Morphological and genomic characterisation of the Schistosoma hybrid infecting humans in Europe reveals admixture between Schistosoma haematobium and Schistosoma bovis

Kincaid-Smith, Julien; Tracey, Alan S.; Augusto, Ronaldo de Carvalho; Bulla, Ingo; Holroyd, Nancy; Rognon, Anne; Rey, Olivier; Chaparro, Cristian; Oleaga, Ana; Mas‐Coma, Santiago; Allienne, Jean‐François; Grunau, Christoph; Berriman, Matthew; Boissier, Jérôme; Toulza, Ève

doi:10.1371/journal.pntd.0010062

Cited by 32 publications

(28 citation statements)

References 62 publications

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“…The strain was installed in the lab in 1984 after a generous gift of Pr D. Rollinson (British Museum, London). The S. haematobium-bovis hybrid strain was recovered from eggs isolated from a patient infected in the Cavu River, Corsica, France [32]. Since 2014 this strain is maintained in golden hamster as definitive host and Bulinus truncatus (Corsican strain) as intermediate host.…”

Section: Methodsmentioning

confidence: 99%

MALDI-TOF : A new tool for the identification of Schistosoma cercariae and detection of hybrids

Huguenin

Kincaid-Smith

Depaquit

et al. 2022

Preprint

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Schistosomiasis is a neglected water-born parasitic disease caused by Schistosoma affecting more than 200 million people. Introgressive hybridization is common among these parasites and raises issues concerning their zoonotic transmission. Morphological identification of Schistosoma cercariae is difficult and does not permit hybrids detection. Our objective was to assess the performance of MALDI-TOF for the specific identification of cercariae in human and non-human Schistosoma and for the detection of hybridization between S. bovis and S. haematobium Spectra were collected from laboratory reared molluscs infested with strains of S. haematobium , S. mansoni , S . bovis , S. rodhaini and S. bovis x S. haematobium natural (Corsican hybrid) and artificial hybrids. Cluster analysis showed a clear separation between S. haematobium , S. bovis , S. mansoni and S. rodhaini. Corsican hybrids are classified with those of the parental strain of S. haematobium whereas other hybrids formed a distinct cluster. In blind test analysis the developed MALDI-TOF spectral database permits identification of Schistosoma cercariae with high accuracy (94%) and good specificity ( S. bovis : 99.59%, S. haematobium 99.56%, S. mansoni and S. rodhaini : 100%). Most misidentifications were between S. haematobium and the Corsican hybrids. The use of machine learning permits to improve the discrimination between these last two taxa, with accuracy, F1 score and Sensitivity/Specificity > 97%. In multivariate analysis the factors associated with obtaining a valid identification score (> 1.7) were absence of ethanol preservation (p < 0.001) and a number of 2-3 cercariae deposited per well (p < 0.001). Also spectra acquired from S. mansoni cercariae are more likely to obtain a valid identification score than those acquired from S. haematobium (p<0.001). MALDI-TOF is a reliable technique for high-throughput identification of Schistosoma cercariae of medical and veterinary importance and could be useful for field survey in endemic areas.

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Section: Methodsmentioning

confidence: 99%

MALDI-TOF : A new tool for the identification of Schistosoma cercariae and detection of hybrids

Huguenin

Kincaid-Smith

Depaquit

et al. 2022

Preprint

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“…Three cercariae from each infected snail were individually captured for molecular sexing and each snail was separated into a plastic cup and fed ad libitum. Molecular sexing of S. mansoni and S. bovis cercariae was performed according to [14,28] respectively (see Supplementary Materials for detailed molecular biology protocols [28,29]). The snails were finally separated into four distinct tanks according to sex and species of cercariae.…”

Section: Experimental Protocol 231 Snail Infection and Obtention Of U...mentioning

confidence: 99%

“…These experimental studies have evidenced either random mating or a preponderance of homo-specific pairing according to the phylogenetic distance of the interacting species [13]. When closely related species interact such as S. haematobium × S. bovis [14], S. bovis × S. curassoni [15], S. haematobium × S. intercalatum [16] or S. intercalatum × S. guineensis [17] the pairing is random. All these latter species are included in the same monophyletic S. haematobium group [3].…”

Section: Introductionmentioning

confidence: 99%

“…At the opposite when the species belong to two different evolutionary lineages mate preference is observed as evidenced for S. mansoni × S. intercalatum crosses [18]. The genetic background of the resulting progeny may also depend on the phylogenetic distance between the interacting species, ranging from parthenogenetic individuals [19] to substantial genomic introgression [14,20,21]. One visible consequence of such genetic signatures may be observed at the parasites' life history trait level, and in particular for the parasite-mollusc compatibility.…”

Section: Introductionmentioning

confidence: 99%

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Mating Interactions between Schistosoma bovis and S. mansoni and Compatibility of Their F1 Progeny with Biomphalaria glabrata and Bulinus truncatus

et al. 2022

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Contrary to the majority of other Trematoda, Schistosoma species are gonochoric. Consequently, in endemic areas where several schistosome species overlap and can co-infect the same definitive host, there may be frequent opportunities for interspecific pairing. Our experimental study provides novel insight on the pairing behavior between Schistosoma bovis and S. mansoni in mixed infections in mice. We used six mate choice experiments to assess mating interactions between the two schistosome species. We show that mating between the two Schistosoma species is not random and that S. mansoni exhibits greater mate recognition compared to S. bovis. We also performed reciprocal crosses (male S. mansoni × female S. bovis) and (female S. mansoni × male S. bovis) that produce active swimming miracidia. These miracidia were genotyped by ITS2 sequencing and proposed for mollusc infection. Molecular analyses show that all the miracidia are parthenogenetically produced (i.e., their harbor the mother ITS2 genotype) and as a consequence can only infect the mollusc of the maternal species. Offspring produced by male S. mansoni × female S. bovis pairing can only infect Bulinus truncatus whereas offspring produced by female S. mansoni × male S. bovis can only infect Biomphalaria glabrata snails. Evolutionary and epidemiological consequences are discussed.

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“…For instance, Boissier et al reported an outbreak of urogenital schistosomiasis in Europe, in Corsica Island (France), produced by parasites imported from Senegal, and alerted the potential risk of schistosomiasis outbreaks in other European areas [7]. European schistosomes had previously been identified as hybrids between the livestock-and the human-infective species Schistosoma bovis and Schistosoma haematobium, respectively [8,9]. Recently, after an in-depth clinical and epidemiological study of several cases, evidence of autochthonous transmission of urogenital schistosomiasis in Almería (Spain) was demonstrated [10], and new cases of acute schistosomiasis have been reported in people from Antwerp, Belgium after staying in South Africa [11].…”

Section: Introductionmentioning

confidence: 99%

Research on Schistosomiasis in the Era of the COVID-19 Pandemic: A Bibliometric Analysis

Sanchez-Marquès

Mas‐Coma

Salas-Coronas

et al. 2022

IJERPH

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The objectives of this work are to check whether the COVID-19 pandemic affected the research on schistosomiasis, to provide an insight into the most productive countries and journals and the most cited publications, and to analyse any association between the total publications of countries and a set of socio-economic and demographic factors. Based on PRISMA methodology, we used the Scopus database to search for articles published between 1 January 2020 and 26 March 2022. VOSviewer was used to generate the co-authorship and the co-occurrence networks, and Spearman’s rank correlation was applied to study associations. A total of 1988 articles were included in the study. Although we found that the year-wise distribution of publications suggests no impact on schistosomiasis research, many resources have been devoted to research on COVID-19, and the Global Schistosomiasis Alliance revealed the main activities for eradication of schistosomiasis had been affected. The most productive country was the United States of America. The articles were mainly published in PLoS Neglected Tropical Diseases. The most prolific funding institution was the National Natural Science Foundation of China. The total publications per country were significantly correlated with population, GERD, and researchers per million inhabitants, but not with GDP per capita and MPM.

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Morphological and genomic characterisation of the Schistosoma hybrid infecting humans in Europe reveals admixture between Schistosoma haematobium and Schistosoma bovis

Cited by 32 publications

References 62 publications

MALDI-TOF : A new tool for the identification of Schistosoma cercariae and detection of hybrids

MALDI-TOF : A new tool for the identification of Schistosoma cercariae and detection of hybrids

Mating Interactions between Schistosoma bovis and S. mansoni and Compatibility of Their F1 Progeny with Biomphalaria glabrata and Bulinus truncatus

Research on Schistosomiasis in the Era of the COVID-19 Pandemic: A Bibliometric Analysis

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