Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential

Clostridium perfringens is the causative agent of many enterotoxic diseases in humans and animals, and it is present in diverse environments (soil, food, sewage, and water). Multilocus Sequence Typing (MLST) and Whole Genome Sequencing (WGS) have provided a general approach about genetic diversity o...

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Main Authors: Anny Camargo, Enzo Guerrero-Araya, Sergio Castañeda, Laura Vega, María X. Cardenas-Alvarez, César Rodríguez, Daniel Paredes-Sabja, Juan David Ramírez, Marina Muñoz
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.952081/full
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author Anny Camargo
Anny Camargo
Enzo Guerrero-Araya
Sergio Castañeda
Laura Vega
María X. Cardenas-Alvarez
María X. Cardenas-Alvarez
César Rodríguez
Daniel Paredes-Sabja
Daniel Paredes-Sabja
Juan David Ramírez
Juan David Ramírez
Marina Muñoz
Marina Muñoz
author_facet Anny Camargo
Anny Camargo
Enzo Guerrero-Araya
Sergio Castañeda
Laura Vega
María X. Cardenas-Alvarez
María X. Cardenas-Alvarez
César Rodríguez
Daniel Paredes-Sabja
Daniel Paredes-Sabja
Juan David Ramírez
Juan David Ramírez
Marina Muñoz
Marina Muñoz
author_sort Anny Camargo
collection DOAJ
description Clostridium perfringens is the causative agent of many enterotoxic diseases in humans and animals, and it is present in diverse environments (soil, food, sewage, and water). Multilocus Sequence Typing (MLST) and Whole Genome Sequencing (WGS) have provided a general approach about genetic diversity of C. perfringens; however, those studies are limited to specific locations and often include a reduced number of genomes. In this study, 372 C. perfringens genomes from multiple locations and sources were used to assess the genetic diversity and phylogenetic relatedness of this pathogen. In silico MLST was used for typing the isolates, and the resulting sequence types (ST) were assigned to clonal complexes (CC) based on allelic profiles that differ from its founder by up to double-locus variants. A pangenome analysis was conducted, and a core genome-based phylogenetic tree was created to define phylogenetic groups. Additionally, key virulence factors, toxinotypes, and antibiotic resistance genes were identified using ABRicate against Virulence Factor Database (VFDB), TOXiper, and Resfinder, respectively. The majority of the C. perfringens genomes found in publicly available databases were derived from food (n = 85) and bird (n = 85) isolates. A total of 195 STs, some of them shared between sources such as food and human, horses and dogs, and environment and birds, were grouped in 25 CC and distributed along five phylogenetic groups. Fifty-three percent of the genomes were allocated to toxinotype A, followed by F (32%) and G (7%). The most frequently found virulence factors based on > 70% coverage and 99.95% identity were plc (100%), nanH (99%), ccp (99%), and colA (98%), which encode an alpha-toxin, a sialidase, an alpha-clostripain, and a collagenase, respectively, while tetA (39.5%) and tetB (36.2%), which mediate tetracycline resistance determinants, were the most common antibiotic resistance genes detected. The analyses conducted here showed a better view of the presence of this pathogen across several host species. They also confirm that the genetic diversity of C. perfringens is based on a large number of virulence factors that vary among phylogroups, and antibiotic resistance markers, especially to tetracyclines, aminoglycosides, and macrolides. Those characteristics highlight the importance of C. perfringens as a one of the most common causes of foodborne illness.
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spelling doaj.art-e68a57e91f5c490892d7a094b98fd5db2022-12-22T03:04:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.952081952081Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potentialAnny Camargo0Anny Camargo1Enzo Guerrero-Araya2Sergio Castañeda3Laura Vega4María X. Cardenas-Alvarez5María X. Cardenas-Alvarez6César Rodríguez7Daniel Paredes-Sabja8Daniel Paredes-Sabja9Juan David Ramírez10Juan David Ramírez11Marina Muñoz12Marina Muñoz13Centro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaFaculty of Health Sciences, Universidad de Boyacá, Tunja, ColombiaANID, Millennium Science Initiative Program, Millennium Nucleus in the Biology of the Intestinal Microbiota, Santiago, ChileCentro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaCentro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaCentro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaDepartment of Pharmacology, University of North Carolina, Chapel Hill, NC, United StatesLaboratorio de Investigación en Bacteriología Anaerobia, Facultad de Microbiología, Centro de Investigación en Enfermedades Tropicales, Universidad de Costa Rica, San José, Costa RicaANID, Millennium Science Initiative Program, Millennium Nucleus in the Biology of the Intestinal Microbiota, Santiago, ChileDepartment of Biology, Texas A&M University, College Station, TX, United StatesCentro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaMolecular Microbiology Laboratory, Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, United StatesCentro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, ColombiaANID, Millennium Science Initiative Program, Millennium Nucleus in the Biology of the Intestinal Microbiota, Santiago, ChileClostridium perfringens is the causative agent of many enterotoxic diseases in humans and animals, and it is present in diverse environments (soil, food, sewage, and water). Multilocus Sequence Typing (MLST) and Whole Genome Sequencing (WGS) have provided a general approach about genetic diversity of C. perfringens; however, those studies are limited to specific locations and often include a reduced number of genomes. In this study, 372 C. perfringens genomes from multiple locations and sources were used to assess the genetic diversity and phylogenetic relatedness of this pathogen. In silico MLST was used for typing the isolates, and the resulting sequence types (ST) were assigned to clonal complexes (CC) based on allelic profiles that differ from its founder by up to double-locus variants. A pangenome analysis was conducted, and a core genome-based phylogenetic tree was created to define phylogenetic groups. Additionally, key virulence factors, toxinotypes, and antibiotic resistance genes were identified using ABRicate against Virulence Factor Database (VFDB), TOXiper, and Resfinder, respectively. The majority of the C. perfringens genomes found in publicly available databases were derived from food (n = 85) and bird (n = 85) isolates. A total of 195 STs, some of them shared between sources such as food and human, horses and dogs, and environment and birds, were grouped in 25 CC and distributed along five phylogenetic groups. Fifty-three percent of the genomes were allocated to toxinotype A, followed by F (32%) and G (7%). The most frequently found virulence factors based on > 70% coverage and 99.95% identity were plc (100%), nanH (99%), ccp (99%), and colA (98%), which encode an alpha-toxin, a sialidase, an alpha-clostripain, and a collagenase, respectively, while tetA (39.5%) and tetB (36.2%), which mediate tetracycline resistance determinants, were the most common antibiotic resistance genes detected. The analyses conducted here showed a better view of the presence of this pathogen across several host species. They also confirm that the genetic diversity of C. perfringens is based on a large number of virulence factors that vary among phylogroups, and antibiotic resistance markers, especially to tetracyclines, aminoglycosides, and macrolides. Those characteristics highlight the importance of C. perfringens as a one of the most common causes of foodborne illness.https://www.frontiersin.org/articles/10.3389/fmicb.2022.952081/fullClostridium perfringensintra-species diversitymultilocus sequence typinggenomic epidemiologytoxinotypes
spellingShingle Anny Camargo
Anny Camargo
Enzo Guerrero-Araya
Sergio Castañeda
Laura Vega
María X. Cardenas-Alvarez
María X. Cardenas-Alvarez
César Rodríguez
Daniel Paredes-Sabja
Daniel Paredes-Sabja
Juan David Ramírez
Juan David Ramírez
Marina Muñoz
Marina Muñoz
Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
Frontiers in Microbiology
Clostridium perfringens
intra-species diversity
multilocus sequence typing
genomic epidemiology
toxinotypes
title Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
title_full Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
title_fullStr Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
title_full_unstemmed Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
title_short Intra-species diversity of Clostridium perfringens: A diverse genetic repertoire reveals its pathogenic potential
title_sort intra species diversity of clostridium perfringens a diverse genetic repertoire reveals its pathogenic potential
topic Clostridium perfringens
intra-species diversity
multilocus sequence typing
genomic epidemiology
toxinotypes
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.952081/full
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