Genetic Crosses and Linkage Mapping in Schistosome Parasites

Anderson, Timothy J.; LoVerde, Philip T.; Clec’h, Winka Le; Chevalier, Frédéric D.

doi:10.1016/j.pt.2018.08.001

Cited by 32 publications

(26 citation statements)

References 95 publications

(138 reference statements)

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“…Conversely, in low prevalence sites, where coinfections are rare, the SmBRE (LS) strategy and limited virulence to the snail host may be advantageous. Genetic crosses between parasites from these two distinctive S. mansoni populations, followed by a classical quantitative trait locus analysis [44], now provides the opportunity to determine the genetic basis of these key transmission-related phenotypes in an important human helminth infection.…”

Section: Resultsmentioning

confidence: 99%

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Clec’h

Diaz

Chevalier

et al. 2019

Preprint

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BackgroundParasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait – the number of cercariae larvae shed from infected Biomphalaria spp. snails – varies significantly within and between different parasite populations and selection experiments demonstrate that this variation has a strong genetic basis. In this study, we compared the transmission strategies of two laboratory schistosome population and their consequences for their snail host.MethodsWe infected inbred Biomphalaria glabrata snails using two Schistosoma mansoni parasite populations (SmBRE and SmLE), both isolated from Brazil and maintained in the laboratory for decades. We compared life history traits of these two parasite populations by quantifying sporocyst growth within infected snails (assayed using qPCR), output of cercaria larvae, and impact on snail host physiological response (i.e. hemoglobin rate, laccase-like activity) and survival.ResultsWe identified striking differences in virulence and transmission between the two studied parasite populations. SmBRE (low shedder (LS) parasite population) sheds very low numbers of cercariae, and causes minimal impact on the snail physiological response (i.e. laccase-like activity, hemoglobin rate and snail survival). In contrast, SmLE (high shedder (HS) parasite population) sheds 8-fold more cercariae (mean ± se cercariae per shedding: 284±19 vs 2352±113), causes high snail mortality, and has strong impact on snail physiology. We found that HS sporocysts grow more rapidly inside the snail host, comprising up to 60% of cells within infected snails, compared to LS sporocysts which comprised up to 31%. Cercarial production is strongly correlated to the number of S. mansoni sporocyst cells present within the snail host tissue, although the proportion of sporocyst cells alone does not explain the low cercarial shedding of SmBRE.ConclusionsWe demonstrated the existence of alternative transmission strategies in the S. mansoni parasite consistent with trade-offs between parasite transmission and host survival: a “boom-bust” strategy characterized by high virulence, high transmission and short duration infections and a “slow and steady” strategy with low virulence, low transmission but long duration of snail host infections.

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Section: Resultsmentioning

confidence: 99%

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Clec’h

Diaz

Chevalier

et al. 2019

Preprint

Self Cite

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“…Linkage mapping has been applied to P. falciparum to identify key genes related to drug resistance and cell development (Ranford-Cartwright and Mwangi, 2012). This method has made it possible to map genes, causing a given phenotype, to genome regions and to find the responsible genes and/or mutations by performing functional genomics experiments (Anderson et al, 2018). Additionally, there are a number of next-generation sequencing tools that can be used to explore the components of the EV cargo as well as the evolutionary history of host-parasite interaction mediated by EVs.…”

Section: Testing For the Role Of Evsmentioning

confidence: 99%

Extracellular Vesicles Could Carry an Evolutionary Footprint in Interkingdom Communication

Corrêa

Caballero

León

et al. 2020

Front. Cell. Infect. Microbiol.

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Extracellular vesicles (EVs) are minute particles secreted by the cells of living organisms. Although the functional role of EVs is not yet clear, recent work has highlighted their role in intercellular communication. Here, we expand on this view by suggesting that EVs can also mediate communication among interacting organisms such as hosts, pathogens and vectors. This inter-kingdom communication via EVs is likely to have important evolutionary consequences ranging from adaptation of parasites to specialized niches in the host, to host resistance and evolution and maintenance of parasite virulence and transmissibility. A potential system to explore these consequences is the interaction among the human host, the mosquito vector and Plasmodium parasite involved in the malaria disease. Indeed, recent studies have found that EVs derived from Plasmodium infected red blood cells in humans are likely mediating the parasite's transition from the asexual to sexual stage, which might facilitate transmission to the mosquito vector. However, more work is needed to establish the adaptive consequences of this EV signaling among different taxa. We suggest that an integrative molecular approach, including a comparative phylogenetic analysis of the molecules (e.g., proteins and nucleic acids) derived from the EVs of interacting organisms (and their closely-related species) in the malaria system will prove useful for understanding interkingdom communication. Such analyses will also shed light on the evolution and persistence of host, parasite and vector interactions, with implications for the control of vector borne infectious diseases.

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“…Besides the medical importance of Schistosoma spp. in human health, these parasites are very intriguing as biological, genetic, and evolutionary models [3,4]. The life cycle of schistosomes comprises seven morphologically discrete stages: egg, miracidium, mother sporocyst, daughter sporocyst, cercaria, schistosomulum, and adult.…”

Section: Introductionmentioning

confidence: 99%

Duplex real-time PCR for sexing Schistosoma japonicum cercariae based on W chromosome-specific genes and its applications

et al. 2020

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As a unique feature among otherwise hermaphroditic trematodes, Schistosoma species are gonochoric parasites whose sex is genetically determined (ZZ for males and ZW for females). However, schistosome larvae are morphologically identical, and sex can only be discriminated by molecular methods. Here, we integrated published Schistosoma. japonicum transcriptome and genome data to identify W chromosome-specific genes as sex biomarkers. Three W chromosome-specific genes of S. japonicum were identified as sex biomarkers from a panel of 12 genes expressed only in females. An efficient duplex realtime PCR (qPCR) method for sexing cercariae was developed which could identify the sex of cercariae within 2 h without DNA extraction. Moreover, this method can be used to identify not only single-sex but also mixed-sex schistosome-infected snails. We observed a nearly equal proportion of single-male, single-female, and mixed-sex schistosome infections in artificially infected snails. Sex-known schistosome-infected snail models can be efficiently constructed with the aid of duplex qPCR. A field study revealed that single-sex schistosome infections were predominant among naturally infected snails. Finally, a schistosomiasis mouse model based on sex-known cercariae infection was shown to be more reliable than a model based on sex-unknown cercariae infection. The developed duplex qPCR method for sexing S. japonicum cercariae can be widely used for schistosomiasis modeling, genetic experiments, and field-based molecular epidemiological studies.

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Genetic Crosses and Linkage Mapping in Schistosome Parasites

Cited by 32 publications

References 95 publications

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Extracellular Vesicles Could Carry an Evolutionary Footprint in Interkingdom Communication

Duplex real-time PCR for sexing Schistosoma japonicum cercariae based on W chromosome-specific genes and its applications

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