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Genetic structure inferred from mitochondrial 12S ribosomal RNA sequence of Oncomelania quadrasi, the intermediate snail host of Schistosoma japonicum in the Philippines.

ABSTRACT: Species and subspecies of the Oncomelania hupensis species complex are recognized as intermediate hosts of Schistosoma japonicum. Of these species and subspecies, O. quadrasi is distributed throughout the Philippines. This study used 12S ribosomal RNA sequences to explore the genetic structure of O. quadrasi populations in the Philippines. Three subspecies, O. h. hupensis, O. h. formosana, and O. h. chiui of this group were also examined. The phylogenetic tree and haplotypes network showed that O. quadrasi separated from the subspecies. Ten O. quadrasi haplotypes (Oq1-Oq10) clustered in relation to their geographic origin. Genetic differentiation (FST) and estimated gene flow (Nm) among populations showed significant differences, ranging from 0.556-1.000 to 0.00-0.74, respectively. Genetic differences among groups (FCT = 0.466), populations within a group (FSC = 0.727), and populations (FST = 0.854) were observed. These results indicate that the O. quadrasi populations in the Philippines have a substructure associated with their geographic origin.

SUBMITTER: Saijuntha W

PROVIDER: S-EPMC4047743 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Genetic structure inferred from mitochondrial 12S ribosomal RNA sequence of Oncomelania quadrasi, the intermediate snail host of Schistosoma japonicum in the Philippines.

Saijuntha Weerachai W Jarilla Blanca B Leonardo Alvin K AK Sunico Louie S LS Leonardo Lydia R LR Andrews Ross H RH Sithithaworn Paiboon P Petney Trevor N TN Kirinoki Masashi M Kato-Hayashi Naoko N Kikuchi Mihoko M Chigusa Yuichi Y Agatsuma Takeshi T

The American journal of tropical medicine and hygiene 20140331 6

Species and subspecies of the Oncomelania hupensis species complex are recognized as intermediate hosts of Schistosoma japonicum. Of these species and subspecies, O. quadrasi is distributed throughout the Philippines. This study used 12S ribosomal RNA sequences to explore the genetic structure of O. quadrasi populations in the Philippines. Three subspecies, O. h. hupensis, O. h. formosana, and O. h. chiui of this group were also examined. The phylogenetic tree and haplotypes network showed that ...[more]

PMID: 24686739

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Project description:BACKGROUND:Schistosoma japonicum causes major public health problems in China and the Philippines; this parasite, which is transmitted by freshwater snails of the species Oncomelania hupensis, causes the disease intestinal schistosomiasis in humans and cattle. Researchers working on Schistosoma in Africa have described the relationship between the parasites and their snail intermediate hosts as coevolved or even as an evolutionary arms race. In the present study this hypothesis of coevolution is evaluated for S. japonicum and O. hupensis. The origins and radiation of the snails and the parasite across China, and the taxonomic validity of the sub-species of O. hupensis, are also assessed. METHODOLOGY/PRINCIPAL FINDINGS:The findings provide no evidence for coevolution between S. japonicum and O. hupensis, and the phylogeographical analysis suggests a heterochronous radiation of the parasites and snails in response to different palaeogeographical and climatic triggers. The results are consistent with a hypothesis of East to West colonisation of China by Oncomelania with a re-invasion of Japan by O. hupensis from China. The Taiwan population of S. japonicum appears to be recently established in comparison with mainland Chinese populations. CONCLUSIONS/SIGNIFICANCE:The snail and parasite populations of the western mountain region of China (Yunnan and Sichuan) appear to have been isolated from Southeast Asian populations since the Pleistocene; this has implications for road and rail links being constructed in the region, which will breach biogeographical barriers between China and Southeast Asia. The results also have implications for the spread of S. japonicum. In the absence of coevolution, the parasite may more readily colonise new snail populations to which it is not locally adapted, or even new intermediate host species; this can facilitate its dispersal into new areas. Additional work is required to assess further the risk of spread of S. japonicum.

Project description:BACKGROUND: Oncomelania hupensis is the unique intermediate host of Schistosoma japonicum, which causes schistosomiasis endemic in the Far East, and especially in mainland China. O. hupensis largely determines the parasite's geographical range. How O. hupensis's genetic diversity is distributed geographically in mainland China has never been well examined with DNA sequence data. METHODOLOGY/PRINCIPAL FINDINGS: In this study we investigate the genetic variation among O. hupensis from different geographical origins using the combined complete internal transcribed spacer 1 (ITS1) and ITS2 regions of nuclear ribosomal DNA. 165 O. hupensis isolates were obtained in 29 localities from 7 provinces across mainland China: lake/marshland and hill regions in Anhui, Hubei, Hunan, Jiangxi and Jiangsu provinces, located along the middle and lower reaches of Yangtze River, and mountainous regions in Sichuan and Yunnan provinces. Phylogenetic and haplotype network analyses showed distinct genetic diversity and no shared haplotypes between populations from lake/marshland regions of the middle and lower reaches of the Yangtze River and populations from mountainous regions of Sichuan and Yunnan provinces. The genetic distance between these two groups is up to 0.81 based on Fst, and branch time was estimated as 2-6 Ma. As revealed in the phylogenetic tree, snails from Sichuan and Yunnan provinces were also clustered separately. Geographical separation appears to be an important factor accounting for the diversification of the two groups of O. hupensis in mainland China, and probably for the separate clades between snails from Sichuan and Yunnan provinces. In lake/marshland and hill regions along the middle and lower reaches of the Yangtze River, three clades were identified in the phylogenetic tree, but without any obvious clustering of snails from different provinces. CONCLUSIONS: O. hupensis in mainland China may have considerable genetic diversity, and a more complex population structure than expected. It will be of significant importance to consider the genetic diversity of O. hupensis when assessing co-evolutionary interactions with S. japonicum.

Project description:In recent years, the prevalence and infection intensity of Schistosoma japonicum in endemic areas of the Philippines have significantly decreased due to yearly population-based treatment strategies, yet transmission rates remain high and uninterrupted. An important indicator of active disease transmission is the presence of Schistosoma japonicum and its snail intermediate host Oncomelania hupensis quadrasi in freshwater habitats. In this study, we sought to apply a species-specific real-time PCR (qPCR) assay for the detection of S. japonicum and O. hupensis quadrasi in freshwater samples using environmental DNA approach that can complement the commonly utilized malacological survey in determining potential transmission foci in order to have a more effective snail surveillance strategy for schistosomiasis japonica in endemic areas. The newly developed assay was specific to S. japonicum and O. hupensis quadrasi with no amplification detected against non-target trematode Fasciola spp. and snails such as Lymnaea spp., Pomacea canaliculata, and Melanoides spp. that typically co-exist in the same environment. The assay effectiveness was determined using 19 environmental water samples collected from Northern Samar (N = 5 sites), Leyte (N = 11 sites) and Compostela Valley (N = 3 sites) and compared to malacological survey for determining O. hupensis quadrasi snail colonies and snail crushing to visualize S. japonicum cercariae. TaqMan qPCR targeting a short fragment of the cytochrome c oxidase subunit 1 (cox1) gene was positive for S. japonicum in 9 sites, for O. hupensis quadrasi in 9 sites, and for both S. japonicum and O. hupensis quadrasi in 5 sampling sites. Moreover, it was able to detect O. hupensis quadrasi in 3 out of 12 sites found negative and 6 out of 7 sites found positive through malacological survey, and in 4 of the 5 snail sites positive for snails with cercariae. Overall, this method can complement malacological surveys for monitoring of schistosomes in endemic areas of the Philippines, especially those with high risk of human infection.

Project description:Background:The freshwater snail Oncomelania hupensis is the obligate intermediate host for Schistosoma japonicum in China. Transcriptomic examination of snail-schistosome interactions can provide valuable information of host response at physiological and immune levels. Methods:To investigate S. japonicum-induced changes in O. hupensis gene expression, we utilized high-throughput sequencing to identify transcripts that were differentially expressed between infected snails and their uninfected controls at two key time-point, Day 7 and Day 30 after challenge. Time-series transcriptomic profiles were analyzed using R package DESeq 2, followed by GO, KEGG and (weighted gene correlation network analysis) WGCNA analysis to elucidate and identify important molecular mechanism, and subsequently understand host-parasite relationship. The identified unigenes was verified by bioinformatics and real-time PCR. Possible adaptation molecular mechanisms of O. hupensis to S. japonicum challenge were proposed. Results:Transcriptomic analyses of O. hupensis by S. japonicum invasion yielded billion reads including 92,144 annotated transcripts. Over 5000 differentially expressed genes (DEGs) were identified by pairwise comparisons of infected libraries from two time points to uninfected libraries in O. hupensis. In total, 6032 gene ontology terms and 149 KEGG pathways were enriched. After the snails were infected with S. japonicum on Day 7 and Day 30, DEGs were shown to be involved in many key processes associated with biological regulation and innate immunity pathways. Gene expression patterns differed after exposure to S. japonicum. Using WGCNA, 16 modules were identified. Module-trait analysis identified that a module involved in RNA binding, ribosome, translation, mRNA processing, and structural constituent of ribosome were strongly associated with S. japonicum invasion. Many of the genes from enriched KEGG pathways were involved in lysosome, spliceosome and ribosome, indicating that S. japonicum invasion may activate the regulation of ribosomes and immune response to infection in O. hupensis. Conclusions:Our analysis provided a temporally dynamic gene expression pattern of O. hupensis by S. japonicum invasion. The identification of gene candidates serves as a foundation for future investigations of S. japonicum infection. Additionally, major DEGs expression patterns and putative key regulatory pathways would provide useful information to construct gene regulatory networks between host-parasite crosstalk.

Project description:BackgroundWhile the dispersal of hosts and vectors-through active or passive movement-is known to facilitate the spread and re-emergence of certain infectious diseases, little is known about the movement ecology of Oncomelania spp., intermediate snail host of the parasite Schistosoma japonicum, and its consequences for the spread of schistosomiasis in East and Southeast Asia. In China, despite intense control programs aimed at preventing schistosomiasis transmission, there is evidence in recent years of re-emergence and persistence of infection in some areas, as well as an increase in the spatial extent of the snail host. A quantitative understanding of the dispersal characteristics of the intermediate host can provide new insights into the spatial dynamics of transmission, and can assist public health officials in limiting the geographic spread of infection.Methodology/principal findingsOncomelania hupensis robertsoni snails (n = 833) were sampled from 29 sites in Sichuan, China, genotyped, and analyzed using Bayesian assignment to estimate the rate of recent snail migration across sites. Landscape connectivity between each site pair was estimated using the geographic distance distributions derived from nine environmental models: Euclidean, topography, incline, wetness, land use, watershed, stream use, streams and channels, and stream velocity. Among sites, 14.4% to 32.8% of sampled snails were identified as recent migrants, with 20 sites comprising >20% migrants. Migration rates were generally low between sites, but at 8 sites, over 10% of the overall host population originated from one proximal site. Greater landscape connectivity was significantly associated with increased odds of migration, with the minimum path distance (as opposed to median or first quartile) emerging as the strongest predictor across all environmental models. Models accounting for land use explained the largest proportion of the variance in migration rates between sites. A greater number of irrigation channels leading into a site was associated with an increase in the site's propensity to both attract and retain snails.Conclusions/significanceOur findings have important implications for controlling the geographic spread of schistosomiasis in China, through improved understanding of the dispersal capacity of the parasite's intermediate host.

Project description:BackgroundOncomelania hupensis is only intermediate snail host of Schistosoma japonicum, and distribution of O. hupensis is an important indicator for the surveillance of schistosomiasis. This study explored the feasibility of a random forest algorithm weighted by spatial distance for risk prediction of schistosomiasis distribution in the Yangtze River Basin in China, with the aim to produce an improved precision reference for the national schistosomiasis control programme by reducing the number of snail survey sites without losing predictive accuracy.MethodsThe snail presence and absence records were collected from Anhui, Hunan, Hubei, Jiangxi and Jiangsu provinces in 2018. A machine learning of random forest algorithm based on a set of environmental and climatic variables was developed to predict the breeding sites of the O. hupensis intermediated snail host of S. japonicum. Different spatial sizes of a hexagonal grid system were compared to estimate the need for required snail sampling sites. The predictive accuracy related to geographic distances between snail sampling sites was estimated by calculating Kappa and the area under the curve (AUC).ResultsThe highest accuracy (AUC = 0.889 and Kappa = 0.618) was achieved at the 5 km distance weight. The five factors with the strongest correlation to O. hupensis infestation probability were: (1) distance to lake (48.9%), (2) distance to river (36.6%), (3) isothermality (29.5%), (4) mean daily difference in temperature (28.1%), and (5) altitude (26.0%). The risk map showed that areas characterized by snail infestation were mainly located along the Yangtze River, with the highest probability in the dividing, slow-flowing river arms in the middle and lower reaches of the Yangtze River in Anhui, followed by areas near the shores of China's two main lakes, the Dongting Lake in Hunan and Hubei and the Poyang Lake in Jiangxi.ConclusionsApplying the machine learning of random forest algorithm made it feasible to precisely predict snail infestation probability, an approach that could improve the sensitivity of the Chinese schistosome surveillance system. Redesign of the snail surveillance system by spatial bias correction of O. hupensis infestation in the Yangtze River Basin to reduce the number of sites required to investigate from 2369 to 1747.

Dataset Information

Genetic structure inferred from mitochondrial 12S ribosomal RNA sequence of Oncomelania quadrasi, the intermediate snail host of Schistosoma japonicum in the Philippines.

Publications

Genetic structure inferred from mitochondrial 12S ribosomal RNA sequence of Oncomelania quadrasi, the intermediate snail host of Schistosoma japonicum in the Philippines.

Similar Datasets

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