Plasmid- and strain-specific factors drive variation in ESBL-plasmid spread in vitro and in vivo

Benz, Fabienne; Huisman, Jana S.; Bakkeren, Erik; Herter, Joana Anuschka; Stadler, Tanja; Ackermann, Martin; Diard, Médéric; Egli, Adrian; Hall, Alex R.; Hardt, Wolf‐Dietrich; Bonhoeffer, Sebastian

doi:10.1038/s41396-020-00819-4

Cited by 79 publications

(91 citation statements)

References 102 publications

(73 reference statements)

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“…Conjugative plasmids, which can mediate their own horizontal transmission, are important vectors of horizontal gene transfer in prokaryotes and a key source of microbial genetic diversity. Many conjugative plasmids carry accessory genes, which can confer resistance to heavy metals or antibiotics [1, 2]. Understanding plasmid dynamics is therefore not only important to understanding bacterial ecology and evolution in general, but also to predict the rise of antibiotic resistance.…”

Section: Introductionmentioning

confidence: 99%

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

Igler

Schwyter

Gehrig

et al. 2021

Preprint

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Antibiotic resistance spread via plasmids is a serious threat to successful treatment and makes understanding plasmid transfer in nature crucial to preventing the global rise of antibiotic resistance. However, plasmid dynamics have so far neglected one omnipresent factor: active prophages (phages that are integrated into the bacterial genome), whose activation can kill co-occurring bacteria. To investigate how prophages influence the spread of a multi-drug resistant plasmid, we combined experiments and mathematical modelling. Using E. coli, prophage lambda and the plasmid Rp4 we find that prophages clearly limit the spread of conjugative plasmids. This effect was even more pronounced when we studied this interaction in a phage-friendly environment that favoured phage adsorption. Our empirically parameterized model reproduces experimental dynamics in some environments well, but fails to predict them in others, suggesting more complex interactions between plasmid and prophage infection dynamics. Varying phage and plasmid infection parameters over an empirically realistic range suggests that plasmids can overcome the negative impact of prophages through high conjugation rates. Overall, we find that the presence of prophages introduces an additional death rate for plasmid carriers, the magnitude of which is determined in non-trivial ways by the environment, the phage and the plasmid.

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Section: Introductionmentioning

confidence: 99%

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

Igler

Schwyter

Gehrig

et al. 2021

Preprint

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“…The IncI1-complex are widespread in Enterobacteriaceae and have been reported to be the major driver of AR in Salmonella and E. coli . Our understanding of their mode of transfer and AR evolution have been limited to studies on their prevalence, mating experiments and in vivo challenge with mice 21, 30, 31 . Fischer et al 32 showed that E. coli populations in broiler chickens acquired β-lactam resistance after 4-days old broiler chicks were gavaged with an E. coli strain carrying blaCTX-M-1 on an IncI1 plasmid.…”

Section: Discussionmentioning

confidence: 99%

“…?ES"7(%0"EM".NO:"5)+"E"():&'%(*):" =.,992&4&)%5'8"+5%5"K^".,992&4&)%5'8"?512&"E>! "?0&"():&'%(*):"7&'&"9'&:&)%"()"*) 28 E. coli was the major IncI1 reservoir in broiler chicks. The application of proximityligation method (Hi-C) has improved the assembly of metagenomes and made it possible to detect plasmid-host associations 21 .…”

mentioning

confidence: 99%

“…; https://doi.org/10.1101/2021.02.25.432983 doi: bioRxiv preprint18The IncI1-complex are widespread in Enterobacteriaceae and have been reported to be the major driver of AR in Salmonella and E. coli. Our understanding of their mode of transfer and AR evolution have been limited to studies on their prevalence, mating experiments and in vivo challenge with mice 20,28,29 .Fischer et al 30 showed that E. coli populations in broiler chickens acquired â-lactam resistance after 4-days old broiler chicks were gavaged with an E. coli strain carrying blaCTX-M-1 on an IncI1 plasmid. In a twin pair experiment, Hagbo et al 31 revealed that IncI1 carrying blaCMY-2, ColE1 and P1 bacteriophage are frequently transferred between microbiota present in pre-term infant gut.…”

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confidence: 99%

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Gene flux and acid-imposed selection are the main drivers of antimicrobial resistance in broiler chicks infected withSalmonella entericaserovar Heidelberg

Oladeine

Abdo

et al. 2021

Preprint

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Salmonella enterica serovar Heidelberg (SH) is one of the prolific serovars causing poultry-associated food-borne illness in the world. Their ability to cause invasive infections and their promiscuity to plasmids that confer multidrug resistance to antibiotics of human health importance makes them a public health threat. Although, horizontal gene transfer (HGT) is recognized as the major mechanism used by Salmonella for acquiring antimicrobial resistance (AR) and virulence genes, the biology behind acquisition of new genes in SH is still unknown. In this study, we show that one day old broiler chicks challenged orally or via the cloaca with an antibiotic susceptible SH strain and raised without antibiotics carried susceptible and multidrug resistance SH strains 14 days after challenge. SH infection perturbed the bacterial community of broiler chicks and orally challenged chicks acquired AR at a higher rate than chicks challenged through the cloaca. Furthermore, SH strains lost and gained new genes, while some inverted their chromosome after colonizing the gut of broiler chicks. The acquisition of IncI1 plasmid multilocus sequence type 26 (pST26) from commensal Escherichia coli population present in the gut of broiler chicks conferred multidrug resistance phenotype to SH recipients and carriage of pST26 increased the fitness of SH under acidic selection pressure. Our results suggest that HGT shapes the evolution of AR in SH and that antibiotic use reduction alone is insufficient to limit AR plasmid transfer from commensal bacteria to Salmonella.

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“…Several factors play a role in the ability of plasmids to be transferred between bacteria. For instance, incompatibility restriction, host genetics, and strain-specific factors can influence the transfer of plasmids [ 38 , 74 , 75 ]. In this study, we investigated a total of 18 plasmid incompatibility groups in all E. coli isolates.…”

Section: Discussionmentioning

confidence: 99%

Bacteria Broadly-Resistant to Last Resort Antibiotics Detected in Commercial Chicken Farms

et al. 2021

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Resistance to last resort antibiotics in bacteria is an emerging threat to human and animal health. It is important to identify the source of these antimicrobial resistant (AMR) bacteria that are resistant to clinically important antibiotics and evaluate their potential transfer among bacteria. The objectives of this study were to (i) detect bacteria resistant to colistin, carbapenems, and β-lactams in commercial poultry farms, (ii) characterize phylogenetic and virulence markers of E. coli isolates to potentiate virulence risk, and (iii) assess potential transfer of AMR from these isolates via conjugation. Ceca contents from laying hens from conventional cage (CC) and cage-free (CF) farms at three maturity stages were randomly sampled and screened for extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae, carbapenem-resistant Acinetobacter (CRA), and colistin resistant Escherichia coli (CRE) using CHROMagar™ selective media. We found a wide-spread abundance of CRE in both CC and CF hens across all three maturity stages. Extraintestinal pathogenic Escherichia coli phylogenetic groups B2 and D, as well as plasmidic virulence markers iss and iutA, were widely associated with AMR E. coli isolates. ESBL-producing Enterobacteriaceae were uniquely detected in the early lay period of both CC and CF, while multidrug resistant (MDR) Acinetobacter were found in peak and late lay periods of both CC and CF. CRA was detected in CF hens only. blaCMY was detected in ESBL-producing E. coli in CC and CF and MDR Acinetobacter spp. in CC. Finally, the blaCMY was shown to be transferrable via an IncK/B plasmid in CC. The presence of MDR to the last-resort antibiotics that are transferable between bacteria in food-producing animals is alarming and warrants studies to develop strategies for their mitigation in the environment.

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Plasmid- and strain-specific factors drive variation in ESBL-plasmid spread in vitro and in vivo

Cited by 79 publications

References 102 publications

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

Conjugative plasmid transfer is limited by prophages but can be overcome by high conjugation rates

Gene flux and acid-imposed selection are the main drivers of antimicrobial resistance in broiler chicks infected withSalmonella entericaserovar Heidelberg

Bacteria Broadly-Resistant to Last Resort Antibiotics Detected in Commercial Chicken Farms

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