomes in Chinook salmon exposed to two genotypes of <i>Ceratonova shasta</i> (myxozoan parasite). We assessed i) virulence (host mortality, median days to death), ii) within-host competition (abundance in host), and iii) success (spore production, proportion of myxospore-producing hosts) following concurrent and sequential exposures to single or ...[more]

PMID: 30976514

Similar Datasets

Project description:Co-infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co-infections may affect their competitive interactions, thereby influencing the success of the parasites and their impact on the host. This may have important consequence for epidemiological and eco-evolutionary dynamics. We examined in two ecological conditions the effect of sequential co-infection on the outcome of infection by two microsporidians, Vavraia culicis and Edhazardia aedis, that infect the mosquito Aedes aegypti. The two parasites have different transmission strategies: V. culicis is transmitted horizontally either among larvae or from adults to larvae, while E. aedis can be transmitted horizontally among larvae or vertically from females to their eggs. We investigated how the timing and order of the co-infection and how the host's food availability affected the parasite's transmission potential (the percentage of individuals that harboured transmissible spores) and the host's juvenile survival, its age at emergence and its longevity. The outcome of co-infection was strongly affected by the order at which the parasites arrived. In co-infections, V. culicis had greater horizontal transmission if it arrived early, whereas the transmission potential of E. aedis, either vertical or horizontal, was not affected by the competitor V. culicis. The availability of food determined the duration of infection leading to variation in mortality and in the transmission potential. For both parasites low food decreased juvenile survival, delayed emergence to adulthood and increased horizontal transmission potential. High food increased juvenile survival and the probability of emergence with higher vertical transmission for E. aedis. Overall, our results suggest that early infection favours transmission and that (a) V. culicis plastically responded to co-infection, (b) E. aedis was not affected by co-infection but it was more susceptible to factors extending or decreasing the time it spent in the host (time of infection and food). Our results emphasize the complexity of the impact of co-infection on host-parasite interactions. In particular, the timing and order of sequential co-infections can result in different within-host dynamics and modify infection outcomes.

Project description:Motility factors are fundamental for parasite invasion, migration, proliferation and immune evasion and thus can influence parasitic disease pathogenesis and virulence. Salmonid enteronecrosis is caused by a myxozoan (Phylum Cnidarian) parasite, Ceratonova shasta. Three parasite genotypes (0, I, II) occur, with varying degrees of virulence in its host, making it a good model for examining the role of motility in virulence. We compare C. shasta cell motility between genotypes and describe how the cellular protrusions interact with the host. We support these observations with motility gene expression analyses. C. shasta stages can move by single or combined used of filopodia, lamellipodia and blebs, with different behaviors such as static adhesion, crawling or blebbing, some previously unobserved in myxozoans. C. shasta stages showed high flexibility of switching between different morphotypes, suggesting a high capacity to adapt to their microenvironment. Exposure to fibronectin showed that C. shasta stages have extraordinary adhesive affinities to glycoprotein components of the extracellular matrix (ECM). When comparing C. shasta genotypes 0 (low virulence, no mortality) and IIR (high virulence, high mortality) infections in rainbow trout, major differences were observed with regard to their migration to the target organ, gene expression patterns and proliferation rate in the host. IIR is characterized by rapid multiplication and fast amoeboid bleb-based migration to the gut, where adhesion (mediated by integrin-? and talin), ECM disruption and virulent systemic dispersion of the parasite causes massive pathology. Genotype 0 is characterized by low proliferation rates, slow directional and early adhesive migration and localized, non-destructive development in the gut. We conclude that parasite adhesion drives virulence in C. shasta and that effectors, such as integrins, reveal themselves as attractive therapeutic targets in a group of parasites for which no effective treatments are known.

Dataset Information

Outcome of within-host competition demonstrates that parasite virulence doesn't equal success in a myxozoan model system.

Publications

Outcome of within-host competition demonstrates that parasite virulence doesn't equal success in a myxozoan model system.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets