Cargando…

Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene

Microbes live within complex communities of interacting populations, either free-living in waters and soils or symbionts of animals and plants. Their interactions include the production of antimicrobial peptides (bacteriocins) to antagonize competitors, and these producers must carry their own immun...

Descripción completa

Detalles Bibliográficos
Autores principales: Teso-Pérez, Claudia, Martínez-Bueno, Manuel, Peralta Sánchez, Juan Manuel, Valdivia, Eva, Fárez-Vidal, María Esther, Martín-Platero, Antonio Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10598978/
https://www.ncbi.nlm.nih.gov/pubmed/37875795
http://dx.doi.org/10.1186/s12864-023-09750-2
_version_ 1785125675679612928
author Teso-Pérez, Claudia
Martínez-Bueno, Manuel
Peralta Sánchez, Juan Manuel
Valdivia, Eva
Fárez-Vidal, María Esther
Martín-Platero, Antonio Manuel
author_facet Teso-Pérez, Claudia
Martínez-Bueno, Manuel
Peralta Sánchez, Juan Manuel
Valdivia, Eva
Fárez-Vidal, María Esther
Martín-Platero, Antonio Manuel
author_sort Teso-Pérez, Claudia
collection PubMed
description Microbes live within complex communities of interacting populations, either free-living in waters and soils or symbionts of animals and plants. Their interactions include the production of antimicrobial peptides (bacteriocins) to antagonize competitors, and these producers must carry their own immunity gene for self-protection. Whether other coexisting populations are sensitive or resistant to the bacteriocin producer will be key for the population dynamics within the microbial community. The immunity gene frequently consists of an ABC transporter to repel its own bacteriocin but rarely protects against a nonrelated bacteriocin. A case where this cross-resistance occurs mediated by a shared ABC transporter has been shown between enterocins MR10A/B and AS-48. The first is an L50-like leaderless enterocin, while AS-48 is a circular enterocin. In addition, L50-like enterocins such as MR10A/B have been found in E. faecalis and E. faecium, but AS-48 appears only in E. faecalis. Thus, using the ABC transporter of the enterocin MR10A/B gene cluster of Enterococcus faecalis MRR10-3 as a cross-resistance model, we aimed to unravel to what extent a particular ABC transporter can be shared across multiple bacteriocinogenic bacterial populations. To this end, we screened the MR10A/B-ABC transporters in available microbial genomes and analyzed their sequence homologies and distribution. Overall, our main findings are as follows: (i) the MR10A/B-ABC transporter is associated with multiple enterocin gene clusters; (ii) the different enterocins associated with this transporter have a saposin-like fold in common; (iii) the Mr10E component of the transporter is more conserved within its associated enterocin, while the Mr10FGH components are more conserved within the carrying species. This is the least known component of the transporter, but it has shown the greatest specificity to its corresponding enterocin. Bacteriocins are now being investigated as an alternative to antibiotics; hence, the wider or narrower distribution of the particular immunity gene should be taken into account for clinical applications to avoid the selection of resistant strains. Further research will be needed to investigate the mechanistic interactions between the Mr10E transporter component and the bacteriocin as well as the specific ecological and evolutionary mechanisms involved in the spread of the immunity transporter across multiple bacteriocins. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09750-2.
format Online
Article
Text
id pubmed-10598978
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-105989782023-10-26 Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene Teso-Pérez, Claudia Martínez-Bueno, Manuel Peralta Sánchez, Juan Manuel Valdivia, Eva Fárez-Vidal, María Esther Martín-Platero, Antonio Manuel BMC Genomics Research Microbes live within complex communities of interacting populations, either free-living in waters and soils or symbionts of animals and plants. Their interactions include the production of antimicrobial peptides (bacteriocins) to antagonize competitors, and these producers must carry their own immunity gene for self-protection. Whether other coexisting populations are sensitive or resistant to the bacteriocin producer will be key for the population dynamics within the microbial community. The immunity gene frequently consists of an ABC transporter to repel its own bacteriocin but rarely protects against a nonrelated bacteriocin. A case where this cross-resistance occurs mediated by a shared ABC transporter has been shown between enterocins MR10A/B and AS-48. The first is an L50-like leaderless enterocin, while AS-48 is a circular enterocin. In addition, L50-like enterocins such as MR10A/B have been found in E. faecalis and E. faecium, but AS-48 appears only in E. faecalis. Thus, using the ABC transporter of the enterocin MR10A/B gene cluster of Enterococcus faecalis MRR10-3 as a cross-resistance model, we aimed to unravel to what extent a particular ABC transporter can be shared across multiple bacteriocinogenic bacterial populations. To this end, we screened the MR10A/B-ABC transporters in available microbial genomes and analyzed their sequence homologies and distribution. Overall, our main findings are as follows: (i) the MR10A/B-ABC transporter is associated with multiple enterocin gene clusters; (ii) the different enterocins associated with this transporter have a saposin-like fold in common; (iii) the Mr10E component of the transporter is more conserved within its associated enterocin, while the Mr10FGH components are more conserved within the carrying species. This is the least known component of the transporter, but it has shown the greatest specificity to its corresponding enterocin. Bacteriocins are now being investigated as an alternative to antibiotics; hence, the wider or narrower distribution of the particular immunity gene should be taken into account for clinical applications to avoid the selection of resistant strains. Further research will be needed to investigate the mechanistic interactions between the Mr10E transporter component and the bacteriocin as well as the specific ecological and evolutionary mechanisms involved in the spread of the immunity transporter across multiple bacteriocins. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09750-2. BioMed Central 2023-10-24 /pmc/articles/PMC10598978/ /pubmed/37875795 http://dx.doi.org/10.1186/s12864-023-09750-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Teso-Pérez, Claudia
Martínez-Bueno, Manuel
Peralta Sánchez, Juan Manuel
Valdivia, Eva
Fárez-Vidal, María Esther
Martín-Platero, Antonio Manuel
Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title_full Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title_fullStr Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title_full_unstemmed Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title_short Circular and L50-like leaderless enterocins share a common ABC-transporter immunity gene
title_sort circular and l50-like leaderless enterocins share a common abc-transporter immunity gene
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10598978/
https://www.ncbi.nlm.nih.gov/pubmed/37875795
http://dx.doi.org/10.1186/s12864-023-09750-2
work_keys_str_mv AT tesoperezclaudia circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene
AT martinezbuenomanuel circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene
AT peraltasanchezjuanmanuel circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene
AT valdiviaeva circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene
AT farezvidalmariaesther circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene
AT martinplateroantoniomanuel circularandl50likeleaderlessenterocinsshareacommonabctransporterimmunitygene