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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., Author summary Biomphalaria straminea is an important intermediate host for the blood fluke Schistosoma mansoni. B. straminea has spread in Hong Kong and in mainland China since 1973. However, whether resident snails can transmit intestinal schistosomiasis caused by S. mansoni remains unclear. Our results revealed that different types of B. straminea are widespread in cities such as Hong Kong, Shenzhen, Dongguan, Huizhou and Puning and that the distribution of the species has shifted northwards. The most important finding was that one of the phenotypes (red phenotype of B. straminea, RBS), which is highly susceptible to S. mansoni, has spread into the city of Shenzhen since 2016. The density of RBS in Guangdong Province has increased rapidly since 2014, especially since 2016. Transcriptome analysis showed that the high expression levels of ficolin, C1q, MASP-like, and membrane attack complex (MAC)/perforin models of the complement system might be associated with the mechanism of susceptibility. Our study suggested that B. straminea is susceptible to S. mansoni, implying a high potential risk of S. mansoni transmission in South China. More attention should be paid to the potential transmission of S. mansoni, and control measures should be established to prevent the spread of this snail in South China.