Temperature-induced reorganisation of Schistocephalus solidus (Cestoda) proteome during the transition to the warm-blooded host

ABSTRACT The protein composition of the cestode Schistocephalus solidus was measured in an experiment simulating the trophic transmission of the parasite from a cold-blooded to a warm-blooded host. The first hour of host colonisation was studied in a model experiment, in which sticklebacks Gasterosteus aculeatus infected with S. solidus were heated at 40°C for 1 h. As a result, a decrease in the content of one tegument protein was detected in the plerocercoids of S. solidus. Sexual maturation of the parasites was initiated in an experiment where S. solidus larvae were taken from fish and cultured in vitro at 40°C for 48 h. Temperature-independent changes in the parasite proteome were investigated by incubating plerocercoids at 22°C for 48 h in culture medium. Analysis of the proteome allowed us to distinguish the temperature-induced genes of S. solidus, as well as to specify the molecular markers of the plerocercoid and adult worms. The main conclusion of the study is that the key enzymes of long-term metabolic changes (glycogen consumption, protein production, etc.) in parasites during colonisation of a warm-blooded host are induced by temperature.

The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

Background Manipulative parasites are thought to liberate molecules in their external environment, acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. It is necessary to study the molecular interaction between a manipulative parasite and its host to better understand how such alterations evolve. Methods Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes take place in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We produced a novel genome sequence and assembly of S. solidus to improve protein coding gene prediction and annotation for this parasite. We then described the whole worm’s proteome and its secretome during fish host infection using LC–MS/MS. Results A total of 2290 proteins were detected in the proteome of S. solidus, and 30 additional proteins were detected specifically in the secretome. We found that the secretome contains proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We detected receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be manipulation factors. We also detected 12 S. solidus-specific proteins in the secretome that may play important roles in host–parasite interactions. Conclusions Our results suggest that S. solidus liberates molecules with putative host manipulation functions in the host and that many of them are species-specific. Graphical abstract

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Parasites impose fitness costs on their hosts. Biologists therefore tend to assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests selection may instead favor loss of resistance. Immune costs are rarely documented in nature, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes they gained resistance to the freshwater-associated tapeworm, Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation contribute to suppression of cestode growth and viability, but also impose a substantial cost of reduced fecundity. Combining genetic mapping and population genomics, we find that the immune differences between tolerant and resistant populations arise from opposing selection in both populations acting, respectively, to reduce and increase resistance consistent with divergent optimization.

The host phenotype and microbiome varies with infection status, parasite origin and parasite microbiome composition

Background: A growing literature demonstrates the impact of helminths on their host gut microbiome. However, there is now a need to investigate helminth associated microbes and the complex tripartite interactions between parasite, microbes, and hosts. Methods: We investigated whether the stickleback host microbiome depends on eco-evolutionary variables by testing the impact of exposure to the parasite Schistocephalus solidus, infection success, host genotype, parasite genotype, and parasite microbiome composition. Results: We observed constitutive differences in the microbiome of stickleback of different origin that increased when sticklebacks exposed to the parasite resisted infection. In contrast, the microbiome of successfully infected sticklebacks varies with parasite genotype. More specifically, we reveal that the association between microbiome and immune gene expression increases in infected individuals, and varies with parasite genotype. In addition, we showed that S. solidus hosts a complex endo-microbiome and that the abundance and prevalence of an unknown Chloroflexi in the parasite correlate with expression of host immune genes including foxp3, tnfr1, cd97, stat6 and marco. Conclusions: Within this first comprehensive analysis of a cestode’s interaction with bacteria, we demonstrate that (i) regardless of infection success, parasites contribute to modulating the host microbiome, (ii). when infection is successful, the host microbiome varies with parasite genotype due to genotype-dependent variation in parasite immunomodulation, and (iii) the parasite-associated microbiome is distinct from its host’s and contribute to the host immune response to infection. While a growing number of studies focus on determining the genetic and environmental factors contributing to host microbiome composition, this study reveals that parasites, parasite genetic factors, and parasite microbiomes can contribute regardless of whether the infection was successful.

Temperature-induced reorganisation of Schistocephalus solidus (Cestoda) proteome during the transition to the warm-blooded host

The protein composition (proteome) of cestode Schistocephalus solidus was measured in an experiment simulating the transition of the parasite from a cold-blooded to a warm-blooded host. Infective S. solidus plerocercoids obtained from the three-spined stickleback Gasterosteus aculeatus were heated at 40 °C for 1 hour or cultured in vitro at 40 °C and 22 °C for 48 hours. In short-term experiment, the content of only one tegument protein was evidenced to decrease after heating. After long-term heating, which triggered parasite sexual maturation, an increase in the content of ribosomal proteins, translation initiation factors and enzymes of the amino acid biosynthesis pathway was observed. The synthesis of certain gene products for carbohydrate metabolism, including glycolysis/gluconeogenesis, was found to be regulated in parasite by temperature.

Parasite infection disrupts escape behaviours in fish shoals

Many prey species have evolved collective responses to avoid predation. They rapidly transfer information about potential predators to trigger and coordinate escape waves. Predation avoidance behaviour is often manipulated by trophically transmitted parasites, to facilitate their transmission to the next host. We hypothesized that the presence of infected, behaviourally altered individuals might disturb the spread of escape waves. We used the tapeworm Schistocephalus solidus , which increases risk-taking behaviour and decreases social responsiveness of its host, the three-spined stickleback, to test this hypothesis. Three subgroups of sticklebacks were placed next to one another in separate compartments with shelter. The middle subgroup contained either uninfected or infected sticklebacks. We confronted an outer subgroup with an artificial bird strike and studied how the escape response spread through the subgroups. With uninfected sticklebacks in the middle, escape waves spread rapidly through the entire shoal and fish remained in shelter thereafter. With infected sticklebacks in the middle, the escape wave was disrupted and uninfected fish rarely used the shelter. Infected individuals can disrupt the transmission of flight responses, thereby not only increasing their own predation risk but also that of their uninfected shoal members. Our study uncovers a potentially far-reaching fitness consequence of grouping with infected individuals.

Sick of Eating: eco-evo-immuno dynamics of predators and their trophically acquired parasites

When predators consume prey, they risk becoming infected with their prey’s parasites, which can then establish the predator as a secondary host. For example, stickleback in northern temperate lakes consume benthic or limnetic prey, which are intermediate hosts for distinct species of parasites (e.g. Eustrongylides nematodes in benthic oligocheates and Schistocephalus solidus copepods in limnetic copepods). These worms then establish the stickleback as a secondary host and can cause behavioral changes linked to increased predation by birds. In this study, we use a quantitative genetics framework to consider the simultaneous eco-evolutionary dynamics of predator ecomorphology and predator immunity when alternative prey may confer different parasite exposures. When evolutionary tradeoffs are sufficiently weak, predator ecomorphology and immunity are correclated among populations, potentially generating a negative correlation between parasite intake and infection.

The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

ABSTRACTManipulative parasites are predicted to liberate molecules in their external environment acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are expected to be part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes have been described in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We re-sequenced the genome of S. solidus using a combination of long and short reads to improve protein coding gene prediction and annotation for this parasite species. We then described the whole worm’s proteome and its secretome during fish host infection, using LC-MS/MS. A total of 2 290 proteins were detected in the proteome of S. solidus, with 30 proteins detected only in the secretome. We found that the secretome contained proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We also detected Receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be strong manipulation factors. The secretome also contained a Phospholipid scramblase that clustered phylogenetically with a stickleback Phospholipid scramblase, suggesting it could have the potential to interfere with the function of the scramblase in the host’s brain. Finally, we detected 12 S. solidus-specific proteins in the secretome that may play important roles in host-parasite interactions. Our results suggest that this parasite liberates molecules with putative host manipulation functions in the host and that many of them are species specific.