Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production
Colistin is classified as a high-priority critical antimicrobial by the World Health Organization (WHO). A better understanding of the biological cost imposed by <i>mcr</i>-plasmids is paramount to comprehending their spread and may facilitate the decision about the ban of colistin in li...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-10-01
|
| Series: | Antibiotics |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-6382/11/10/1356 |
| _version_ | 1797475872797622272 |
|---|---|
| author | Tiago Lima Dina Loureiro Ana Henriques Fernando Ramos Constança Pomba Sara Domingues Gabriela Jorge da Silva |
| author_facet | Tiago Lima Dina Loureiro Ana Henriques Fernando Ramos Constança Pomba Sara Domingues Gabriela Jorge da Silva |
| author_sort | Tiago Lima |
| collection | DOAJ |
| description | Colistin is classified as a high-priority critical antimicrobial by the World Health Organization (WHO). A better understanding of the biological cost imposed by <i>mcr</i>-plasmids is paramount to comprehending their spread and may facilitate the decision about the ban of colistin in livestock. This study aimed to assess the prevalence of <i>mcr</i> and ESBL genes from 98 <i>Escherichia coli</i> and 142 <i>Salmonella enterica</i> isolates from food-producing animals and the impact of the <i>mcr-1</i> acquisition on bacterial fitness. Only <i>mcr-1</i> was identified by multiplex PCR (<i>mcr-1</i> to <i>mcr</i>-<i>10</i>) in 15.3% of <i>E. coli</i>. Colistin MICs ranged between 8–32 mg/L. In four isolates, <i>bla</i><sub><i>TEM-1</i></sub>, <i>bla</i><sub><i>CTX-M-1</i></sub>, and <i>bla</i><sub><i>CTX-M-15</i></sub> co-existed with <i>mcr-1</i>. The IncH12, IncHI1, IncP, IncN, and IncI plasmids were transferred by conjugation to <i>E. coli</i> J53 at frequencies of 10<sup>−7</sup> to 10<sup>−2</sup> cells/recipient. Growth kinetics assays showed that transconjugants had a significantly lower growth rate than the recipient (<i>p</i> < 0.05), and transconjugants’ average growth rate was higher in the absence than in the presence of colistin (1.66 versus 1.32 (<i>p</i> = 0.0003)). Serial transfer assay during 10 days demonstrated that plasmid retention ranged from complete loss to full retention. Overall, <i>mcr-1</i>-bearing plasmids impose a fitness cost, but the loss of plasmids is highly variable, suggesting that other factors beyond colistin pressure regulate the plasmid maintenance in a bacterial population, and colistin withdrawal will not completely lead to a decrease of <i>mcr-1</i> levels. |
| first_indexed | 2024-03-09T20:50:56Z |
| format | Article |
| id | doaj.art-be713c002ede48c29fc0c33c5b6c7fa5 |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-09T20:50:56Z |
| publishDate | 2022-10-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-be713c002ede48c29fc0c33c5b6c7fa52023-11-23T22:35:05ZengMDPI AGAntibiotics2079-63822022-10-011110135610.3390/antibiotics11101356Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal ProductionTiago Lima0Dina Loureiro1Ana Henriques2Fernando Ramos3Constança Pomba4Sara Domingues5Gabriela Jorge da Silva6Faculty of Pharmacy, University of Coimbra, 3000-458 Coimbra, PortugalALS-Controlvet, 3460-070 Tondela, PortugalALS-Controlvet, 3460-070 Tondela, PortugalFaculty of Pharmacy, University of Coimbra, 3000-458 Coimbra, PortugalCentre for Interdisciplinary Research in Animal Health, Laboratory of Antibiotic Resistance, CIISA, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, PortugalFaculty of Pharmacy, University of Coimbra, 3000-458 Coimbra, PortugalFaculty of Pharmacy, University of Coimbra, 3000-458 Coimbra, PortugalColistin is classified as a high-priority critical antimicrobial by the World Health Organization (WHO). A better understanding of the biological cost imposed by <i>mcr</i>-plasmids is paramount to comprehending their spread and may facilitate the decision about the ban of colistin in livestock. This study aimed to assess the prevalence of <i>mcr</i> and ESBL genes from 98 <i>Escherichia coli</i> and 142 <i>Salmonella enterica</i> isolates from food-producing animals and the impact of the <i>mcr-1</i> acquisition on bacterial fitness. Only <i>mcr-1</i> was identified by multiplex PCR (<i>mcr-1</i> to <i>mcr</i>-<i>10</i>) in 15.3% of <i>E. coli</i>. Colistin MICs ranged between 8–32 mg/L. In four isolates, <i>bla</i><sub><i>TEM-1</i></sub>, <i>bla</i><sub><i>CTX-M-1</i></sub>, and <i>bla</i><sub><i>CTX-M-15</i></sub> co-existed with <i>mcr-1</i>. The IncH12, IncHI1, IncP, IncN, and IncI plasmids were transferred by conjugation to <i>E. coli</i> J53 at frequencies of 10<sup>−7</sup> to 10<sup>−2</sup> cells/recipient. Growth kinetics assays showed that transconjugants had a significantly lower growth rate than the recipient (<i>p</i> < 0.05), and transconjugants’ average growth rate was higher in the absence than in the presence of colistin (1.66 versus 1.32 (<i>p</i> = 0.0003)). Serial transfer assay during 10 days demonstrated that plasmid retention ranged from complete loss to full retention. Overall, <i>mcr-1</i>-bearing plasmids impose a fitness cost, but the loss of plasmids is highly variable, suggesting that other factors beyond colistin pressure regulate the plasmid maintenance in a bacterial population, and colistin withdrawal will not completely lead to a decrease of <i>mcr-1</i> levels.https://www.mdpi.com/2079-6382/11/10/1356colistin resistance<i>mcr-1</i>CTX-Mfitness costconjugationlivestock |
| spellingShingle | Tiago Lima Dina Loureiro Ana Henriques Fernando Ramos Constança Pomba Sara Domingues Gabriela Jorge da Silva Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production Antibiotics colistin resistance <i>mcr-1</i> CTX-M fitness cost conjugation livestock |
| title | Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production |
| title_full | Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production |
| title_fullStr | Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production |
| title_full_unstemmed | Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production |
| title_short | Occurrence and Biological Cost of <i>mcr-1</i>-Carrying Plasmids Co-harbouring Beta-Lactamase Resistance Genes in Zoonotic Pathogens from Intensive Animal Production |
| title_sort | occurrence and biological cost of i mcr 1 i carrying plasmids co harbouring beta lactamase resistance genes in zoonotic pathogens from intensive animal production |
| topic | colistin resistance <i>mcr-1</i> CTX-M fitness cost conjugation livestock |
| url | https://www.mdpi.com/2079-6382/11/10/1356 |
| work_keys_str_mv | AT tiagolima occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT dinaloureiro occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT anahenriques occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT fernandoramos occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT constancapomba occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT saradomingues occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction AT gabrielajorgedasilva occurrenceandbiologicalcostofimcr1icarryingplasmidscoharbouringbetalactamaseresistancegenesinzoonoticpathogensfromintensiveanimalproduction |