The extent of carbapenemase-encoding genes in public genome sequences

Genome sequences provide information on the genetic elements present in an organism, and currently there are databases containing hundreds of thousands of bacterial genome sequences. These repositories allow for mining patterns concerning antibiotic resistance gene occurrence in both pathogenic and non-pathogenic bacteria in e.g. natural or animal environments, and link these to relevant metadata such as bacterial host species, country and year of isolation, and co-occurrence with other resistance genes. In addition, the advances in the prediction of mobile genetic elements, and discerning chromosomal from plasmid DNA, broadens our view on the mechanism mediating dissemination. In this study we utilize the vast amount of data in the public database PATRIC to investigate the dissemination of carbapenemase-encoding genes (CEGs), the emergence and spread of which is considered a grave public health concern. Based on publicly available genome sequences from PATRIC and manually curated CEG sequences from the beta lactam database, we found 7,964 bacterial genomes, belonging to at least 70 distinct species, that carry in total 9,892 CEGs, amongst which blaNDM, blaOXA, blaVIM, blaIMP and blaKPC. We were able to distinguish between chromosomally located resistance genes (4,137; 42%) and plasmid-located resistance genes (5,753; 58%). We found that a large proportion of the identified CEGs were identical, i.e. displayed 100% nucleotide similarity in multiple bacterial species (8,361 out of 9,892 genes; 85%). For example, the New Delhi metallo-beta-lactamase NDM-1 was found in 42 distinct bacterial species, and present in seven different environments. Our data show the extent of carbapenem-resistance far beyond the canonical species Acetinobacter baumannii, Klebsiella pneumoniae or Pseudomonas aeruginosa. These types of data complement previous systematic reviews, in which carbapenem-resistant Enterobacteriaceae were found in wildlife, livestock and companion animals. Considering the widespread distribution of CEGs, we see a need for comprehensive surveillance and transmission studies covering more host species and environments, akin to previous extensive surveys that focused on extended spectrum beta-lactamases. This may help to fully appreciate the spread of CEGs and improve the understanding of mechanisms underlying transmission, which could lead to interventions minimizing transmission to humans.

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The use of aminoglycosides in animals within the EU: development of resistance in animals and possible impact on human and animal health: a review

Journal of Antimicrobial Chemotherapy ◽

10.1093/jac/dkz161 ◽

2019 ◽

Vol 74 (9) ◽

pp. 2480-2496 ◽

Cited By ~ 5

Author(s):

Engeline van Duijkeren ◽

Christine Schwarz ◽

Damien Bouchard ◽

Boudewijn Catry ◽

Constança Pomba ◽

...

Keyword(s):

Veterinary Medicine ◽

Resistance Genes ◽

Bacterial Species ◽

Animal Health ◽

Acquired Resistance ◽

Companion Animals ◽

Mobile Genetic Elements ◽

Salmonella Spp ◽

Genetic Elements ◽

Animal Pathogens

AbstractAminoglycosides (AGs) are important antibacterial agents for the treatment of various infections in humans and animals. Following extensive use of AGs in humans, food-producing animals and companion animals, acquired resistance among human and animal pathogens and commensal bacteria has emerged. Acquired resistance occurs through several mechanisms, but enzymatic inactivation of AGs is the most common one. Resistance genes are often located on mobile genetic elements, facilitating their spread between different bacterial species and between animals and humans. AG resistance has been found in many different bacterial species, including those with zoonotic potential such as Salmonella spp., Campylobacter spp. and livestock-associated MRSA. The highest risk is anticipated from transfer of resistant enterococci or coliforms (Escherichia coli) since infections with these pathogens in humans would potentially be treated with AGs. There is evidence that the use of AGs in human and veterinary medicine is associated with the increased prevalence of resistance. The same resistance genes have been found in isolates from humans and animals. Evaluation of risk factors indicates that the probability of transmission of AG resistance from animals to humans through transfer of zoonotic or commensal foodborne bacteria and/or their mobile genetic elements can be regarded as high, although there are no quantitative data on the actual contribution of animals to AG resistance in human pathogens. Responsible use of AGs is of great importance in order to safeguard their clinical efficacy for human and veterinary medicine.

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Characterisation of Bacterial Isolates from Infected Post-Operative Patients in a Malaysian Tertiary Heart Care Centre

International Journal of Environmental Research and Public Health ◽

10.3390/ijerph18189828 ◽

2021 ◽

Vol 18 (18) ◽

pp. 9828

Author(s):

Yi Keng Yong ◽

Nicole Ce Mun Wen ◽

Genieve Ee Chia Yeo ◽

Zhi Xin Chew ◽

Li Li Chan ◽

...

Keyword(s):

Antibiotic Resistance ◽

Resistance Genes ◽

Bacterial Species ◽

Antibiotic Resistance Gene ◽

Meca Gene ◽

Antibiotic Resistance Genes ◽

Health Concern ◽

Bacterial Isolates ◽

Hospital Patients ◽

Virulence Properties

Several bacterial species cause post-operative infections, which has been a critical health concern among hospital patients. Our study in this direction is a much-needed exploratory study that was carried out at the National Heart Institute (IJN) of Malaysia to examine the virulence properties of causative bacteria obtained from postoperative patients. The bacterial isolates and data were provided by the IJN. Antibiotic resistance gene patterns, and the ability to form biofilm were investigated for 127 isolates. Klebsiella pneumoniae (36.2%) was the most common isolate collected, which was followed by Pseudomonas aeruginosa (26%), Staphylococcus aureus (23.6%), Streptococcus spp. (8.7%) and Acinetobacter baumannii (5.5%). There were 49 isolates that showed the presence of multidrug resistance genes. The mecA gene was surprisingly found in methicillin-susceptible S. aureus (MSSA), which also carried the ermA gene from those erythromycin-susceptible strains. The phenotypic antibiotic resistance profiles varied greatly between isolates. Findings from the biofilm assay revealed that 44 of the 127 isolates demonstrated the ability to produce biofilms. Our findings provide insights into the possibility of some of these bacteria surviving under antibiotic stress, and some antibiotic resistance genes being silenced.

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Inventory of Extended-Spectrum-β-Lactamase-Producing Enterobacteriaceae in France as Assessed by a Multicenter Study

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.01911-16 ◽

2016 ◽

Vol 61 (3) ◽

Cited By ~ 30

Author(s):

F. Robin ◽

R. Beyrouthy ◽

S. Bonacorsi ◽

N. Aissa ◽

L. Bret ◽

...

Keyword(s):

Resistance Genes ◽

Multicenter Study ◽

Bacterial Species ◽

Antibiotic Resistance Genes ◽

Clinical Samples ◽

Content Type ◽

Extended Spectrum ◽

Plasmid Analysis ◽

Encoding Genes ◽

Plasmid Replicons

ABSTRACT The objective of this study was to perform an inventory of the extended-spectrum-β-lactamase (ESBL)-producing Enterobacteriaceae isolates responsible for infections in French hospitals and to assess the mechanisms associated with ESBL diffusion. A total of 200 nonredundant ESBL-producing Enterobacteriaceae strains isolated from clinical samples were collected during a multicenter study performed in 18 representative French hospitals. Antibiotic resistance genes were identified by PCR and sequencing experiments. The clonal relatedness between isolates was investigated by the use of the DiversiLab system. ESBL-encoding plasmids were compared by PCR-based replicon typing and plasmid multilocus sequence typing. CTX-M-15, CTX-M-1, CTX-M-14, and SHV-12 were the most prevalent ESBLs (8% to 46.5%). The three CTX-M-type EBSLs were significantly observed in Escherichia coli (37.1%, 24.2%, and 21.8%, respectively), and CTX-M-15 was the predominant ESBL in Klebsiella pneumoniae (81.1%). SHV-12 was associated with ESBL-encoding Enterobacter cloacae strains (37.9%). qnrB, aac(6′)-Ib-cr, and aac(3)-II genes were the main plasmid-mediated resistance genes, with prevalences ranging between 19.5% and 45% according to the ESBL results. Molecular typing did not identify wide clonal diffusion. Plasmid analysis suggested the diffusion of low numbers of ESBL-encoding plasmids, especially in K. pneumoniae and E. cloacae. However, the ESBL-encoding genes were observed in different plasmid replicons according to the bacterial species. The prevalences of ESBL subtypes differ according to the Enterobacteriaceae species. Plasmid spread is a key determinant of this epidemiology, and the link observed between the ESBL-encoding plasmids and the bacterial host explains the differences observed in the Enterobacteriaceae species.

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A Roadmap of The Human Body Resistome

10.21203/rs.3.rs-546142/v1 ◽

2021 ◽

Author(s):

Lucia Maestre-Carballa ◽

Vicente Navarro ◽

Manuel Martinez-Garcia

Keyword(s):

Antibiotic Resistance ◽

Resistance Genes ◽

Human Body ◽

Bacterial Genome ◽

Tetracycline Resistance ◽

The Body ◽

Health Concern ◽

Body Parts ◽

Body Site ◽

Autochthonous Bacteria

Abstract BackgroundIn response to the global antibiotic resistance crisis, efforts have been focused on gaining a better understanding of resistomes (sets of antibiotic resistance genes (ARGs)) and the dispersion of ARGs in nature. A comprehensive metagenomic characterization of the human body resistome is paramount for laying the foundation to develop a better strategy to address this health concern. Here, we study the resistomes of 771 samples from five major body parts of healthy subjects from the Human Microbiome Project (HMP). In line with the One Health concept (WHO), we also investigated the presence of ARGs from the HMP in 272 pristine environments. ResultsOf all the detected HMP genes/proteins (9.17E+07), 40,816 were ARGs showing high interindividual and inter-body-site abundance variability. Nares had the highest ARG abundance (2.18±2.64 ARGs/Mb; ≈5.5 ARG per bacterial genome), while the gut (0.34±0.34 ARGs/Mb; ≈1.3 ARG per bacterial genome), which also showed the highest richness of different ARG types, had the lowest abundance. Fluroquinolone resistance genes were the most abundant antibiotic resistance gene family, followed by MLS or tetracycline resistance genes, depending on the body site. From all the detected ARGs, we found 366 different ARG types, with parC R (fluoroquinolone resistance) being the most abundant in the oral cavity, mprF (peptide antibiotic resistance) in the skin and nares, and tetQ (tetracycline resistance) in the gut and vagina. Most of the ARGs belonged to common bacterial commensals, and many of them were also multidrug resistance genes and were more abundant in the nares and vagina. The total number of ARGs from the HMP data (n=34) detected in pristine environments (266 samples) was negligible, and most of them (73%) were classified as housekeeping genes in autochthonous bacteria having known mutations conferring antibiotic resistance (natural reservoirs). A significant fraction of ARGs (24%) in pristine environments were actually from exogenous contaminants. The detection of identical HMP ARGs in autochthonous bacteria was extremely infrequent (3%). Conclusions Our results comprehensively reveal the resistomes from all body parts and HMP samples that can serve as a baseline for comparison for long-term survey and monitoring of human resistome variations. Finally, our data provide hope, since the spread of common ARGs from the HMP data to pristine environments thus far remains very unlikely.

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Analytical Performance of Multiplexed Screening Test for 10 Antibiotic Resistance Genes from Perianal Swab Samples

Clinical Chemistry ◽

10.1373/clinchem.2015.246371 ◽

2016 ◽

Vol 62 (2) ◽

pp. 353-359 ◽

Cited By ~ 7

Author(s):

G Terrance Walker ◽

Tony J Rockweiler ◽

Rossio K Kersey ◽

Kelly L Frye ◽

Susan R Mitchner ◽

...

Keyword(s):

Antibiotic Resistance ◽

Resistance Gene ◽

Resistance Genes ◽

Test Performance ◽

Health Care Systems ◽

Bacterial Species ◽

Antibiotic Resistance Gene ◽

Antibiotic Resistance Genes ◽

Resistant Bacteria ◽

Gene Test

Abstract BACKGROUND Multiantibiotic-resistant bacteria pose a threat to patients and place an economic burden on health care systems. Carbapenem-resistant bacilli and extended-spectrum β-lactamase (ESBL) producers drive the need to screen infected and colonized patients for patient management and infection control. METHODS We describe a multiplex microfluidic PCR test for perianal swab samples (Acuitas® MDRO Gene Test, OpGen) that detects the vancomycin-resistance gene vanA plus hundreds of gene subtypes from the carbapenemase and ESBL families Klebsiella pneumoniae carbapenemase (KPC), New Delhi metallo-β-lactamase (NDM), Verona integron-mediated metallo-β-lactamase (VIM), imipenemase metallo-β-lactamase (IMP), OXA-23, OXA-48, OXA-51, CTX-M-1, and CTX-M-2, regardless of the bacterial species harboring the antibiotic resistance. RESULTS Analytical test sensitivity per perianal swab is 11–250 CFU of bacteria harboring the antibiotic resistance genes. Test throughput is 182 samples per test run (1820 antibiotic resistance gene family results). We demonstrate reproducible test performance and 100% gene specificity for 265 clinical bacterial organisms harboring a variety of antibiotic resistance genes. CONCLUSIONS The Acuitas MDRO Gene Test is a sensitive, specific, and high-throughput test to screen colonized patients and diagnose infections for several antibiotic resistance genes directly from perianal swab samples, regardless of the bacterial species harboring the resistance genes.

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Tracking the Taxonomy of the GenusBifidobacteriumBased on a Phylogenomic Approach

Applied and Environmental Microbiology ◽

10.1128/aem.02249-17 ◽

2017 ◽

Vol 84 (4) ◽

Cited By ~ 21

Author(s):

Gabriele Andrea Lugli ◽

Christian Milani ◽

Sabrina Duranti ◽

Leonardo Mancabelli ◽

Marta Mangifesta ◽

...

Keyword(s):

New Technologies ◽

Bacterial Species ◽

Bacterial Genome ◽

Bacterial Taxonomy ◽

Genome Sequences ◽

Content Type ◽

Complete Bacterial Genome ◽

Novel Taxa

ABSTRACTFor decades, bacterial taxonomy has been based onin vitromolecular biology techniques and comparison of molecular marker sequences to measure the degree of genetic similarity and deduce phylogenetic relatedness of novel bacterial species to reference microbial taxa. Due to the advent of the genomic era, access to complete bacterial genome contents has become easier, thereby presenting the opportunity to precisely investigate the overall genetic diversity of microorganisms. Here, we describe a high-accuracy phylogenomic approach to assess the taxonomy of members of the genusBifidobacteriumand identify apparent misclassifications in current bifidobacterial taxonomy. The developed method was validated by the classification of seven novel taxa belonging to the genusBifidobacteriumby employing their overall genetic content. The results of this study demonstrate the potential of this whole-genome approach to become the gold standard for phylogenomics-based taxonomic classification of bacteria.IMPORTANCENowadays, next-generation sequencing has given access to genome sequences of the currently known bacterial taxa. The public databases constructed by means of these new technologies allowed comparison of genome sequences between microorganisms, providing information to perform genomic, phylogenomic, and evolutionary analyses. In order to avoid misclassifications in the taxonomy of novel bacterial isolates, new (bifido)bacterial taxons should be validated with a phylogenomic assessment like the approach presented here.

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Characterization of Extended-Spectrum β-Lactamase-Producing and AmpC β-Lactamase-Producing Enterobacterales Isolated from Companion Animals in Korea

Antibiotics ◽

10.3390/antibiotics10030249 ◽

2021 ◽

Vol 10 (3) ◽

pp. 249

Author(s):

Se Ra Shin ◽

Seong Mi Noh ◽

Woo Kyung Jung ◽

Sook Shin ◽

Young Kyung Park ◽

...

Keyword(s):

Resistance Genes ◽

Genetic Relatedness ◽

Bacterial Species ◽

Klebsiella Oxytoca ◽

Companion Animals ◽

E Coli ◽

South Korean ◽

Extended Spectrum ◽

Single Clone

The emergence of extended-spectrum cephalosporin (ESC)-resistant Gram-negative bacteria is of great concern in both human and veterinary medicine. The aim of this study was to investigate ESC-resistant bacterial isolates from companion animals in South Korea between 2017 and 2019. Isolates with ESC resistance genes, which were identified by PCR, were assessed for genetic relatedness by multi-locus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE). In total, 91 ESC-resistant Escherichia coli, Klebsiella spp., Serratia spp., and Enterobacter cloacae isolates harbored the blaTEM gene. Among other ESC resistance genes, blaCTX-M-15, blaCIT, and blaCTX-M-55 were predominantly detected in E. coli isolates, whereas blaSHV and blaDHA were more frequently detected in Klebsiella pneumoniae isolates. In addition, all blaEBC-positive isolates were classified as E. cloacae. From the MLST results, blaCTX-M-9-carrying ST131, blaCIT-carrying ST405, and blaCTX-M-1-carrying ST3285 strains were dominant among E. coli isolates. ST273 and ST275 strains harboring blaSHV were frequently detected in K. pneumoniae isolates. Various sequence types were obtained in E. cloacae and Klebsiella oxytoca isolates. All isolates demonstrated unique PFGE profiles (<57–98% similarity) and were unlikely to be derived from a single clone. The present study reveals the presence and wide genetic distribution of ESC-resistant bacterial species in South Korean companion animals.

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Impact of target site mutations and plasmid associated resistance genes acquisition on resistance of Acinetobacter baumannii to fluoroquinolones

Scientific Reports ◽

10.1038/s41598-021-99230-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Mostafa Ahmed Mohammed ◽

Mohammed T. A. Salim ◽

Bahaa E. Anwer ◽

Khaled M. Aboshanab ◽

Mohammad M. Aboulwafa

Keyword(s):

Resistance Genes ◽

Antimicrobial Agents ◽

Bacterial Species ◽

Resistance Mechanism ◽

Resistance Mechanisms ◽

Target Site ◽

Resistant Isolate ◽

Drug Resistant ◽

Site Mutation ◽

Encoding Genes

AbstractAmong bacterial species implicated in hospital-acquired infections are the emerging Pan-Drug Resistant (PDR) and Extensively Drug-Resistant (XDR) Acinetobacter (A.) baumannii strains as they are difficult to eradicate. From 1600 clinical specimens, only 100 A. baumannii isolates could be recovered. A high prevalence of ≥ 78% resistant isolates was recorded for the recovered isolates against a total of 19 tested antimicrobial agents. These isolates could be divided into 12 profiles according to the number of antimicrobial agents to which they were resistant. The isolates were assorted as XDR (68; 68%), Multi-Drug Resistant (MDR: 30; 30%), and PDR (2; 2%). Genotypically, the isolates showed three major clusters with similarities ranging from 10.5 to 97.8% as revealed by ERIC-PCR technique. As a resistance mechanism to fluoroquinolones (FQs), target site mutation analyses in gyrA and parC genes amplified from twelve selected A. baumannii isolates and subjected to sequencing showed 12 profiles. The selected isolates included two CIP-susceptible ones, these showed the wild-type profile of being have no mutations. For the ten selected CIP-resistant isolates, 9 of them (9/10; 90%) had 1 gyrA/1 parC mutations (Ser 81 → Leu mutation for gyrA gene and Ser 84 → Leu mutation for parC gene). The remaining CIP-resistant isolate (1/10; 10%) had 0 gyrA/1 parC mutation (Ser 84 → Leu mutation for parC gene). Detection of plasmid-associated resistance genes revealed that the 86 ciprofloxacin-resistant isolates carry qnrA (66.27%; 57/86), qnrS (70.93%; 61/86), aac (6')-Ib-cr (52.32%; 45/86), oqxA (73.25%; 63/86) and oqxB (39.53%; 34/86), while qepA and qnrB were undetected in these isolates. Different isolates were selected from profiles 1, 2, and 3 and qnrS, acc(6,)-ib-cr, oqxA, and oqxB genes harbored by these isolates were amplified and sequenced. The BLAST results revealed that the oqxA and oqxB sequences were not identified previously in A. baumannii but they were identified in Klebsiella aerogenes strain NCTC9793 and Klebsiella pneumoniae, respectively. On the other hand, the sequence of qnrS, and acc(6,)-ib-cr showed homology to those of A. baumannii. MDR, XDR, and PDR A. baumannii isolates are becoming prevalent in certain hospitals. Chromosomal mutations in the sequences of GyrA and ParC encoding genes and acquisition of PAFQR encoding genes (up to five genes per isolate) are demonstrated to be resistance mechanisms exhibited by fluoroquinolones resistant A. baumannii isolates. It is advisable to monitor the antimicrobial resistance profiles of pathogens causing nosocomial infections and properly apply and update antibiotic stewardship in hospitals and outpatients to control infectious diseases and prevent development of the microbial resistance to antimicrobial agents.

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Bacterial transformation buffers environmental fluctuations through the reversible integration of mobile genetic elements

10.1101/557462 ◽

2019 ◽

Author(s):

Gabriel Carvalho ◽

David Fouchet ◽

Gonché Danesh ◽

Anne-Sophie Godeux ◽

Maria-Halima Laaberki ◽

...

Keyword(s):

Resistance Genes ◽

Bacterial Genome ◽

Antibiotic Resistance Genes ◽

Mobile Genetic Elements ◽

Host Cells ◽

Transformation Rate ◽

Bacterial Cells ◽

Bacterial Populations ◽

Genetic Elements ◽

Intermediate Transformation

AbstractHorizontal gene transfer (HGT) is known to promote the spread of genes in bacterial communities, which is of primary importance to human health when these genes provide resistance to antibiotics. Among the main HGT mechanisms, natural transformation stands out as being widespread and encoded by the bacterial core genome. From an evolutionary perspective, transformation is often viewed as a mean to generate genetic diversity and mixing within bacterial populations. However, another recent paradigm proposes that its main evolutionary function would be to cure bacterial genomes from their parasitic mobile genetic elements (MGEs). Here, we propose to combine these two seemingly opposing points of view because MGEs, although costly for bacterial cells, can carry functions that are point-in-time beneficial to bacteria under stressful conditions (e.g. antibiotic resistance genes under antibiotic exposure). Using computational modeling, we show that, in stochastic environments (unpredictable stress exposure), an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes but costly for the replication of host cells. By ensuring such reversible genetic diversification (acquisition then removal of MGEs), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, which would explain its striking conservation.

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Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements

mBio ◽

10.1128/mbio.02443-19 ◽

2020 ◽

Vol 11 (2) ◽

Cited By ~ 2

Author(s):

Gabriel Carvalho ◽

David Fouchet ◽

Gonché Danesh ◽

Anne-Sophie Godeux ◽

Maria-Halima Laaberki ◽

...

Keyword(s):

Horizontal Gene Transfer ◽

Resistance Genes ◽

Natural Transformation ◽

Bacterial Genome ◽

Mobile Genetic Elements ◽

Bacterial Populations ◽

Genetic Elements ◽

Intermediate Transformation ◽

Bacterial Fitness

ABSTRACT Horizontal gene transfer (HGT) promotes the spread of genes within bacterial communities. Among the HGT mechanisms, natural transformation stands out as being encoded by the bacterial core genome. Natural transformation is often viewed as a way to acquire new genes and to generate genetic mixing within bacterial populations. Another recently proposed function is the curing of bacterial genomes of their infectious parasitic mobile genetic elements (MGEs). Here, we propose that these seemingly opposing theoretical points of view can be unified. Although costly for bacterial cells, MGEs can carry functions that are at points in time beneficial to bacteria under stressful conditions (e.g., antibiotic resistance genes). Using computational modeling, we show that, in stochastic environments, an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes, although these MGEs are costly for host cell replication. Based on this dual function (MGE acquisition and removal), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, and this would explain its striking conservation. IMPORTANCE Natural transformation is the acquisition, controlled by bacteria, of extracellular DNA and is one of the most common mechanisms of horizontal gene transfer, promoting the spread of resistance genes. However, its evolutionary function remains elusive, and two main roles have been proposed: (i) the new gene acquisition and genetic mixing within bacterial populations and (ii) the removal of infectious parasitic mobile genetic elements (MGEs). While the first one promotes genetic diversification, the other one promotes the removal of foreign DNA and thus genome stability, making these two functions apparently antagonistic. Using a computational model, we show that intermediate transformation rates, commonly observed in bacteria, allow the acquisition then removal of MGEs. The transient acquisition of costly MGEs with resistance genes maximizes bacterial fitness in environments with stochastic stress exposure. Thus, transformation would ensure both a strong dynamic of the bacterial genome in the short term and its long-term stabilization.

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