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The potential risk of Schistosoma mansoni transmission by the invasive freshwater snail Biomphalaria straminea in South China.

ABSTRACT: Schistosomes infect more than 200 million people worldwide, and globally, over 700 million people are at risk of infection. The snail Biomphalaria straminea, as one of the intermediate hosts of Schistosoma mansoni, consecutively invaded Hong Kong in 1973, raising great concern in China. In this study, a malacological survey was conducted over a period of four years, and investigations were performed on the mechanism of susceptibility of B. straminea to S. mansoni. B. straminea was investigated in China from 2014 to 2018. Out of 185 investigated sites, 61 were positive for stages of black B. straminea (BBS), which shows pigmented spots. Twenty of the 61 sites were positive for red B. straminea (RBS), which is partially albino and red colored. Phylogenetic analyses based on cox1 and 18S rRNA sequences demonstrated that both phenotypes were clustered with Brazilian strains. No S. mansoni infections were detected in field-collected snail. However, in laboratory experiments, 4.17% of RBS were susceptible to a Puerto Rican strain of S. mansoni, while BBS was not susceptible. The highest susceptibility rate (70.83%) was observed in the F2 generation of RBS in lab. The density of RBS has increased from south to north and from west to east in Guangdong since 2014. Five tyrosinase tyrosine metabolism genes were upregulated in BBS. Transcriptome comparisons of RBS and BBS showed that ficolin, C1q, MASP-like, and membrane attack complex (MAC)/perforin models of the complement system were significantly upregulated in BBS. Our study demonstrated that B. straminea is widely distributed in Hong Kong and Guangdong Province, which is expanding northwards very rapidly as a consequence of its adaptation to local environments. Our results suggest that B. straminea from South China is susceptible to S. mansoni, implying the high potential for S. mansoni transmission and increased S. mansoni infection risk in China.

SUBMITTER: Lin D

PROVIDER: S-EPMC7302743 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSchistosomiasis is a snail-borne parasitic disease and is endemic in many tropical and subtropical countries. Biomphalaria straminea, an intermediate host for Schistosoma mansoni, is native to the southeastern part of South America and has established in other regions of South America, Central America and southern China during the last decades. S. mansoni is endemic in Africa, the Middle East, South America and the Caribbean. Knowledge of the potential global distribution of this snail is essential for risk assessment, monitoring, disease prevention and control.Methods and findingsA comprehensive database of cross-continental occurrence for B. straminea was compiled to construct ecological models. We used several approaches to investigate the distribution of B. straminea, including direct comparison of climatic conditions, principal component analysis and niche overlap analyses to detect niche shifts. We also investigated the impacts of bioclimatic and human factors, and then used the bioclimatic and footprint layers to predict the potential distribution of B. straminea at global scale. We detected niche shifts accompanying the invasions of B. straminea in the Americas and China. The introduced populations had enlarged its habitats to subtropical regions where annual mean temperature is relatively low. Annual mean temperature, isothermality and temperature seasonality were identified as most important climatic features for the occurrence of B. straminea. Additionally, human factors improved the model prediction (P<0.001). Our model showed that under current climate conditions the snail should mostly be confined to the tropic and subtropic regions, including South America, Central America, Sub-Saharan Africa and Southeast Asia.ConclusionsOur results confirmed that niche shifts took place in the invasions of B. straminea, in which bioclimatic and human factors played an important role. Our model predicted the global distribution of B. straminea based on habitat suitability, which would help for prioritizing monitoring and management efforts for B. straminea control in the context of ongoing climate change and human disturbances.

Project description:BackgroundBiomphalaria pfeifferi is highly compatible with the widespread human-infecting blood fluke Schistosoma mansoni and transmits more cases of this parasite to people than any other snail species. For these reasons, B. pfeifferi is the world's most important vector snail for S. mansoni, yet we know relatively little at the molecular level regarding the interactions between B. pfeifferi and S. mansoni from early-stage sporocyst transformation to the development of cercariae.Methodology/principal findingsWe sought to capture a portrait of the response of B. pfeifferi to S. mansoni as it occurs in nature by undertaking Illumina dual RNA-Seq on uninfected control B. pfeifferi and three intramolluscan developmental stages (1- and 3-days post infection and patent, cercariae-producing infections) using field-derived west Kenyan specimens. A high-quality, well-annotated de novo B. pfeifferi transcriptome was assembled from over a half billion non-S. mansoni paired-end reads. Reads associated with potential symbionts were noted. Some infected snails yielded fewer normalized S. mansoni reads and showed different patterns of transcriptional response than others, an indication that the ability of field-derived snails to support and respond to infection is variable. Alterations in transcripts associated with reproduction were noted, including for the oviposition-related hormone ovipostatin and enzymes involved in metabolism of bioactive amines like dopamine or serotonin. Shedding snails exhibited responses consistent with the need for tissue repair. Both generalized stress and immune factors immune factors (VIgLs, PGRPs, BGBPs, complement C1q-like, chitinases) exhibited complex transcriptional responses in this compatible host-parasite system.SignificanceThis study provides for the first time a large sequence data set to help in interpreting the important vector role of the neglected snail B. pfeifferi in transmission of S. mansoni, including with an emphasis on more natural, field-derived specimens. We have identified B. pfeifferi targets particularly responsive during infection that enable further dissection of the functional role of these candidate molecules.

Project description:BackgroundSchistosomiasis is a common parasitic disease designated as a neglected tropical disease by the World Health Organization. Schistosomiasis mansoni is a form of the disease that is caused by the digenean trematode Schistosoma mansoni, transmitted through Biomphalaria spp. as an intermediate host. Biomphalaria was introduced to Hong Kong, China in aquatic plants shipments coming from Brazil and the snail rapidly established its habitats in southern China. Earlier studies of Biomphalaria spp. introduced to southern China identified the snails as Biomphalaria straminea, one of the susceptible species implicated in S. mansoni transmission in South America. However, recent molecular investigations also indicated the presence of another South American species, B. kuhniana, which is refractory to infection. As such, it is important to identify accurately the species currently distributed in southern China, especially with emerging reports of active S. mansoni infections in Chinese workers returning from Africa.MethodsWe combined morphological and molecular taxonomy tools to precisely identify Biomphalaria spp. distributed in Guangdong Province, southern China. In order to clearly understand the molecular profile of the species, we constructed a phylogeny using mtDNA data (COI and 16S rRNA sequences) from six populations of Biomphalaria spp. from Shenzhen City in Guangdong Province. In addition, we examined the external morphology of the shell and internal anatomy of the reproductive organs.ResultsBoth morphological and molecular evidences indicated a close affinity between Biomphalaria spp. populations from Guangdong and B. straminea from Brazil. The shell morphology was roughly identical in all the populations collected with rounded whorls on one side and subangulated on the other, a smooth periphery, an egg-shaped aperture bowed to one side, and a deep umbilicus. The shape and number of prostate diverticula (ranged from 11.67 to 17.67) in Guangdong populations supports its close affinity to B. straminea rather than B. kuhniana. Molecular analysis did not conflict with morphological analysis. Little genetic differentiation was observed within Biomphalaria populations collected. Phylogenetic analysis of COI and 16S rRNA haplotypes from snails collected and B. straminea sequences from Brazil and China using Bayesian inference revealed that Guangdong populations were clustered in one clade with B. straminea from Hong Kong of China and B. straminea from Brazil indicating their close affinity to each other.ConclusionsData obtained in the current study clearly show that the populations of Biomphalaria spp. investigated are B. straminea, and we assume that those snails were either introduced via passive dispersal from Hong Kong of China or as a result of multiple introduction routes from Brazil.

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The potential risk of Schistosoma mansoni transmission by the invasive freshwater snail Biomphalaria straminea in South China.

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