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Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection

Clostridioides difficile infection (CDI) creates an imbalance in the intestinal microbiota due to the interaction of the components making up this ecosystem, but little is known about the impact of this disease on other microbial members. This work has thus been aimed at evaluating the taxonomic com...

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Autores principales: Herrera, Giovanny, Arboleda, Juan Camilo, Pérez-Jaramillo, Juan E., Patarroyo, Manuel Alfonso, Ramírez, Juan David, Muñoz, Marina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9602525/
https://www.ncbi.nlm.nih.gov/pubmed/36154277
http://dx.doi.org/10.1128/spectrum.00502-22
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author Herrera, Giovanny
Arboleda, Juan Camilo
Pérez-Jaramillo, Juan E.
Patarroyo, Manuel Alfonso
Ramírez, Juan David
Muñoz, Marina
author_facet Herrera, Giovanny
Arboleda, Juan Camilo
Pérez-Jaramillo, Juan E.
Patarroyo, Manuel Alfonso
Ramírez, Juan David
Muñoz, Marina
author_sort Herrera, Giovanny
collection PubMed
description Clostridioides difficile infection (CDI) creates an imbalance in the intestinal microbiota due to the interaction of the components making up this ecosystem, but little is known about the impact of this disease on other microbial members. This work has thus been aimed at evaluating the taxonomic composition, potential gene-associated functions, virulence factors, and antimicrobial resistance profiles of gut microbiomes. A total of 48 DNA samples obtained from patients with health care facility-acquired (HCFO) and community-onset (CO) diarrhea were distributed in the following four groups according to CDI status: HCFO/+ (n = 13), HCFO/– (n = 8), CO/+ (n = 13), and CO/– (n = 14). These samples were subjected to shotgun metagenomics sequencing. Although the CDI groups’ microbiota had microbiome alterations, the greatest imbalance was observed in the in the HCFO+/– groups, with an increase in common pathogens and phage populations, as well as a decrease in beneficial microorganisms that leads to a negative impact on some intestinal homeostasis-related metabolic processes. A reduction in the relative abundance of butyrate metabolism-associated genes was also detected in the HCFO groups (P < 0.01), with an increase in some virulence factors and antibiotic-resistance markers. A set of 51 differentially abundant species in the groups with potential association to CDI enabled its characterization, leading to their spatial separation by onset. Strong correlations between phages and some archaeal and bacterial phyla were identified. This highlighted the need to study the microbiota’s various components since their imbalance is multifactorial, with some pathogens contributing to a greater or lesser extent because of their interaction with the ecosystem they inhabit. IMPORTANCE Clostridioides difficile infection represents a serious public health problem in different countries due to its high morbi-mortality and the high costs it represents for health care systems. Studies have shown the impact of this infection on intestinal microbiome homeostasis, mainly on bacterial populations. Our research provides evidence of the impact of CDI at both the compositional (bacteria, archaea, and viruses), and functional levels, allowing us to understand that the alterations of the microbiota occur systemically and are caused by multiple perturbations generated by different members of the microbiota as well as by some pathogens that take advantage of the imbalance to proliferate. Likewise, the 51 differentially abundant species in the study groups with potential association to CDI found in this study could help us envisage future treatments against this and other inflammatory diseases, improving future therapeutic options for patients.
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spelling pubmed-96025252022-10-27 Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection Herrera, Giovanny Arboleda, Juan Camilo Pérez-Jaramillo, Juan E. Patarroyo, Manuel Alfonso Ramírez, Juan David Muñoz, Marina Microbiol Spectr Research Article Clostridioides difficile infection (CDI) creates an imbalance in the intestinal microbiota due to the interaction of the components making up this ecosystem, but little is known about the impact of this disease on other microbial members. This work has thus been aimed at evaluating the taxonomic composition, potential gene-associated functions, virulence factors, and antimicrobial resistance profiles of gut microbiomes. A total of 48 DNA samples obtained from patients with health care facility-acquired (HCFO) and community-onset (CO) diarrhea were distributed in the following four groups according to CDI status: HCFO/+ (n = 13), HCFO/– (n = 8), CO/+ (n = 13), and CO/– (n = 14). These samples were subjected to shotgun metagenomics sequencing. Although the CDI groups’ microbiota had microbiome alterations, the greatest imbalance was observed in the in the HCFO+/– groups, with an increase in common pathogens and phage populations, as well as a decrease in beneficial microorganisms that leads to a negative impact on some intestinal homeostasis-related metabolic processes. A reduction in the relative abundance of butyrate metabolism-associated genes was also detected in the HCFO groups (P < 0.01), with an increase in some virulence factors and antibiotic-resistance markers. A set of 51 differentially abundant species in the groups with potential association to CDI enabled its characterization, leading to their spatial separation by onset. Strong correlations between phages and some archaeal and bacterial phyla were identified. This highlighted the need to study the microbiota’s various components since their imbalance is multifactorial, with some pathogens contributing to a greater or lesser extent because of their interaction with the ecosystem they inhabit. IMPORTANCE Clostridioides difficile infection represents a serious public health problem in different countries due to its high morbi-mortality and the high costs it represents for health care systems. Studies have shown the impact of this infection on intestinal microbiome homeostasis, mainly on bacterial populations. Our research provides evidence of the impact of CDI at both the compositional (bacteria, archaea, and viruses), and functional levels, allowing us to understand that the alterations of the microbiota occur systemically and are caused by multiple perturbations generated by different members of the microbiota as well as by some pathogens that take advantage of the imbalance to proliferate. Likewise, the 51 differentially abundant species in the study groups with potential association to CDI found in this study could help us envisage future treatments against this and other inflammatory diseases, improving future therapeutic options for patients. American Society for Microbiology 2022-09-26 /pmc/articles/PMC9602525/ /pubmed/36154277 http://dx.doi.org/10.1128/spectrum.00502-22 Text en Copyright © 2022 Herrera et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Herrera, Giovanny
Arboleda, Juan Camilo
Pérez-Jaramillo, Juan E.
Patarroyo, Manuel Alfonso
Ramírez, Juan David
Muñoz, Marina
Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title_full Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title_fullStr Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title_full_unstemmed Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title_short Microbial Interdomain Interactions Delineate the Disruptive Intestinal Homeostasis in Clostridioides difficile Infection
title_sort microbial interdomain interactions delineate the disruptive intestinal homeostasis in clostridioides difficile infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9602525/
https://www.ncbi.nlm.nih.gov/pubmed/36154277
http://dx.doi.org/10.1128/spectrum.00502-22
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