Adaptive and Evolutionary Aspects of Integrons

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Molecular Microbiology and Immunology".

Deadline for manuscript submissions: closed (31 January 2022) | Viewed by 18635

Special Issue Editors


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Guest Editor
Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, Madrid, Spain
Interests: antibiotic resistance; integrin; adaptation; Evolution; innovation; recombination

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Guest Editor
Département Génomes et Génétique, Unité de Plasticité du Génome Bactérien, Institut Pasteur, Paris, France
Interests: bacterial plasticity; recombination; integron, genetics; single-stranded DNA

Special Issue Information

Dear Colleagues

Integrons are bacterial genetic elements that provide their host with enhanced evolvability. They do so by capturing and stockpiling small mobile genetic elements called integron cassettes, that bring novel functions to the host. Integrons are ancient structures naturally found in the chromosomes of roughly 10% of bacterial species associated to countless cassettes. A handful of integrons managed to reach our hospitals after being transposed onto conjugative plasmids, bringing antibiotic resistance cassettes as a cargo and triggering the rise of multidrug resistance in the 50’s. Integrons are now commonplace in clinical isolates worldwide and are generally regarded as major resistance determinants in the most dangerous Gram-negative pathogens.

Although the role that integrons play in the adaptation of environmental bacteria is a major issue that has been less explored, the prevalence and importance of these elements among clinical isolates is a testimony to the adaptive value they provide to their bacterial hosts. Part of this value comes from the streamlining of integrons to become subtly coupled to bacterial physiology, providing adaptation on demand. How such a nifty and unique piece of genetic equipment has originated is a story of evolutionary innovation that is only starting to be unveiled. 

The aim of this Special issue of Microorganisms is to gather new data that highlight the adaptive value of integrons in all environments -including the clinical setting- as well as to provide a deeper view on the possible evolutionary origins of these structures.

 

Dr. Jose A. Escudero
Dr. Céline Loot
Guest Editors

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Keywords

  • Antibiotic Resistance
  • Integron
  • Evolution
  • Adaptation
  • Recombination

Published Papers (4 papers)

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Research

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17 pages, 2411 KiB  
Article
Novel Mobile Integrons and Strain-Specific Integrase Genes within Shewanella spp. Unveil Multiple Lateral Genetic Transfer Events within The Genus
by Teolincacihuatl Ayala Nuñez, Gabriela N. Cerbino, María Florencia Rapisardi, Cecilia Quiroga and Daniela Centrón
Microorganisms 2022, 10(6), 1102; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10061102 - 26 May 2022
Cited by 2 | Viewed by 1802
Abstract
Shewanella spp. are Gram-negative bacteria that thrive in aquatic niches and also can cause infectious diseases as opportunistic pathogens. Chromosomal (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems [...] Read more.
Shewanella spp. are Gram-negative bacteria that thrive in aquatic niches and also can cause infectious diseases as opportunistic pathogens. Chromosomal (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems and their genetic surroundings in the genus. We identified 22 integrase gene types, 17 of which were newly described, showing traits of multiple events of lateral genetic transfer (LGT). Phylogenetic analysis showed that most of them were strain-specific, except for Shewanella algae, where SonIntIA-like may have co-evolved within the host as typical CIs. It is noteworthy that co-existence of up to five different integrase genes within a strain, as well as their wide dissemination to Alteromonadales, Vibrionales, Chromatiales, Oceanospirillales and Enterobacterales was observed. In addition, identification of two novel MIs suggests that continuous LGT events may have occurred resembling the behavior of class 1 integrons. The constant emergence of determinants associated to antimicrobial resistance worldwide, concomitantly with novel MIs in strains capable to harbor several types of integrons, may be an alarming threat for the recruitment of novel antimicrobial resistance gene cassettes in the genus Shewanella, with its consequent contribution towards multidrug resistance in clinical isolates. Full article
(This article belongs to the Special Issue Adaptive and Evolutionary Aspects of Integrons)
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14 pages, 16297 KiB  
Article
IntegronFinder 2.0: Identification and Analysis of Integrons across Bacteria, with a Focus on Antibiotic Resistance in Klebsiella
by Bertrand Néron, Eloi Littner, Matthieu Haudiquet, Amandine Perrin, Jean Cury and Eduardo P. C. Rocha
Microorganisms 2022, 10(4), 700; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10040700 - 24 Mar 2022
Cited by 58 | Viewed by 7776
Abstract
Integrons are flexible gene-exchanging platforms that contain multiple cassettes encoding accessory genes whose order is shuffled by a specific integrase. Integrons embedded within mobile genetic elements often contain multiple antibiotic resistance genes that they spread among nosocomial pathogens and contribute to the current [...] Read more.
Integrons are flexible gene-exchanging platforms that contain multiple cassettes encoding accessory genes whose order is shuffled by a specific integrase. Integrons embedded within mobile genetic elements often contain multiple antibiotic resistance genes that they spread among nosocomial pathogens and contribute to the current antibiotic resistance crisis. However, most integrons are presumably sedentary and encode a much broader diversity of functions. IntegronFinder is a widely used software to identify novel integrons in bacterial genomes, but has aged and lacks some useful functionalities to handle very large datasets of draft genomes or metagenomes. Here, we present IntegronFinder version 2. We have updated the code, improved its efficiency and usability, adapted the output to incomplete genome data, and added a few novel functions. We describe these changes and illustrate the relevance of the program by analyzing the distribution of integrons across more than 20,000 fully sequenced genomes. We also take full advantage of its novel capabilities to analyze close to 4000 Klebsiella pneumoniae genomes for the presence of integrons and antibiotic resistance genes within them. Our data show that K. pneumoniae has a large diversity of integrons and the largest mobile integron in our database of plasmids. The pangenome of these integrons contains a total of 165 different gene families with most of the largest families being related with resistance to numerous types of antibiotics. IntegronFinder is a free and open-source software available on multiple public platforms. Full article
(This article belongs to the Special Issue Adaptive and Evolutionary Aspects of Integrons)
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Review

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34 pages, 4918 KiB  
Review
Integron Functionality and Genome Innovation: An Update on the Subtle and Smart Strategy of Integrase and Gene Cassette Expression Regulation
by Érica L. Fonseca and Ana Carolina Vicente
Microorganisms 2022, 10(2), 224; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10020224 - 20 Jan 2022
Cited by 9 | Viewed by 3059
Abstract
Integrons are considered hot spots for bacterial evolution, since these platforms allow one-step genomic innovation by capturing and expressing genes that provide advantageous novelties, such as antibiotic resistance. The acquisition and shuffling of gene cassettes featured by integrons enable the population to rapidly [...] Read more.
Integrons are considered hot spots for bacterial evolution, since these platforms allow one-step genomic innovation by capturing and expressing genes that provide advantageous novelties, such as antibiotic resistance. The acquisition and shuffling of gene cassettes featured by integrons enable the population to rapidly respond to changing selective pressures. However, in order to avoid deleterious effects and fitness burden, the integron activity must be tightly controlled, which happens in an elegant and elaborate fashion, as discussed in detail in the present review. Here, we aimed to provide an up-to-date overview of the complex regulatory networks that permeate the expression and functionality of integrons at both transcriptional and translational levels. It was possible to compile strong shreds of evidence clearly proving that these versatile platforms include functions other than acquiring and expressing gene cassettes. The well-balanced mechanism of integron expression is intricately related with environmental signals, host cell physiology, fitness, and survival, ultimately leading to adaptation on the demand. Full article
(This article belongs to the Special Issue Adaptive and Evolutionary Aspects of Integrons)
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12 pages, 651 KiB  
Review
The Natural History of Integrons
by Timothy M. Ghaly, Michael R. Gillings, Anahit Penesyan, Qin Qi, Vaheesan Rajabal and Sasha G. Tetu
Microorganisms 2021, 9(11), 2212; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9112212 - 25 Oct 2021
Cited by 29 | Viewed by 4945
Abstract
Integrons were first identified because of their central role in assembling and disseminating antibiotic resistance genes in commensal and pathogenic bacteria. However, these clinically relevant integrons represent only a small proportion of integron diversity. Integrons are now known to be ancient genetic elements [...] Read more.
Integrons were first identified because of their central role in assembling and disseminating antibiotic resistance genes in commensal and pathogenic bacteria. However, these clinically relevant integrons represent only a small proportion of integron diversity. Integrons are now known to be ancient genetic elements that are hotspots for genomic diversity, helping to generate adaptive phenotypes. This perspective examines the diversity, functions, and activities of integrons within both natural and clinical environments. We show how the fundamental properties of integrons exquisitely pre-adapted them to respond to the selection pressures imposed by the human use of antimicrobial compounds. We then follow the extraordinary increase in abundance of one class of integrons (class 1) that has resulted from its acquisition by multiple mobile genetic elements, and subsequent colonisation of diverse bacterial species, and a wide range of animal hosts. Consequently, this class of integrons has become a significant pollutant in its own right, to the extent that it can now be detected in most ecosystems. As human activities continue to drive environmental instability, integrons will likely continue to play key roles in bacterial adaptation in both natural and clinical settings. Understanding the ecological and evolutionary dynamics of integrons can help us predict and shape these outcomes that have direct relevance to human and ecosystem health. Full article
(This article belongs to the Special Issue Adaptive and Evolutionary Aspects of Integrons)
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