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      Gut microbiota in parasite-transmitting gastropods

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          Abstract

          Background

          Gastropoda, the largest class within the phylum Mollusca, houses diverse gut microbiota, and some gastropods serve as intermediate hosts for parasites. Studies have revealed that gut bacteria in gastropods are associated with various biological aspects, such as growth, immunity and host–parasite interactions. Here, we summarize our current knowledge of gastropod gut microbiomes and highlight future research priorities and perspectives.

          Methods

          A literature search was undertaken using PubMed, Web of Science and CNKI for the articles on the gut microbiota of gastropods until December 31, 2022. We retrieved a total of 166 articles and identified 73 eligible articles for inclusion in this review based on the inclusion and exclusion criteria.

          Results

          Our analysis encompassed freshwater, seawater and land snails, with a specific focus on parasite-transmitting gastropods. We found that most studies on gastropod gut microbiota have primarily utilized 16S rRNA gene sequencing to analyze microbial composition, rather than employing metagenomic, metatranscriptomic, or metabolomic approaches. This comprehensive review provided an overview of the parasites carried by snail species in the context of gut microbiota studies. We presented the gut microbial trends, a comprehensive summary of the diversity and composition, influencing factors, and potential functions of gastropod gut microbiota. Additionally, we discussed the potential applications, research gaps and future perspectives of gut microbiomes in parasite-transmitting gastropods. Furthermore, several strategies for enhancing our comprehension of gut microbiomes in snails were also discussed.

          Conclusions

          This review comprehensively summarizes the current knowledge on the composition, potential function, influencing factors, potential applications, limitations, and challenges of gut microbiomes in gastropods, with a specific emphasis on parasite-transmitting gastropods. These findings provide important insights for future studies aiming to understand the potential role of gastropod gut microbiota in controlling snail populations and snail-borne diseases.

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          Supplementary Information

          The online version contains supplementary material available at 10.1186/s40249-023-01159-z.

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          Most cited references162

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          Diversity, stability and resilience of the human gut microbiota.

          Trillions of microbes inhabit the human intestine, forming a complex ecological community that influences normal physiology and susceptibility to disease through its collective metabolic activities and host interactions. Understanding the factors that underlie changes in the composition and function of the gut microbiota will aid in the design of therapies that target it. This goal is formidable. The gut microbiota is immensely diverse, varies between individuals and can fluctuate over time - especially during disease and early development. Viewing the microbiota from an ecological perspective could provide insight into how to promote health by targeting this microbial community in clinical treatments.
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            The Human Intestinal Microbiome in Health and Disease.

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              • Article: not found

              A microbial symbiosis factor prevents intestinal inflammatory disease.

              Humans are colonized by multitudes of commensal organisms representing members of five of the six kingdoms of life; however, our gastrointestinal tract provides residence to both beneficial and potentially pathogenic microorganisms. Imbalances in the composition of the bacterial microbiota, known as dysbiosis, are postulated to be a major factor in human disorders such as inflammatory bowel disease. We report here that the prominent human symbiont Bacteroides fragilis protects animals from experimental colitis induced by Helicobacter hepaticus, a commensal bacterium with pathogenic potential. This beneficial activity requires a single microbial molecule (polysaccharide A, PSA). In animals harbouring B. fragilis not expressing PSA, H. hepaticus colonization leads to disease and pro-inflammatory cytokine production in colonic tissues. Purified PSA administered to animals is required to suppress pro-inflammatory interleukin-17 production by intestinal immune cells and also inhibits in vitro reactions in cell cultures. Furthermore, PSA protects from inflammatory disease through a functional requirement for interleukin-10-producing CD4+ T cells. These results show that molecules of the bacterial microbiota can mediate the critical balance between health and disease. Harnessing the immunomodulatory capacity of symbiosis factors such as PSA might potentially provide therapeutics for human inflammatory disorders on the basis of entirely novel biological principles.
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                Author and article information

                Contributors
                wuzhd@mail.sysu.edu.cn
                sunxi2@mail.sysu.edu.cn
                lindt5@mail.sysu.edu.cn
                Journal
                Infect Dis Poverty
                Infect Dis Poverty
                Infectious Diseases of Poverty
                BioMed Central (London )
                2095-5162
                2049-9957
                24 November 2023
                24 November 2023
                2023
                : 12
                : 105
                Affiliations
                [1 ]Department of Parasitology, Zhongshan School of Medicine, Sun Yat-Sen University, ( https://ror.org/0064kty71) Guangzhou, China
                [2 ]GRID grid.12981.33, ISNI 0000 0001 2360 039X, Key Laboratory of Tropical Disease Control, Ministry of Education, , Sun Yat-Sen University, ; Guangzhou, China
                [3 ]Chinese Atomic Energy Agency Center of Excellence on Nuclear Technology Applications for Insect Control, Provincial Engineering Technology Research Center for Diseases-Vectors Control, Sun Yat-Sen University, ( https://ror.org/0064kty71) Guangzhou, China
                [4 ]GRID grid.284723.8, ISNI 0000 0000 8877 7471, Department of Traditional Chinese Medicine, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, , Southern Medical University, ; Guangzhou, China
                Article
                1159
                10.1186/s40249-023-01159-z
                10668521
                38001502
                3e8dc89e-2a0e-48d3-94e2-c2e72aeb693b
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 7 August 2023
                : 13 November 2023
                Funding
                Funded by: the National Key R&D Program of China
                Award ID: 2020YFC1200100
                Award ID: 2020YFC1200103
                Award ID: 2021YFC2300800
                Award ID: 2016YFC1200500
                Award Recipient :
                Funded by: the National Natural Science Foundation of China
                Award ID: 82202560
                Award ID: 82161160343
                Award ID: 82272361
                Award Recipient :
                Funded by: the Science and Technology Planning Project of Guangdong Province
                Award ID: 2021B1212040017
                Award Recipient :
                Funded by: the R&D Program in Key Areas of Guangdong Province
                Award ID: 2022B1111030002
                Award Recipient :
                Funded by: the Fundamental Research Funds for the Central University
                Award ID: 22qntd4813
                Award Recipient :
                Funded by: the 111 Project
                Award ID: B12003
                Award Recipient :
                Funded by: the 6th Nuclear Energy R&D Project
                Award ID: 20201192
                Award Recipient :
                Funded by: the National Parasitic Resource Center and Ministry of Science and Technology
                Award ID: NPRC-2019-194-30
                Award Recipient :
                Categories
                Scoping Review
                Custom metadata
                © National Institute of Parasitic Diseases 2023

                snail,intermediate host,gut microbiome,potential application,snail-born parasite,schistosome,schistosomiasis,angiostrongyluscantonensis,vector

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