scholarly journals The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

2020 ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Jérôme Laroche ◽  
Halim Maaroufi ◽  
Hélène Martin ◽  
Kyung-Mee Moon ◽  
...  
Keyword(s):  
Gasterosteus Aculeatus ◽  
Gene Prediction ◽  
Life Stage ◽  
Complex Mixture ◽  
Fish Host ◽  
Complex Life Cycle ◽  
Host Manipulation ◽  
Immune Functions ◽  
Phospholipid Scramblase ◽  
Schistocephalus Solidus

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.

scholarly journals The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Chloé Suzanne Berger ◽  
Jérôme Laroche ◽  
Halim Maaroufi ◽  
Hélène Martin ◽  
Kyung-Mee Moon ◽  
...  
Keyword(s):  
Gasterosteus Aculeatus ◽  
Gene Prediction ◽  
Life Stage ◽  
Cell Communication ◽  
Complex Mixture ◽  
Fish Host ◽  
Complex Life Cycle ◽  
Host Manipulation ◽  
Immune Functions ◽  
Schistocephalus Solidus

Abstract 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

The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host

Parasitology ◽  
2003 ◽  
Vol 126 (4) ◽  
pp. 369-378 ◽  
Author(s):  
M. CHRISTEN ◽  
M. MILINSKI
Keyword(s):  
Intermediate Host ◽  
Gasterosteus Aculeatus ◽  
Life Stage ◽  
Life History Strategy ◽  
Body Cavity ◽  
Infected Fish ◽  
Mixed Mating ◽  
Schistocephalus Solidus ◽  
Self Fertilization ◽  
Second Intermediate Host

Many hermaphroditic parasites reproduce by both cross-fertilization and self-fertilization. To understand the maintenance of such mixed mating systems it is necessary to compare the fitness consequences of the two reproductive modes. This has, however, almost never been done in the context of host–parasite coevolution. Here we show the consequences of outcrossing and selfing in an advanced life-stage of the cestode Schistocephalus solidus, i.e. in its second intermediate host, the three-spined stickleback (Gasterosteus aculeatus). Each juvenile stickleback was simultaneously exposed to 2 experimentally infected copepods, one harbouring outcrossed the other selfed parasites. At 60 days p.i. parasites were removed from the fish's body cavity and, with microsatellite markers, assigned to either outcrossed or selfed origin. Prevalence was not significantly higher in outcrossed parasites. However, those fish that were infected contained significantly more outcrossed than selfed parasites. Thus the probability of a selfed parasite to progress in the life-cycle is reduced in the second intermediate host. Furthermore, we found that even the multiply infected fish increased in weight during the experiment. Nevertheless, total worm weight in multiply infected fish was significantly lower than in singly infected ones, which thus might be a parasite life-history strategy.

Segregation and co-occurrence of larval cestodes in freshwater fishes in the Bothnian Bay, Finland

Parasitology ◽  
1992 ◽  
Vol 104 (1) ◽  
pp. 161-168 ◽  
Author(s):  
K. I. Andersen ◽  
E. T. Valtonen
Keyword(s):  
Fish Species ◽  
Definitive Host ◽  
Gasterosteus Aculeatus ◽  
Infected Fish ◽  
Fish Host ◽  
Cestode Species ◽  
Larval Population ◽  
Schistocephalus Solidus ◽  
Bothnian Bay ◽  
Diphyllobothrium Latum

SUMMARYTwo autogenic (Triaenophorus crassus and T. nodulosus) and four allogenic (Diphyllobothrium latum, D. dendriticum, D. ditremum and Schistocephalus solidus) larval cestode species were found in 13 out of 31 fish species studied from the Bothnian Bay, NE Baltic. Gasterosteus aculeatus was the most heavily infected fish with 4 larval cestode species; for two of them (D. ditremum and S. solidus) the three-spined stickleback was found to be the required fish intermediate host. Among allogenic cestode species, those restricted to different definitive host species segregated their larval population in relation to the fish host, while, for example, D. ditremum and S. solidus, both maturing in fish-eating birds, had the highest percentage of co-occurrences. D. dendriticum, which had the widest range of definitive hosts, was found in the greatest number (8) of fish species and co-occurred with all other species found except T. crassus. The two autogenic species totally segregated their larval population from each other although they both require pike as definitive host. The ecological and evolutionary relationships behind the patterns found for larval cestodes are discussed.

Maintenance of Schistocephalus solidus in the Laboratory with Observations on Rate of Growth of, and Proglottid Formation in, the Plerocercoid

1969 ◽  
Vol 26 (4) ◽  
pp. 741-752 ◽  
Author(s):  
T. S. C. Orr ◽  
C. A. Hopkins
Keyword(s):  
Gasterosteus Aculeatus ◽  
Fish Host ◽  
Statistical Evidence ◽  
Fresh Weight ◽  
Rate Of Growth ◽  
Schistocephalus Solidus ◽  
Conflicting Evidence ◽  
Mesocyclops Leuckarti

Procedures for the maintenance of Schistocephalus solidus in the laboratory are described: recovery of eggs from low bulk faeces; incubation and hatching of eggs at 25 C; and infection of Cyclops agilis, Diaptomus gracilis, and Mesocyclops leuckarti with procercoids that at 25 C become infective in 10, 8, and 8 days, respectively. Methods for infecting Gasterosteus aculeatus with specific numbers of plerocercoids, and procedures for maintaining infected sticklebacks, are described. The rate of growth of S. solidus in G. aculeatus at 19 C has been determined up to day 83, by which time plerocercoids are infective and weigh 50 mg fresh weight. The problem of speciation in Schistocephalus is discussed with reference to the conflicting evidence concerning the number of proglottids in the plerocercoid. Statistical evidence shows the number of proglottids increases slowly during growth contrary to previous statements, and ontogenesis is discussed with reference to metamerism. Problems of growth of Schistocephalus in the fish host are enumerated.

scholarly journals Experimental evolution of parasitic host manipulation

2019 ◽  
Vol 286 (1895) ◽  
pp. 20182413 ◽  
Author(s):  
Nina Hafer-Hahmann
Keyword(s):  
Experimental Evolution ◽  
Fish Host ◽  
Host Manipulation ◽  
Extended Phenotype ◽  
Parasite Fitness ◽  
Three Generations ◽  
Schistocephalus Solidus ◽  
Trade Offs

Host manipulation is a parasite-induced alteration of a host's phenotype that increases parasite fitness. However, if genetically encoded in the parasite, it should be under selection in the parasite. Such host manipulation has often been assumed to be energetically costly, which should restrict its evolution. Evidence of such costs, however, remains elusive. The trophically transmitted cestode Schistocephalus solidus manipulates the activity of its first intermediate copepod host to reduce its predation susceptibility before the parasite is ready for transmission. Thereafter, S. solidus increases host activity to facilitate transmission to its subsequent fish host. I selected S. solidus for or against host manipulation over three generations to investigate the evolvability of manipulation and identify potential trade-offs. Host manipulation responded to selection, confirming that this trait is heritable in the parasite and hence can present an extended phenotype. Changes in host manipulation were not restrained by any obvious costs.

scholarly journals Inter- and intraspecific conflicts between parasites over host manipulation

2016 ◽  
Vol 283 (1824) ◽  
pp. 20152870 ◽  
Author(s):  
Nina Hafer ◽  
Manfred Milinski
Keyword(s):  
Intermediate Host ◽  
Fish Host ◽  
Host Manipulation ◽  
Schistocephalus Solidus ◽  
Common Strategy ◽  
First Intermediate Host

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.

Mitochondrial adenosine triphosphatase activity and temperature adaptation in Schistocephalus solidus (Cestoda: Pseudophyllidea)

Parasitology ◽  
1983 ◽  
Vol 87 (2) ◽  
pp. 307-326 ◽  
Author(s):  
R. W. Walker ◽  
J. Barrett
Keyword(s):  
Temperature Compensation ◽  
Adenosine Triphosphatase ◽  
Gasterosteus Aculeatus ◽  
Arrhenius Plot ◽  
Fish Host ◽  
Temperature Adaptation ◽  
Effect Of Temperature ◽  
Mitochondrial Atpase ◽  
Arrhenius Plots ◽  
Schistocephalus Solidus

SUMMARYDuring its life-cycle, the cestode Schistocephalus solidus is parasitic in both an ectotherm (Gasterosteus aculeatus) and an endotherm (Gallus domesticus) host, and so provides an excellent model with which to study temperature adaptation in parasites. A mitochondrial fraction was prepared from the adults and plerocercoids of S. solidus and from their respective hosts; the activities of the mitochondrial adenosine triphosphatase (ATPase) were then measured over the temperature range 1–45 °C. The plerocercoids of S. solidus show evidence of immediate temperature compensation; this would provide a mechanism for withstanding the abrupt temperature change experienced during infection of the final host. Analysis of the Michaelis constant data suggests that variation of Km, a with temperature may be a major factor in this immediate temperature compensation. In response to acclimation at 5 and 19°C, plerocercoid ATPase showed inverse or paradoxical rate compensation, as did the enzyme from the fish host. Acclimation at the two temperatures had no effect on the Q10 or on the linearity of the Arrhenius plots for the plerocercoid mitochondrial ATPase and only a small effect on the Km a. Acclimation of the fish host again had only a small effect on the Km, a of the fish mitochondrial ATPase but, in contrast to the plerocercoid, there was also a significant effect on the Q10 and the Arrhenius plots. Adult S. solidus ATPase showed partial rate compensation and had a biphasic Arrhenius plot, suggesting that after infection there had been a change in the enzyme or its micro-environment. In terms of the effect of temperature on the Q10 amd Km, a and in the biphasic nature of the Arrhenius plot, the mitochondrial ATPase of adult S. solidus showed similarities with the enzyme from its bird host.

Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus

Parasitology ◽  
2010 ◽  
Vol 137 (11) ◽  
pp. 1681-1686 ◽  
Author(s):  
D. C. HEINS ◽  
E. L. BIRDEN ◽  
J. A. BAKER
Keyword(s):  
Gasterosteus Aculeatus ◽  
Infected Fish ◽  
Threespine Stickleback ◽  
Intensity Of Infection ◽  
Host Fish ◽  
Schistocephalus Solidus ◽  
Second Intermediate Host ◽  
Host Mortality ◽  
Abiotic And Biotic Factors ◽  
Host Behaviour

SUMMARYAn analysis of the metrics of Schistocephalus solidus infection of the threespine stickleback, Gasterosteus aculeatus, in Walby Lake, Alaska, showed that an epizootic ended between 1996 and 1998 and another occurred between 1998 and 2003. The end of the first epizootic was associated with a crash in population size of the stickleback, which serves as the second intermediate host. The likely cause of the end of that epizootic is mass mortality of host fish over winter in 1996–1997. The deleterious impact of the parasite on host reproduction and increased host predation associated with parasitic manipulation of host behaviour and morphology to facilitate transmission might also have played a role, along with unknown environmental factors acting on heavily infected fish or fish in poor condition. The second epizootic was linked to relatively high levels of prevalence and mean intensity of infection, but parasite:host mass ratios were quite low at the peak and there were no apparent mass deaths of the host. A number of abiotic and biotic factors are likely to interact to contribute to the occurrence of epizootics in S. solidus, which appear to be unstable and variable. Epizootics appear to depend on particular and, at times, rare sets of circumstances.

scholarly journals Novel insights from the Plasmodium falciparum sporozoite-specific proteome by probabilistic integration of 26 studies

2021 ◽  
Vol 17 (4) ◽  
pp. e1008067
Author(s):  
Lisette Meerstein-Kessel ◽  
Jeron Venhuizen ◽  
Daniel Garza ◽  
Nicholas I. Proellochs ◽  
Emma J. Vos ◽  
...  
Keyword(s):  
Plasmodium Falciparum ◽  
Salivary Glands ◽  
Molecular Mechanisms ◽  
Life Stage ◽  
Acid Synthesis ◽  
Complex Life Cycle ◽  
Quiescent State ◽  
Extended Phase ◽  
Human Host ◽  
Falciparum Sporozoite

Plasmodium species, the causative agent of malaria, have a complex life cycle involving two hosts. The sporozoite life stage is characterized by an extended phase in the mosquito salivary glands followed by free movement and rapid invasion of hepatocytes in the human host. This transmission stage has been the subject of many transcriptomics and proteomics studies and is also targeted by the most advanced malaria vaccine. We applied Bayesian data integration to determine which proteins are not only present in sporozoites but are also specific to that stage. Transcriptomic and proteomic Plasmodium data sets from 26 studies were weighted for how representative they are for sporozoites, based on a carefully assembled gold standard for Plasmodium falciparum (Pf) proteins known to be present or absent during the sporozoite life stage. Of 5418 Pf genes for which expression data were available at the RNA level or at the protein level, 975 were identified as enriched in sporozoites and 90 specific to them. We show that Pf sporozoites are enriched for proteins involved in type II fatty acid synthesis in the apicoplast and GPI anchor synthesis, but otherwise appear metabolically relatively inactive in the salivary glands of mosquitos. Newly annotated hypothetical sporozoite-specific and sporozoite-enriched proteins highlight sporozoite-specific functions. They include PF3D7_0104100 that we identified to be homologous to the prominin family, which in human has been related to a quiescent state of cancer cells. We document high levels of genetic variability for sporozoite proteins, specifically for sporozoite-specific proteins that elicit antibodies in the human host. Nevertheless, we can identify nine relatively well-conserved sporozoite proteins that elicit antibodies and that together can serve as markers for previous exposure. Our understanding of sporozoite biology benefits from identifying key pathways that are enriched during this life stage. This work can guide studies of molecular mechanisms underlying sporozoite biology and potential well-conserved targets for marker and drug development.

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

Biology Open ◽  
2021 ◽  
Vol 10 (11) ◽  
Author(s):  
Ekaterina V. Borvinskaya ◽  
Albina A. Kochneva ◽  
Polina B. Drozdova ◽  
Olga V. Balan ◽  
Victor G. Zgoda
Keyword(s):  
Model Experiment ◽  
Protein Production ◽  
Culture Medium ◽  
Gasterosteus Aculeatus ◽  
Protein Composition ◽  
Tegument Protein ◽  
Schistocephalus Solidus ◽  
Induced Genes

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.

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