Metagenomic Analysis Reveals Variations in Gut Microbiomes of the Schistosoma mansoni-Transmitting Snails Biomphalaria straminea and Biomphalaria glabrata

Biomphalaria snails play a crucial role in the transmission of the human blood fluke Schistosoma mansoni. The gut microbiota of intermediate hosts is known to influence their physiological functions, but little is known about its composition and role in Biomphalaria snails. To gain insights into the biological characteristics of these freshwater intermediate hosts, we conducted metagenomic sequencing on Biomphalaria straminea and B. glabrata to investigate variations in their gut microbiota. This study revealed that the dominant members of the gut microbiota in B. glabrata belong to the phyla Bacteroidetes and Proteobacteria, which were also found to be the top two most abundant gut bacteria in B. straminea. We identified Firmicutes, Acidovorax and Bosea as distinctive gut microbes in B. straminea, while Aeromonas, Cloacibacterium and Chryseobacterium were found to be dependent features of the B. glabrata gut microbiota. We observed significant differences in the community structures and bacterial functions of the gut microbiota between the two host species. Notably, we found a distinctive richness of antibiotic resistance genes (ARGs) associated with various classes of antibiotics, including bacitracin, chloramphenicol, tetracycline, sulfonamide, penicillin, cephalosporin_ii and cephalosporin_i, fluoroquinolone, aminoglycoside, beta-lactam, multidrug and trimethoprim, in the digestive tracts of the snails. Furthermore, this study revealed the potential correlations between snail gut microbiota and the infection rate of S. mansoni using Spearman correlation analysis. Through metagenomic analysis, our study provided new insights into the gut microbiota of Biomphalaria snails and how it is influenced by host species, thereby enhancing our understanding of variant patterns of gut microbial communities in intermediate hosts. Our findings may contribute to future studies on gastropod–microbe interactions and may provide valuable knowledge for developing snail control strategies to combat schistosomiasis in the future.

[1]  Yaping Wang,et al.  Multi-omics reveal microbial determinants impacting the treatment outcome of antidepressants in major depressive disorder , 2023, Microbiome.

[2]  C. Ubeda,et al.  Microbiome-mediated fructose depletion restricts murine gut colonization by vancomycin-resistant Enterococcus , 2022, Nature communications.

[3]  Zhen-Yu Wang,et al.  The influence of species identity and geographic locations on gut microbiota of small rodents , 2022, Frontiers in Microbiology.

[4]  G. Iraola,et al.  Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates , 2022, Microbiome.

[5]  Benjamin W. Frable,et al.  Host biology, ecology and the environment influence microbial biomass and diversity in 101 marine fish species , 2022, Nature Communications.

[6]  Zhenchao Zhou,et al.  Roles of substrates in removing antibiotics and antibiotic resistance genes in constructed wetlands: A review. , 2022, The Science of the total environment.

[7]  T. Luo,et al.  Rumen and fecal microbiota profiles associated with immunity of young and adult goats , 2022, Frontiers in Immunology.

[8]  A. C. Madureira.  Programmed Cell Death-Ligand-1 expression in Bladder Schistosomal Squamous Cell Carcinoma – There’s room for Immune Checkpoint Blockage? , 2022, Frontiers in Immunology.

[9]  Phornpimon Tipthara,et al.  Untargeted serum metabolomic profiling for early detection of Schistosoma mekongi infection in mouse model , 2022, Frontiers in Cellular and Infection Microbiology.

[10]  S. Knopp,et al.  Fine-scale-mapping of Schistosoma haematobium infections at the school and community levels and intermediate host snail abundance in the north of Pemba Island: baseline cross-sectional survey findings before the onset of a 3-year intervention study , 2022, Parasites & Vectors.

[11]  D. Karmacharya,et al.  Antibiotic resistance genes of public health importance in livestock and humans in an informal urban community in Nepal , 2022, Scientific Reports.

[12]  Mingqing Zhang,et al.  Composition and distribution of bacterial communities and antibiotic resistance genes in fish of four mariculture systems. , 2022, Environmental pollution.

[13]  Min Wang,et al.  Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants , 2022, Microbiome.

[14]  Xi Sun,et al.  Potential Gut Microbiota Features for Non-Invasive Detection of Schistosomiasis , 2022, Frontiers in Immunology.

[15]  P. Brodin.  Immune-microbe interactions early in life: A determinant of health and disease long term , 2022, Science.

[16]  Zhongming Zheng,et al.  Responses of Gut Microbial Community Composition and Function of the Freshwater Gastropod Bellamya aeruginosa to Cyanobacterial Bloom , 2022, Frontiers in Microbiology.

[17]  Haoyu Lang,et al.  Geographical resistome profiling in the honeybee microbiome reveals resistance gene transfer conferred by mobilizable plasmids , 2022, Microbiome.

[18]  Xi Sun,et al.  Metagenome-Assembled Genomes Reveal Mechanisms of Carbohydrate and Nitrogen Metabolism of Schistosomiasis-Transmitting Vector Biomphalaria Glabrata , 2022, Microbiology spectrum.

[19]  Yichun Xie,et al.  Genome of the ramshorn snail Biomphalaria straminea—an obligate intermediate host of schistosomiasis , 2022, GigaScience.

[20]  Guo-Hua Liu,et al.  Metagenomics of the midgut microbiome of Rhipicephalus microplus from China , 2022, Parasites & vectors.

[21]  M. Jin,et al.  High-sugar, high-fat, and high-protein diets promote antibiotic resistance gene spreading in the mouse intestinal microbiota , 2022, Gut microbes.

[22]  Xi Sun,et al.  Bacterial composition of midgut and entire body of laboratory colonies of Aedes aegypti and Aedes albopictus from Southern China , 2021, Parasites & vectors.

[23]  Xi Sun,et al.  Bacillus subtilis Attenuates Hepatic and Intestinal Injuries and Modulates Gut Microbiota and Gene Expression Profiles in Mice Infected with Schistosoma japonicum , 2021, Frontiers in Cell and Developmental Biology.

[24]  J. Cryan,et al.  Microbiota-brain interactions: Moving toward mechanisms in model organisms , 2021, Neuron.

[25]  Xi Sun,et al.  Molecular Characterization of Rotifers and Their Potential Use in the Biological Control of Biomphalaria , 2021, Frontiers in Cellular and Infection Microbiology.

[26]  Phornpimon Tipthara,et al.  Metabolomics reveal alterations in arachidonic acid metabolism in Schistosoma mekongi after exposure to praziquantel , 2021, PLoS neglected tropical diseases.

[27]  N. Gunathilaka,et al.  Diversity of midgut bacteria in larvae and females of Aedes aegypti and Aedes albopictus from Gampaha District, Sri Lanka , 2021, Parasites & Vectors.

[28]  Lian Chen,et al.  Composition and diversity of gut microbiota in Pomacea canaliculata in sexes and between developmental stages , 2021, BMC Microbiology.

[29]  E. Toulza,et al.  Experimental Infection of the Biomphalaria glabrata Vector Snail by Schistosoma mansoni Parasites Drives Snail Microbiota Dysbiosis , 2021, Microorganisms.

[30]  T. W. Whon,et al.  Host habitat is the major determinant of the gut microbiome of fish , 2021, Microbiome.

[31]  E. Ota,et al.  Diagnostic test accuracy for detecting Schistosoma japonicum and S. mekongi in humans: A systematic review and meta-analysis , 2021, PLoS neglected tropical diseases.

[32]  Se Jin Song,et al.  Early-life gut dysbiosis linked to juvenile mortality in ostriches , 2020, Microbiome.

[33]  Z. Lv,et al.  Alterations of Gut Microbiome and Metabolite Profiling in Mice Infected by Schistosoma japonicum , 2020, Frontiers in Immunology.

[34]  J. Beehner,et al.  Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas , 2020, bioRxiv.

[35]  Malcolm K. Jones,et al.  Mollusk microbiota shift during Angiostrongylus cantonensis infection in the freshwater snail Biomphalaria glabrata and the terrestrial slug Phillocaulis soleiformis , 2020, Parasitology Research.

[36]  Dongjuan Yuan,et al.  The potential risk of Schistosoma mansoni transmission by the invasive freshwater snail Biomphalaria straminea in South China , 2020, PLoS neglected tropical diseases.

[37]  P. Dekumyoy,et al.  Myricetin Possesses Anthelmintic Activity and Attenuates Hepatic Fibrosis via Modulating TGFβ1 and Akt Signaling and Shifting Th1/Th2 Balance in Schistosoma japonicum-Infected Mice , 2020, Frontiers in Immunology.

[38]  G. Gao,et al.  Integrated metagenomic and metatranscriptomic profiling reveals differentially expressed resistomes in human, chicken, and pig gut microbiomes. , 2020, Environment international.

[39]  P. Engel,et al.  The gut microbiota - brain axis of insects. , 2020, Current opinion in insect science.

[40]  F. Brayner,et al.  Investigation of defense response and immune priming in Biomphalaria glabrata and Biomphalaria straminea, two species with different susceptibility to Schistosoma mansoni , 2019, Parasitology Research.

[41]  Yi Zhang,et al.  Spatial structure of the microbiome in the gut of Pomacea canaliculata , 2019, BMC Microbiology.

[42]  I. Mizrahi,et al.  Core gut microbial communities are maintained by beneficial interactions and strain variability in fish , 2019, Nature Microbiology.

[43]  Y. Li,et al.  Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria , 2019, Microbiome.

[44]  G. Plastow,et al.  Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle , 2019, Microbiome.

[45]  Richard S. Barnett.  Schistosomiasis , 2018, The Lancet.

[46]  F. Cicala,et al.  Structure, dynamics and predicted functional role of the gut microbiota of the blue (Haliotis fulgens) and yellow (H. corrugata) abalone from Baja California Sur, Mexico , 2018, PeerJ.

[47]  Bin Chen,et al.  Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure , 2018, Microbiome.

[48]  Xi Sun,et al.  Chi3l3: a potential key orchestrator of eosinophil recruitment in meningitis induced by Angiostrongylus cantonensis , 2018, Journal of Neuroinflammation.

[49]  P. Agre,et al.  Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria , 2017, Science.

[50]  Zhong-dao Wu,et al.  Parasitology should not be abandoned: data from outpatient parasitological testing in Guangdong, China , 2017, Infectious Diseases of Poverty.

[51]  A. Franke,et al.  Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis , 2017, Nature Medicine.

[52]  Min Zhao,et al.  Whole genome analysis of a schistosomiasis-transmitting freshwater snail , 2017, Nature Communications.

[53]  Zheng Minghui,et al.  Study on the tolerance and adaptation of rats to Angiostrongylus cantonensis infection , 2017, Parasitology Research.

[54]  You-sheng Liang,et al.  Evaluating the risk of Schistosoma mansoni transmission in mainland China , 2016, Parasitology Research.

[55]  F. Zhao,et al.  Convergent Evolution of Rumen Microbiomes in High-Altitude Mammals , 2016, Current Biology.

[56]  M. N. Rocha,et al.  Wolbachia Blocks Currently Circulating Zika Virus Isolates in Brazilian Aedes aegypti Mosquitoes , 2016, Cell host & microbe.

[57]  Nicola Zamboni,et al.  Gut Microbiota Orchestrates Energy Homeostasis during Cold , 2015, Cell.

[58]  B. Bohannan,et al.  The composition of the zebrafish intestinal microbial community varies across development , 2015, The ISME Journal.

[59]  W. de Souza,et al.  Isolation of aerobic cultivable cellulolytic bacteria from different regions of the gastrointestinal tract of giant land snail Achatina fulica , 2015, Front. Microbiol..

[60]  Johan Bengtsson-Palme,et al.  Antibiotic resistance genes in the environment: prioritizing risks , 2015, Nature Reviews Microbiology.

[61]  D. Huson,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[62]  W. Ittiprasert,et al.  Differential Spatial Repositioning of Activated Genes in Biomphalaria glabrata Snails Infected with Schistosoma mansoni , 2014, PLoS neglected tropical diseases.

[63]  C. King,et al.  Human schistosomiasis , 2014, The Lancet.

[64]  J. Pointier,et al.  Comparative evaluation of Schistosoma mansoni, Schistosoma intercalatum, and Schistosoma haematobium alkaline phosphatase antigenicity by the alkaline phosphatase immunoassay (APIA) , 2014, Parasitology Research.

[65]  Jian Wang,et al.  Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota , 2013, Nature Communications.

[66]  K. Rudi,et al.  De novo Semi-alignment of 16S rRNA Gene Sequences for Deep Phylogenetic Characterization of Next Generation Sequencing Data , 2013, Microbes and environments.

[67]  V. Tremaroli,et al.  Functional interactions between the gut microbiota and host metabolism , 2012, Nature.

[68]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[69]  Brian J. Bennett,et al.  Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease , 2011, Nature.

[70]  G. Dimopoulos,et al.  Implication of the Mosquito Midgut Microbiota in the Defense against Malaria Parasites , 2009, PLoS pathogens.

[71]  T. Takagi,et al.  MetaGene: prokaryotic gene finding from environmental genome shotgun sequences , 2006, Nucleic acids research.

[72]  Z. Qin,et al.  Intestinal microbiome profiles in Oncomelania hupensis in mainland China. , 2019, Acta tropica.

[73]  S. Thiengo,et al.  Susceptibility of Biomphalaria straminea (Dunker, 1848) from Serra da Mesa Dam, Goiás, Brazil to infection with three strains of Schistosoma mansoni Sambon, 1907. , 2002, Memorias do Instituto Oswaldo Cruz.

[74]  Heng Li,et al.  BIOINFORMATICS ORIGINAL PAPER , 2022 .