High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan
A total of seventy VanA-type vancomycin-resistant enterococci (VRE) isolates obtained in Taiwan in the early 2000s were retrospectively characterized. Forty isolates were obtained from human patients and thirty from livestock. Of these VRE isolates, twenty-three (57.5%) of the human VRE and thirty (...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-11-01
|
| Series: | Antibiotics |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2079-6382/12/12/1668 |
| _version_ | 1797382231262494720 |
|---|---|
| author | Haruyoshi Tomita Jang-Jih Lu Yasuyoshi Ike |
| author_facet | Haruyoshi Tomita Jang-Jih Lu Yasuyoshi Ike |
| author_sort | Haruyoshi Tomita |
| collection | DOAJ |
| description | A total of seventy VanA-type vancomycin-resistant enterococci (VRE) isolates obtained in Taiwan in the early 2000s were retrospectively characterized. Forty isolates were obtained from human patients and thirty from livestock. Of these VRE isolates, twenty-three (57.5%) of the human VRE and thirty (100%) of the livestock VRE were <i>Enterococcus faecalis</i>, and the remaining seventeen (42.5%) of the human VRE were <i>E. faecium</i>. Of the 53 <i>E. faecalis</i> isolates, twenty-two (96%) of the human VRE and thirty (100%) of the livestock VRE exhibited a high level of resistance to vancomycin and sensitivity to teicoplanin. They also had three amino acid substitutions in the N-terminal region of the deduced VanS sequence. The vancomycin resistance of all of the 22 human isolates, and 20 of the 30 livestock isolates, transferred to <i>E. faecalis</i> FA2-2 at a frequency of 10<sup>−5</sup> to 10<sup>−3</sup> per donor cell in broth. Each of the transconjugants responded to <i>E. faecalis</i> pheromone (i.e., <i>E. faecalis</i> FA2-2 culture filtrate), indicating that the conjugative plasmids were pheromone-responsive plasmids. Three of the conjugative plasmids originated from human isolates, and five plasmids from livestock isolates were corresponded and classified as type A plasmid. Two plasmids originated from human isolates and six plasmids from livestock isolates were corresponded and classified as type B plasmid. <i>E. faecalis</i> FA2-2 containing either the type A or type B plasmid responded to the synthetic pheromone cAD1. The type A and type B plasmids transferred between <i>E. faecalis</i> FA2-2 and JH2SS at a frequency of about 10<sup>−2</sup> per donor cell and conferred vancomycin, bacitracin, and erythromycin resistances. The complete DNA sequence of the representative type A plasmid pTW9 (85,068 bp) showed that the plasmid carried a Tn<i>1546</i>-like element encoding <i>vanA</i>-type resistance, erythromycin resistance (<i>ermB</i>), and bacitracin resistance (<i>bcrABDR</i>). The plasmid contained the regulatory region found in the pheromone-responsive plasmid and encoded the genes <i>traA</i>, <i>traD</i> and <i>iad1</i>, which are the key negative regulatory elements, and <i>traE1</i>, a key positive regulator of plasmid pAD1, indicating that plasmid pTW9 was pAD1-type pheromone-responsive plasmid. PFGE analysis of SmaI-digested chromosomal DNAs showed that several <i>E. faecalis</i> strains harboring an identical type A pheromone-responsive plasmid were indistinguishable, and that these were identified both in human and livestock isolates, indicating the transmissions of the VRE strains between livestock and humans. These data showed that the multiple-drug-resistant pheromone-responsive conjugative plasmids have been widely spread in both human and livestock VRE, and there was high potential for transfers of VRE from food animals to humans in Taiwan in the early 2000s. |
| first_indexed | 2024-03-08T21:03:26Z |
| format | Article |
| id | doaj.art-5037813c16d24bd093afeab50c360122 |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-08T21:03:26Z |
| publishDate | 2023-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-5037813c16d24bd093afeab50c3601222023-12-22T13:47:50ZengMDPI AGAntibiotics2079-63822023-11-011212166810.3390/antibiotics12121668High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in TaiwanHaruyoshi Tomita0Jang-Jih Lu1Yasuyoshi Ike2Department of Bacteriology, Gunma University Graduate School of Medicine, Maebashi 371-8511, Gunma, JapanDepartment of Laboratory Medicine, Linkou Chang Gung Memorial Hospital, Taoyuan 333, TaiwanDepartment of Bacteriology, Gunma University Graduate School of Medicine, Maebashi 371-8511, Gunma, JapanA total of seventy VanA-type vancomycin-resistant enterococci (VRE) isolates obtained in Taiwan in the early 2000s were retrospectively characterized. Forty isolates were obtained from human patients and thirty from livestock. Of these VRE isolates, twenty-three (57.5%) of the human VRE and thirty (100%) of the livestock VRE were <i>Enterococcus faecalis</i>, and the remaining seventeen (42.5%) of the human VRE were <i>E. faecium</i>. Of the 53 <i>E. faecalis</i> isolates, twenty-two (96%) of the human VRE and thirty (100%) of the livestock VRE exhibited a high level of resistance to vancomycin and sensitivity to teicoplanin. They also had three amino acid substitutions in the N-terminal region of the deduced VanS sequence. The vancomycin resistance of all of the 22 human isolates, and 20 of the 30 livestock isolates, transferred to <i>E. faecalis</i> FA2-2 at a frequency of 10<sup>−5</sup> to 10<sup>−3</sup> per donor cell in broth. Each of the transconjugants responded to <i>E. faecalis</i> pheromone (i.e., <i>E. faecalis</i> FA2-2 culture filtrate), indicating that the conjugative plasmids were pheromone-responsive plasmids. Three of the conjugative plasmids originated from human isolates, and five plasmids from livestock isolates were corresponded and classified as type A plasmid. Two plasmids originated from human isolates and six plasmids from livestock isolates were corresponded and classified as type B plasmid. <i>E. faecalis</i> FA2-2 containing either the type A or type B plasmid responded to the synthetic pheromone cAD1. The type A and type B plasmids transferred between <i>E. faecalis</i> FA2-2 and JH2SS at a frequency of about 10<sup>−2</sup> per donor cell and conferred vancomycin, bacitracin, and erythromycin resistances. The complete DNA sequence of the representative type A plasmid pTW9 (85,068 bp) showed that the plasmid carried a Tn<i>1546</i>-like element encoding <i>vanA</i>-type resistance, erythromycin resistance (<i>ermB</i>), and bacitracin resistance (<i>bcrABDR</i>). The plasmid contained the regulatory region found in the pheromone-responsive plasmid and encoded the genes <i>traA</i>, <i>traD</i> and <i>iad1</i>, which are the key negative regulatory elements, and <i>traE1</i>, a key positive regulator of plasmid pAD1, indicating that plasmid pTW9 was pAD1-type pheromone-responsive plasmid. PFGE analysis of SmaI-digested chromosomal DNAs showed that several <i>E. faecalis</i> strains harboring an identical type A pheromone-responsive plasmid were indistinguishable, and that these were identified both in human and livestock isolates, indicating the transmissions of the VRE strains between livestock and humans. These data showed that the multiple-drug-resistant pheromone-responsive conjugative plasmids have been widely spread in both human and livestock VRE, and there was high potential for transfers of VRE from food animals to humans in Taiwan in the early 2000s.https://www.mdpi.com/2079-6382/12/12/1668VREVanA<i>E. faecalis</i>pheromone-responsive plasmidTaiwanlivestock |
| spellingShingle | Haruyoshi Tomita Jang-Jih Lu Yasuyoshi Ike High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan Antibiotics VRE VanA <i>E. faecalis</i> pheromone-responsive plasmid Taiwan livestock |
| title | High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan |
| title_full | High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan |
| title_fullStr | High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan |
| title_full_unstemmed | High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan |
| title_short | High Incidence of Multiple-Drug-Resistant Pheromone-Responsive Plasmids and Transmissions of VanA-Type Vancomycin-Resistant <i>Enterococcus faecalis</i> between Livestock and Humans in Taiwan |
| title_sort | high incidence of multiple drug resistant pheromone responsive plasmids and transmissions of vana type vancomycin resistant i enterococcus faecalis i between livestock and humans in taiwan |
| topic | VRE VanA <i>E. faecalis</i> pheromone-responsive plasmid Taiwan livestock |
| url | https://www.mdpi.com/2079-6382/12/12/1668 |
| work_keys_str_mv | AT haruyoshitomita highincidenceofmultipledrugresistantpheromoneresponsiveplasmidsandtransmissionsofvanatypevancomycinresistantienterococcusfaecalisibetweenlivestockandhumansintaiwan AT jangjihlu highincidenceofmultipledrugresistantpheromoneresponsiveplasmidsandtransmissionsofvanatypevancomycinresistantienterococcusfaecalisibetweenlivestockandhumansintaiwan AT yasuyoshiike highincidenceofmultipledrugresistantpheromoneresponsiveplasmidsandtransmissionsofvanatypevancomycinresistantienterococcusfaecalisibetweenlivestockandhumansintaiwan |