Time series analysis of tegument ultrastructure of in vitro transformed miracidium to mother sporocyst of the human parasite Schistosoma mansoni

Poteaux, Pierre; Gourbal, Benjamin; Duval, David Timothy

doi:10.1016/j.actatropica.2023.106840

Cited by 10 publications

(8 citation statements)

References 44 publications

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“…Within the first ~ 16 h most parasites have shed the cilia plates, and their tegument has been remodelled 8 ; however, parasite in-vitro development is not synchronous. Therefore, we decided to culture the mother sporocysts for 5 days (named ‘D5 sporocysts’) to facilitate the complete transformation of > 95% of the parasites 10 , 21 (Fig. 1 A and Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Striking changes have been reported during the miracidium–sporocyst transition, including shedding of the ciliary plates, tegumental remodelling and an overall tissue reorganisation 21 that transforms the free-living miracidium with ~ 365 cells 17 into a simple ‘sac-like structure’ enriched with stem/germinal cells 10 . With the assistance of a novel machine learning approach 22 , we estimated an average of 169 nuclei in a single D5 mother sporocyst (ranging from 112 to 254 nuclei) and have revealed previously uncharacterised variability in cell number among the parasites at this developmental stage.…”

Section: Discussionmentioning

confidence: 99%

“…The parenchyma cells identified in the D5 sporocyst showed a similar distribution to those in the miracidium 17 . Whilst these cells deliver energy, nutrients, and vitamins to the highly proliferating stem/germinal cells, they also start to degenerate and shrink to provide space for the early daughter sporocyst embryos 10 , 21 . Moreover, particles of complex carbohydrates and lipid droplets have previously been described in the cytoplasm of parenchyma cells (historically described as ‘interstitial cells’) 10 .…”

Section: Discussionmentioning

confidence: 99%

“…GO terms associated with microvilli (‘actin filament binding’ and ‘microtubule-based process’) were significantly enriched in the sporocyst tegument. By day 3 post infection, the sporocyst is completely covered with numerous microvilli that increase the exchange surface of the tegument revealing high absorptive activities during the rapid development of the parasite 10 , 21 . Unlike the schistosome intra-mammalian developmental stages, the sporocysts lack a specialised digestive epithelium (i.e., gastrodermis).…”

Section: Discussionmentioning

confidence: 99%

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Single-cell transcriptomics of the human parasite Schistosoma mansoni first intra-molluscan stage reveals tentative tegumental and stem-cell regulators

Diaz Soria,

Attenborough,

et al. 2024

Sci Rep

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Schistosomiasis is a major Neglected Tropical Disease, caused by the infection with blood flukes in the genus Schistosoma. To complete the life cycle, the parasite undergoes asexual and sexual reproduction within an intermediate snail host and a definitive mammalian host, respectively. The intra-molluscan phase provides a critical amplification step that ensures a successful transmission. However, the cellular and molecular mechanisms underlying the development of the intra-molluscan stages remain poorly understood. Here, single cell suspensions from S. mansoni mother sporocysts were produced and sequenced using the droplet-based 10X Genomics Chromium platform. Six cell clusters comprising two tegument, muscle, neuron, parenchyma and stem/germinal cell clusters were identified and validated by in situ hybridisation. Gene Ontology term analysis predicted key biological processes for each of the clusters, including three stem/germinal sub-clusters. Furthermore, putative transcription factors predicted for stem/germinal and tegument clusters may play key roles during parasite development and interaction with the intermediate host.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Single-cell transcriptomics of the human parasite Schistosoma mansoni first intra-molluscan stage reveals tentative tegumental and stem-cell regulators

Diaz Soria,

Attenborough,

et al. 2024

Sci Rep

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“…The newly appearing tegument of the sporocyst is differentiated by the appearance of the microvilli (Basch & DiConza, 1974). At about 6 h after the transformation of the miracidium into the mother sporocyst in vitro, the microvilli of S. mansoni tegument began to appear and became denser as the development progressed, increasing the exchange surface area (Poteaux et al, 2023). The large increase in the surface area of sporocysts may be related to their ability to actively transport between snail tissues (Uglem & Lee, 1985).…”

Section: Discussionmentioning

confidence: 99%

Molecular detection of Schistosoma haematobium in infected Bulinus truncatus snails associated with immune response

Mansour,

El Einin,

Tadrous

et al. 2023

Microscopy Res & Technique

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Schistosomiasis is one of the most common waterborne parasite illnesses, it is a major public health issue in developing countries. The polymerase chain reaction (PCR) technique is used to find Schistosoma haematobium DNA in Bulinus truncatus, which could speed up the discovery of infections before cercariae are shed. DraI‐PCR detected S. haematobium infection at different infection intervals with bands at 300 bp in shedding snails 40 days after exposure and even on the first day after B. turancuts snails exposure to miracidia. Transmission electron microscopy showed the structure of sporocyst from 1 to 40 days post‐exposure and activated hemocytes in infected non‐shedding snails as well as sporocyst degradation. Flow cytometry was used to measure the percentage of Bax and TGF‐β1 positive stained cells that have been linked with infection progression. In conclusion, molecular tools and immune response play an important role in the strategy of controlling schistosomiasis through the early detection of larval stages in intermediate hosts toward certification of schistosomiasis elimination.Research Highlights DraI‐PCR allowed early detection of S. haematobium at 300 bp in B. truncatus snail. Transmission electron microscopy showed the structure of S. haematobium sporocyst in snail and activated hemocytes in non‐shedding snail. Bax protein that induced apoptotic changes and Transforming Growth Factor Beta1 level have been linked with parasite development.

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A single-cell atlas of the miracidium larva of the human blood flukeSchistosoma mansoni: cell types, developmental pathways and tissue architecture

Rawlinson

Attenborough

Soria

et al. 2023

Preprint

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Schistosomes are parasitic flatworms whose infections affect millions of people worldwide. The parasite has a complex life cycle that is poorly understood at a cellular level. We have developed a cellular transcriptome atlas of the miracidium larva of Schistosoma mansoni, the first post-embryonic stage of development. The miracidium infects a snail host, inside which its stem cells generate daughter sporocysts that give rise to human-infective cercariae larvae. We use a combination of single-cell RNA sequencing, in situ hybridisation and image analysis to characterise the miracidia. Each larva comprises ~365 cells and 19 transcriptionally distinct cell types. We show that 93% of miracidium cells are somatic (>45% neural, 19% muscle, 13% tegument, 2% parenchyma, 2% protonephridia) and the remaining 7% are stem cells. Cellular diversity within tissue types is revealed, including two transcriptionally distinct muscle clusters, corresponding to the circular and the longitudinal muscles of the body wall, as well as two stem cell populations that show different activation states and cluster further by sex. This whole-body atlas provides new insight into the organisation of the larva and lays the foundation for understanding how the somatic cells drive the behaviour and physiology necessary for infection and propagation of the stem cells inside the snail.

show abstract

Time series analysis of tegument ultrastructure of in vitro transformed miracidium to mother sporocyst of the human parasite Schistosoma mansoni

Cited by 10 publications

References 44 publications

Single-cell transcriptomics of the human parasite Schistosoma mansoni first intra-molluscan stage reveals tentative tegumental and stem-cell regulators

Single-cell transcriptomics of the human parasite Schistosoma mansoni first intra-molluscan stage reveals tentative tegumental and stem-cell regulators

Molecular detection of Schistosoma haematobium in infected Bulinus truncatus snails associated with immune response

A single-cell atlas of the miracidium larva of the human blood flukeSchistosoma mansoni: cell types, developmental pathways and tissue architecture

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