Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes

Background Hypertension is associated with gut dysbiosis, altered intestinal immunity, and gut pathology in animal models and humans. Although these findings have implicated impaired interactions between gut and gut microbiota in hypertension, little is known about the specific functional gut microb...

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Main Authors: Jing Li, Elaine M. Richards, Ramakumar Tummala, Carl J. Pepine, Mohan K. Raizada, Tao Yang
Format: Article
Language:English
Published: Wiley 2023-02-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
Subjects:
Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.122.027918
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author Jing Li
Elaine M. Richards
Ramakumar Tummala
Carl J. Pepine
Mohan K. Raizada
Tao Yang
author_facet Jing Li
Elaine M. Richards
Ramakumar Tummala
Carl J. Pepine
Mohan K. Raizada
Tao Yang
author_sort Jing Li
collection DOAJ
description Background Hypertension is associated with gut dysbiosis, altered intestinal immunity, and gut pathology in animal models and humans. Although these findings have implicated impaired interactions between gut and gut microbiota in hypertension, little is known about the specific functional gut microbes that interact with intestinal mucosa. Methods and Results To identify these microbes, we sorted Immunoglobin A (IgA)‐coated (IgA+) and IgA‐noncoated (IgA−) bacteria using a combination of magnetic‐activated cell sorting and fluorescence‐activated cell sorting, and subsequently performed 16 S rRNA gene sequencing (IgA‐SEQ) to determine the microbial composition of IgA+ and IgA− fractions in spontaneously hypertensive rats (SHR) and normotensive Wistar Kyoto rats. We observed a significant decrease in IgA+ bacteria in SHR compared with Wistar Kyoto and a distinct composition of IgA+ and IgA− bacteria between Wistar Kyoto and SHR, showing more IgA‐bound Proteobacteria, Bacteroidetes and Actinobacteria but less of Firmicutes in SHR at the phylum level. We further identified enriched IgA‐coated Romboutsia, Turicibacter, Ileibacterium, and Dubosiella in SHR that were negatively correlated with the various pathways including antigen presentation, immune response, cell junction organization, epithelium development, and defense response to virus. Conclusions We demonstrate new IgA‐coated bacteria that participate in host‐microbiota communication in hypertension, suggesting promising therapeutic interventions targeting these bacteria for hypertension management.
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spelling doaj.art-bcbf225d3c214aa394a2bfea559835812023-11-17T17:54:26ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802023-02-0112410.1161/JAHA.122.027918Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut MicrobesJing Li0Elaine M. Richards1Ramakumar Tummala2Carl J. Pepine3Mohan K. Raizada4Tao Yang5Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden Chinese Academy of Sciences Wuhan Hubei ChinaDepartment of Physiology and Functional Genomics University of Florida College of Medicine Gainesville FL USADepartment of Physiology and Pharmacology Center for Hypertension and Precision Medicine College of Medicine and Life Sciences University of Toledo OH USADivision of Cardiovascular Medicine Department of Medicine University of Florida College of Medicine Gainesville FL USADepartment of Physiology and Functional Genomics University of Florida College of Medicine Gainesville FL USADepartment of Physiology and Pharmacology Center for Hypertension and Precision Medicine College of Medicine and Life Sciences University of Toledo OH USABackground Hypertension is associated with gut dysbiosis, altered intestinal immunity, and gut pathology in animal models and humans. Although these findings have implicated impaired interactions between gut and gut microbiota in hypertension, little is known about the specific functional gut microbes that interact with intestinal mucosa. Methods and Results To identify these microbes, we sorted Immunoglobin A (IgA)‐coated (IgA+) and IgA‐noncoated (IgA−) bacteria using a combination of magnetic‐activated cell sorting and fluorescence‐activated cell sorting, and subsequently performed 16 S rRNA gene sequencing (IgA‐SEQ) to determine the microbial composition of IgA+ and IgA− fractions in spontaneously hypertensive rats (SHR) and normotensive Wistar Kyoto rats. We observed a significant decrease in IgA+ bacteria in SHR compared with Wistar Kyoto and a distinct composition of IgA+ and IgA− bacteria between Wistar Kyoto and SHR, showing more IgA‐bound Proteobacteria, Bacteroidetes and Actinobacteria but less of Firmicutes in SHR at the phylum level. We further identified enriched IgA‐coated Romboutsia, Turicibacter, Ileibacterium, and Dubosiella in SHR that were negatively correlated with the various pathways including antigen presentation, immune response, cell junction organization, epithelium development, and defense response to virus. Conclusions We demonstrate new IgA‐coated bacteria that participate in host‐microbiota communication in hypertension, suggesting promising therapeutic interventions targeting these bacteria for hypertension management.https://www.ahajournals.org/doi/10.1161/JAHA.122.027918host‐microbiota communicationhypertensionImmunoglobin A‐coated bacteria
spellingShingle Jing Li
Elaine M. Richards
Ramakumar Tummala
Carl J. Pepine
Mohan K. Raizada
Tao Yang
Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
host‐microbiota communication
hypertension
Immunoglobin A‐coated bacteria
title Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
title_full Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
title_fullStr Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
title_full_unstemmed Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
title_short Host‐Microbiota Communication in Spontaneously Hypertensive Rats Generates Unique IgA‐Coated Gut Microbes
title_sort host microbiota communication in spontaneously hypertensive rats generates unique iga coated gut microbes
topic host‐microbiota communication
hypertension
Immunoglobin A‐coated bacteria
url https://www.ahajournals.org/doi/10.1161/JAHA.122.027918
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