Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene

Abstract Crosstalk between the gut microbiota and intestinal epithelium shapes the gut environment and profoundly influences the intestinal immune homeostasis. Glycosylphosphatidylinositol anchored proteins (GPI – APs) contribute to a variety of gut-associated immune functions, including microbial s...

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Main Authors: Aditi Jangid, Shinji Fukuda, Masahide Seki, Yutaka Suzuki, Todd D. Taylor, Hiroshi Ohno, Tulika Prakash
Format: Article
Language:English
Published: Nature Portfolio 2022-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-15150-5
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author Aditi Jangid
Shinji Fukuda
Masahide Seki
Yutaka Suzuki
Todd D. Taylor
Hiroshi Ohno
Tulika Prakash
author_facet Aditi Jangid
Shinji Fukuda
Masahide Seki
Yutaka Suzuki
Todd D. Taylor
Hiroshi Ohno
Tulika Prakash
author_sort Aditi Jangid
collection DOAJ
description Abstract Crosstalk between the gut microbiota and intestinal epithelium shapes the gut environment and profoundly influences the intestinal immune homeostasis. Glycosylphosphatidylinositol anchored proteins (GPI – APs) contribute to a variety of gut-associated immune functions, including microbial surveillance and defense, and epithelial cell polarity. Properly polarised epithelial cells are essential for the establishment of the barrier function of gut epithelia. The Piga gene is one among seven genes that encode for an enzyme which is involved in the first step of GPI-anchor biosynthesis. This is the first study reporting a knockout of the intestinal epithelial cell-specific Piga gene (Piga-/-) and its association with the gut microbiota in mice using a whole metagenome shotgun-based sequencing approach. An overall reduced microbiota diversity has been observed in the Piga-/- group as compared to the control group (ANOVA p = 0.34). The taxonomic biomarkers, namely: Gammaproteobacteria (class), Enterobacterales (order), Enterobacteriaceae (family), Escherichia (genus), Proteus (genus) and Escherichia coli (species), increased more in the Piga-/- mice as compared to in the control group. Further, the pathogenic E. coli strains, namely E. coli O157:H7 str. EDL 933 (EHEC), E. coli CFT073 (UPEC) and E. coli 536 (UPEC), were found in the Piga-/- mice which also harbored virulence factor transporters. In addition, the taxa responsible for short chain fatty acid production were decreased in the Piga-/- group. The Piga-/- mice gut harbored an increased number of microbial functions responsible for the survival of pathogens in the inflamed gut environment. Our observations clearly indicate that the Piga-/- mice gut might have an overall enhancement in pathogenic behaviour and reduced capabilities beneficial to health.
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spelling doaj.art-1806b405d24249e185752cd3765296a72022-12-22T00:17:12ZengNature PortfolioScientific Reports2045-23222022-06-0112111210.1038/s41598-022-15150-5Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga geneAditi Jangid0Shinji Fukuda1Masahide Seki2Yutaka Suzuki3Todd D. Taylor4Hiroshi Ohno5Tulika Prakash6BioX Centre and School of Basic Sciences, Indian Institute of Technology MandiInstitute for Advanced Biosciences, Keio UniversityDepartment of Computational Biology and Medical Sciences, The University of TokyoDepartment of Computational Biology and Medical Sciences, The University of TokyoLaboratory for Microbiome Sciences, RIKEN Center for Integrative Medical SciencesLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical SciencesBioX Centre and School of Basic Sciences, Indian Institute of Technology MandiAbstract Crosstalk between the gut microbiota and intestinal epithelium shapes the gut environment and profoundly influences the intestinal immune homeostasis. Glycosylphosphatidylinositol anchored proteins (GPI – APs) contribute to a variety of gut-associated immune functions, including microbial surveillance and defense, and epithelial cell polarity. Properly polarised epithelial cells are essential for the establishment of the barrier function of gut epithelia. The Piga gene is one among seven genes that encode for an enzyme which is involved in the first step of GPI-anchor biosynthesis. This is the first study reporting a knockout of the intestinal epithelial cell-specific Piga gene (Piga-/-) and its association with the gut microbiota in mice using a whole metagenome shotgun-based sequencing approach. An overall reduced microbiota diversity has been observed in the Piga-/- group as compared to the control group (ANOVA p = 0.34). The taxonomic biomarkers, namely: Gammaproteobacteria (class), Enterobacterales (order), Enterobacteriaceae (family), Escherichia (genus), Proteus (genus) and Escherichia coli (species), increased more in the Piga-/- mice as compared to in the control group. Further, the pathogenic E. coli strains, namely E. coli O157:H7 str. EDL 933 (EHEC), E. coli CFT073 (UPEC) and E. coli 536 (UPEC), were found in the Piga-/- mice which also harbored virulence factor transporters. In addition, the taxa responsible for short chain fatty acid production were decreased in the Piga-/- group. The Piga-/- mice gut harbored an increased number of microbial functions responsible for the survival of pathogens in the inflamed gut environment. Our observations clearly indicate that the Piga-/- mice gut might have an overall enhancement in pathogenic behaviour and reduced capabilities beneficial to health.https://doi.org/10.1038/s41598-022-15150-5
spellingShingle Aditi Jangid
Shinji Fukuda
Masahide Seki
Yutaka Suzuki
Todd D. Taylor
Hiroshi Ohno
Tulika Prakash
Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
Scientific Reports
title Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
title_full Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
title_fullStr Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
title_full_unstemmed Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
title_short Gut microbiota alternation under the intestinal epithelium-specific knockout of mouse Piga gene
title_sort gut microbiota alternation under the intestinal epithelium specific knockout of mouse piga gene
url https://doi.org/10.1038/s41598-022-15150-5
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