Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively
Abstract Background The ability of bacteria to acquire resistance to antibiotics relies to a large extent on their capacity for genome modification. Prokaryotic genomes are highly plastic and can utilize horizontal gene transfer, point mutations, and gene deletions or amplifications to realize genom...
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BMC
2018-12-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-018-5353-y |
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| author | Marloes Hoeksema Martijs J. Jonker Keshia Bel Stanley Brul Benno H. ter Kuile |
| author_facet | Marloes Hoeksema Martijs J. Jonker Keshia Bel Stanley Brul Benno H. ter Kuile |
| author_sort | Marloes Hoeksema |
| collection | DOAJ |
| description | Abstract Background The ability of bacteria to acquire resistance to antibiotics relies to a large extent on their capacity for genome modification. Prokaryotic genomes are highly plastic and can utilize horizontal gene transfer, point mutations, and gene deletions or amplifications to realize genome expansion and rearrangements. The contribution of point mutations to de novo acquisition of antibiotic resistance is well-established. In this study, the internal genome rearrangement of Escherichia coli during to de novo acquisition of antibiotic resistance was investigated using whole-genome sequencing. Results Cells were made resistant to one of the four antibiotics and subsequently to one of the three remaining. This way the initial genetic rearrangements could be documented together with the effects of an altered genetic background on subsequent development of resistance. A DNA fragment including ampC was amplified by a factor sometimes exceeding 100 as a result of exposure to amoxicillin. Excision of prophage e14 was observed in many samples with a double exposure history, but not in cells exposed to a single antibiotic, indicating that the activation of the SOS stress response alone, normally the trigger for excision, was not sufficient to cause excision of prophage e14. Partial deletion of clpS and clpA occurred in strains exposed to enrofloxacin and tetracycline. Other deletions were observed in some strains, but not in replicates with the exact same exposure history. Various insertion sequence transpositions correlated with exposure to specific antibiotics. Conclusions Many of the genome rearrangements have not been reported before to occur during resistance development. The observed correlation between genome rearrangements and specific antibiotic pressure, as well as their presence in independent replicates indicates that these events do not occur randomly. Taken together, the observed genome rearrangements illustrate the plasticity of the E. coli genome when exposed to antibiotic stress. |
| first_indexed | 2024-12-13T13:12:35Z |
| format | Article |
| id | doaj.art-368326d48e1e49358c3f91404a1d877c |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-13T13:12:35Z |
| publishDate | 2018-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-368326d48e1e49358c3f91404a1d877c2022-12-21T23:44:39ZengBMCBMC Genomics1471-21642018-12-0119111210.1186/s12864-018-5353-yGenome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successivelyMarloes Hoeksema0Martijs J. Jonker1Keshia Bel2Stanley Brul3Benno H. ter Kuile4Laboratory for Molecular Biology and Microbial Food Safety, Swammerdam Institute for Life Sciences, University of AmsterdamRNA Biology & Applied Bioinformatics, Swammerdam Institute for Life Sciences, University of AmsterdamLaboratory for Molecular Biology and Microbial Food Safety, Swammerdam Institute for Life Sciences, University of AmsterdamLaboratory for Molecular Biology and Microbial Food Safety, Swammerdam Institute for Life Sciences, University of AmsterdamLaboratory for Molecular Biology and Microbial Food Safety, Swammerdam Institute for Life Sciences, University of AmsterdamAbstract Background The ability of bacteria to acquire resistance to antibiotics relies to a large extent on their capacity for genome modification. Prokaryotic genomes are highly plastic and can utilize horizontal gene transfer, point mutations, and gene deletions or amplifications to realize genome expansion and rearrangements. The contribution of point mutations to de novo acquisition of antibiotic resistance is well-established. In this study, the internal genome rearrangement of Escherichia coli during to de novo acquisition of antibiotic resistance was investigated using whole-genome sequencing. Results Cells were made resistant to one of the four antibiotics and subsequently to one of the three remaining. This way the initial genetic rearrangements could be documented together with the effects of an altered genetic background on subsequent development of resistance. A DNA fragment including ampC was amplified by a factor sometimes exceeding 100 as a result of exposure to amoxicillin. Excision of prophage e14 was observed in many samples with a double exposure history, but not in cells exposed to a single antibiotic, indicating that the activation of the SOS stress response alone, normally the trigger for excision, was not sufficient to cause excision of prophage e14. Partial deletion of clpS and clpA occurred in strains exposed to enrofloxacin and tetracycline. Other deletions were observed in some strains, but not in replicates with the exact same exposure history. Various insertion sequence transpositions correlated with exposure to specific antibiotics. Conclusions Many of the genome rearrangements have not been reported before to occur during resistance development. The observed correlation between genome rearrangements and specific antibiotic pressure, as well as their presence in independent replicates indicates that these events do not occur randomly. Taken together, the observed genome rearrangements illustrate the plasticity of the E. coli genome when exposed to antibiotic stress.http://link.springer.com/article/10.1186/s12864-018-5353-yGenome rearrangementde novo resistanceGene amplificationProphage |
| spellingShingle | Marloes Hoeksema Martijs J. Jonker Keshia Bel Stanley Brul Benno H. ter Kuile Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively BMC Genomics Genome rearrangement de novo resistance Gene amplification Prophage |
| title | Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| title_full | Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| title_fullStr | Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| title_full_unstemmed | Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| title_short | Genome rearrangements in Escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| title_sort | genome rearrangements in escherichia coli during de novo acquisition of resistance to a single antibiotic or two antibiotics successively |
| topic | Genome rearrangement de novo resistance Gene amplification Prophage |
| url | http://link.springer.com/article/10.1186/s12864-018-5353-y |
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