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Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.

ABSTRACT: In spite of the extensive contribution of intestinal pathology to the pathophysiology of schistosomiasis, little is known of the impact of schistosome infection on the composition of the gut microbiota of its mammalian host. Here, we characterised the fluctuations in the composition of the gut microbial flora of the small and large intestine, as well as the changes in abundance of individual microbial species, of mice experimentally infected with Schistosoma mansoni with the goal of identifying microbial taxa with potential roles in the pathophysiology of infection and disease. Bioinformatic analyses of bacterial 16S rRNA gene data revealed an overall reduction in gut microbial alpha diversity, alongside a significant increase in microbial beta diversity characterised by expanded populations of Akkermansia muciniphila (phylum Verrucomicrobia) and lactobacilli, in the gut microbiota of S. mansoni-infected mice when compared to uninfected control animals. These data support a role of the mammalian gut microbiota in the pathogenesis of hepato-intestinal schistosomiasis and serves as a foundation for the design of mechanistic studies to unravel the complex relationships amongst parasitic helminths, gut microbiota, pathophysiology of infection and host immunity.

SUBMITTER: Jenkins TP

PROVIDER: S-EPMC6089957 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.

Jenkins Timothy P TP Peachey Laura E LE Ajami Nadim J NJ MacDonald Andrew S AS Hsieh Michael H MH Brindley Paul J PJ Cantacessi Cinzia C Rinaldi Gabriel G

Scientific reports 20180813 1

In spite of the extensive contribution of intestinal pathology to the pathophysiology of schistosomiasis, little is known of the impact of schistosome infection on the composition of the gut microbiota of its mammalian host. Here, we characterised the fluctuations in the composition of the gut microbial flora of the small and large intestine, as well as the changes in abundance of individual microbial species, of mice experimentally infected with Schistosoma mansoni with the goal of identifying ...[more]

PMID: 30104612

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Project description:BackgroundThe infective schistosome cercaria develops within the intramolluscan daughter sporocyst from an undifferentiated germ ball, during which synthesis of proteins essential for infection occurs. When the aquatic cercaria locates the mammalian host it rapidly penetrates into the epidermis using glandular secretions. It then undergoes metamorphosis into the schistosomulum, including replacement of its tegument surface membranes, a process taking several days before it exits the skin. Patterns of gene expression underlying this transition have been characterised.Methods and principal findingsAll gene models from the S. mansoni genome (www.GeneDB.org) were incorporated into a high-density oligonucleotide array. Double-stranded cDNA from germ balls, cercariae, and day 3 schistosomula was hybridised to the array without amplification. Statistical analysis was performed using Bioconductor to reveal differentially transcribed loci. Genes were categorised on the basis of biological process, tissue association or molecular function to aid understanding of the complex processes occurring. Genes necessary for DNA replication were enriched only in the germ ball, while those involved in translation were up-regulated in the germ ball and/or day 3 schistosomulum. Different sets of developmental genes were up-regulated at each stage. A large number of genes encoding elastases and invadolysins, and some venom allergen-like proteins were up-regulated in the germ ball, those encoding cysteine and aspartic proteases in the cercaria and schistosomulum. Micro exon genes encoding variant secreted proteins were highly up-regulated in the schistosomulum along with tegument and gut-associated genes, coincident with remodelling of the parasite body. Genes encoding membrane proteins were prominently up-regulated in the cercaria and/or day 3 schistosomulum.Conclusions/significanceOur study highlights an expanded number of transcripts encoding proteins potentially involved in skin invasion. It illuminates the process of metamorphosis into the schistosomulum and highlights the very early activation of gut-associated genes whilst revealing little change in the parasite's energy metabolism or stress responses.

Project description:BACKGROUND:Infection with Schistosoma mansoni is a major cause of morbidity and mortality in endemic areas, and is increasingly diagnosed in migrants and travellers outside transmission areas. Markers for the assessment of morbidity and impact of control programs in endemic areas and for the clinical management of patients in the clinical setting are scant, especially for intestinal involvement. Ultrasonography is well established to evaluate hepatosplenic pathology; on the contrary, ultrasound evaluation of intestinal schistosomiasis is virtually unexplored. In this pilot study, we aimed to describe and evaluate the accuracy of unenhanced intestinal ultrasound for morbidity due to intestinal S. mansoni infection. METHODOLOGY/PRINCIPAL FINDINGS:We performed a blind case-control study of unenhanced intestinal ultrasound on 107 adults accessing the outpatient clinic of our Centre for Tropical Diseases between January-July 2018 as part of a screening for tropical diseases in migrants and travellers returning from endemic areas. Other clinical and laboratory data were obtained routine examination reports. We could not find any overtly pathological thickness of the gut wall in the sigma, proximal ascending colon, and terminal ileum, in patients with S. mansoni infection (n = 17), S. haematobium infection (n = 7), positive anti-Schistosoma serology (n = 31), and uninfected individuals (n = 52), with no difference among groups as assessed by ANOVA. No polyps or other intestinal abnormalities were visualized. There was no significant change in gut wall thickness one month after treatment with praziquantel in patients with S. mansoni infection (n = 11). CONCLUSIONS/SIGNIFICANCE:Our preliminary results suggest that intestinal ultrasound might not be a sensitive tool for detecting minor intestinal morbidity due to schistosomiasis. Further studies in a hospital setting comparing colonoscopy and ultrasonography may be envisaged; in endemic areas, further studies are needed to describe and assess the usefulness of intestinal ultrasound in patients stratified by infection intensity and compared with markers such as calprotectin and fecal occult blood.

Dataset Information

Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.

Publications

Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota.

Similar Datasets

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