Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide.
<h4>Objectives</h4>Antimicrobial-resistant bacteria are a major global health threat. Mobile genetic elements (MGEs) have been crucial for spreading resistance to new bacterial species, including human pathogens. Understanding how MGEs promote resistance could be essential for prevention...
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| Language: | English |
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Public Library of Science (PLoS)
2025-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0330304 |
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| author | Markus H K Johansson Thomas N Petersen Sidsel Nag Timmie M R Lagermann Laura E K Birkedahl Silva Tafaj Susan Bradbury Peter Collignon Denise Daley Victorien Dougnon Kafayath Fabiyi Boubacar Coulibaly Réné Dembélé Natama Magloire Isidore J Ouindgueta Zenat Z Hossain Anowara Begoum Deyan Donchev Mathew Diggle LeeAnn Turnbull Simon Lévesque Livia Berlinger Kirstine K Søgaard Paula D Guevara Carolina Duarte Panagiota Maikanti Jana Amlerova Pavel Drevinek Jan Tkadlec Milica Dilas Achim Kaasch Henrik T Westh Mohamed A Bachtarzi Wahiba Amhis Carolina E S Salazar José E Villacis Mária A D Lúzon Dàmaris B Palau Claire Duployez Maxime Paluche Solomon Asante-Sefa Mie Møller Margaret Ip Ivana Mareković Agnes Pál-Sonnevend Clementiza E Cocuzza Asta Dambrauskiene Alexandre Macanze Anelsio Cossa Inácio Mandomando Philip Nwajiobi-Princewill Iruka N Okeke Aderemi O Kehinde Ini Adebiyi Ifeoluwa Akintayo Oluwafemi Popoola Anthony Onipede Anita Blomfeldt Nora E Nyquist Kiri Bocker James Ussher Amjad Ali Nimat Ullah Habibullah Khan Natalie W Gustafson Ikhlas Jarrar Arif Al-Hamad Viravarn Luvira Wantana Paveenkittiporn Irmak Baran James C L Mwansa Linda Sikakwa Kaunda Yamba Frank M Aarestrup |
| author_facet | Markus H K Johansson Thomas N Petersen Sidsel Nag Timmie M R Lagermann Laura E K Birkedahl Silva Tafaj Susan Bradbury Peter Collignon Denise Daley Victorien Dougnon Kafayath Fabiyi Boubacar Coulibaly Réné Dembélé Natama Magloire Isidore J Ouindgueta Zenat Z Hossain Anowara Begoum Deyan Donchev Mathew Diggle LeeAnn Turnbull Simon Lévesque Livia Berlinger Kirstine K Søgaard Paula D Guevara Carolina Duarte Panagiota Maikanti Jana Amlerova Pavel Drevinek Jan Tkadlec Milica Dilas Achim Kaasch Henrik T Westh Mohamed A Bachtarzi Wahiba Amhis Carolina E S Salazar José E Villacis Mária A D Lúzon Dàmaris B Palau Claire Duployez Maxime Paluche Solomon Asante-Sefa Mie Møller Margaret Ip Ivana Mareković Agnes Pál-Sonnevend Clementiza E Cocuzza Asta Dambrauskiene Alexandre Macanze Anelsio Cossa Inácio Mandomando Philip Nwajiobi-Princewill Iruka N Okeke Aderemi O Kehinde Ini Adebiyi Ifeoluwa Akintayo Oluwafemi Popoola Anthony Onipede Anita Blomfeldt Nora E Nyquist Kiri Bocker James Ussher Amjad Ali Nimat Ullah Habibullah Khan Natalie W Gustafson Ikhlas Jarrar Arif Al-Hamad Viravarn Luvira Wantana Paveenkittiporn Irmak Baran James C L Mwansa Linda Sikakwa Kaunda Yamba Frank M Aarestrup |
| author_sort | Markus H K Johansson |
| collection | DOAJ |
| description | <h4>Objectives</h4>Antimicrobial-resistant bacteria are a major global health threat. Mobile genetic elements (MGEs) have been crucial for spreading resistance to new bacterial species, including human pathogens. Understanding how MGEs promote resistance could be essential for prevention. Here we present an investigation of MGEs and their association with resistance genes in pathogenic bacteria collected from 59 diagnostic units during 2020, representing a snapshot of clinical infections from 35 counties worldwide.<h4>Methods</h4>We analysed 3,095 whole-genome sequenced clinical bacterial isolates from over 100 species to study the relationship between resistance genes and MGEs. The mobiliome of Staphylococcus aureus, Enterococcus faecalis, Escherichia coli, and Klebsiella pneumoniae were further examined for geographic differences, as these species were prevalent in all countries. Genes potentially mobilized by MGEs were identified by finding DNA segments containing MGEs and ARGs preserved in multiple species. Network analysis was used to investigate potential MGE interactions, host range, and transmission pathways.<h4>Results</h4>The prevalence and diversity of MGEs and resistance genes varied among species, with E. coli and S. aureus carrying more diverse elements. MGE composition differed between bacterial lineages, indicating strong vertical inheritance. 102 MGEs associated with resistance were found in multiple species, and four of these elements seemed to be highly transmissible as they were found in different phyla. We identified 21 genomic regions containing resistance genes potentially mobilized by MGEs, highlighting their importance in transmitting genes to clinically significant bacteria.<h4>Conclusion</h4>Resistance genes are spread through various MGEs, including plasmids and transposons. Our findings suggest that multiple factors influence MGE prevalence and their transposability, thereby shaping the MGE population and transmission pathways. Some MGEs have a wider host range, which could make them more important for mobilizing genes. We also identified 103 resistance genes potentially mobilised by MGEs, which could increase their transmissibility to unrelated bacteria. |
| format | Article |
| id | doaj-art-a765e40aed5d444e93a42482981e1a26 |
| institution | Kabale University |
| issn | 1932-6203 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj-art-a765e40aed5d444e93a42482981e1a262025-08-23T05:32:32ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01208e033030410.1371/journal.pone.0330304Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide.Markus H K JohanssonThomas N PetersenSidsel NagTimmie M R LagermannLaura E K BirkedahlSilva TafajSusan BradburyPeter CollignonDenise DaleyVictorien DougnonKafayath FabiyiBoubacar CoulibalyRéné DembéléNatama MagloireIsidore J OuindguetaZenat Z HossainAnowara BegoumDeyan DonchevMathew DiggleLeeAnn TurnbullSimon LévesqueLivia BerlingerKirstine K SøgaardPaula D GuevaraCarolina DuartePanagiota MaikantiJana AmlerovaPavel DrevinekJan TkadlecMilica DilasAchim KaaschHenrik T WesthMohamed A BachtarziWahiba AmhisCarolina E S SalazarJosé E VillacisMária A D LúzonDàmaris B PalauClaire DuployezMaxime PalucheSolomon Asante-SefaMie MøllerMargaret IpIvana MarekovićAgnes Pál-SonnevendClementiza E CocuzzaAsta DambrauskieneAlexandre MacanzeAnelsio CossaInácio MandomandoPhilip Nwajiobi-PrincewillIruka N OkekeAderemi O KehindeIni AdebiyiIfeoluwa AkintayoOluwafemi PopoolaAnthony OnipedeAnita BlomfeldtNora E NyquistKiri BockerJames UssherAmjad AliNimat UllahHabibullah KhanNatalie W GustafsonIkhlas JarrarArif Al-HamadViravarn LuviraWantana PaveenkittipornIrmak BaranJames C L MwansaLinda SikakwaKaunda YambaFrank M Aarestrup<h4>Objectives</h4>Antimicrobial-resistant bacteria are a major global health threat. Mobile genetic elements (MGEs) have been crucial for spreading resistance to new bacterial species, including human pathogens. Understanding how MGEs promote resistance could be essential for prevention. Here we present an investigation of MGEs and their association with resistance genes in pathogenic bacteria collected from 59 diagnostic units during 2020, representing a snapshot of clinical infections from 35 counties worldwide.<h4>Methods</h4>We analysed 3,095 whole-genome sequenced clinical bacterial isolates from over 100 species to study the relationship between resistance genes and MGEs. The mobiliome of Staphylococcus aureus, Enterococcus faecalis, Escherichia coli, and Klebsiella pneumoniae were further examined for geographic differences, as these species were prevalent in all countries. Genes potentially mobilized by MGEs were identified by finding DNA segments containing MGEs and ARGs preserved in multiple species. Network analysis was used to investigate potential MGE interactions, host range, and transmission pathways.<h4>Results</h4>The prevalence and diversity of MGEs and resistance genes varied among species, with E. coli and S. aureus carrying more diverse elements. MGE composition differed between bacterial lineages, indicating strong vertical inheritance. 102 MGEs associated with resistance were found in multiple species, and four of these elements seemed to be highly transmissible as they were found in different phyla. We identified 21 genomic regions containing resistance genes potentially mobilized by MGEs, highlighting their importance in transmitting genes to clinically significant bacteria.<h4>Conclusion</h4>Resistance genes are spread through various MGEs, including plasmids and transposons. Our findings suggest that multiple factors influence MGE prevalence and their transposability, thereby shaping the MGE population and transmission pathways. Some MGEs have a wider host range, which could make them more important for mobilizing genes. We also identified 103 resistance genes potentially mobilised by MGEs, which could increase their transmissibility to unrelated bacteria.https://doi.org/10.1371/journal.pone.0330304 |
| spellingShingle | Markus H K Johansson Thomas N Petersen Sidsel Nag Timmie M R Lagermann Laura E K Birkedahl Silva Tafaj Susan Bradbury Peter Collignon Denise Daley Victorien Dougnon Kafayath Fabiyi Boubacar Coulibaly Réné Dembélé Natama Magloire Isidore J Ouindgueta Zenat Z Hossain Anowara Begoum Deyan Donchev Mathew Diggle LeeAnn Turnbull Simon Lévesque Livia Berlinger Kirstine K Søgaard Paula D Guevara Carolina Duarte Panagiota Maikanti Jana Amlerova Pavel Drevinek Jan Tkadlec Milica Dilas Achim Kaasch Henrik T Westh Mohamed A Bachtarzi Wahiba Amhis Carolina E S Salazar José E Villacis Mária A D Lúzon Dàmaris B Palau Claire Duployez Maxime Paluche Solomon Asante-Sefa Mie Møller Margaret Ip Ivana Mareković Agnes Pál-Sonnevend Clementiza E Cocuzza Asta Dambrauskiene Alexandre Macanze Anelsio Cossa Inácio Mandomando Philip Nwajiobi-Princewill Iruka N Okeke Aderemi O Kehinde Ini Adebiyi Ifeoluwa Akintayo Oluwafemi Popoola Anthony Onipede Anita Blomfeldt Nora E Nyquist Kiri Bocker James Ussher Amjad Ali Nimat Ullah Habibullah Khan Natalie W Gustafson Ikhlas Jarrar Arif Al-Hamad Viravarn Luvira Wantana Paveenkittiporn Irmak Baran James C L Mwansa Linda Sikakwa Kaunda Yamba Frank M Aarestrup Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. PLoS ONE |
| title | Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. |
| title_full | Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. |
| title_fullStr | Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. |
| title_full_unstemmed | Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. |
| title_short | Investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide. |
| title_sort | investigation of mobile genetic elements and their association with antibiotic resistance genes in clinical pathogens worldwide |
| url | https://doi.org/10.1371/journal.pone.0330304 |
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