Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance
Horizontal gene transfer (HGT) plays a major role in the spread of antibiotic resistance. Of particular concern are Acinetobacter baumannii bacteria, which recently emerged as global pathogens, with nosocomial mortality rates reaching 19–54% (Centers for Disease Control and Prevention, 2013; Joly Gu...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/25950 |
| _version_ | 1811252931851190272 |
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| author | Robert M Cooper Lev Tsimring Jeff Hasty |
| author_facet | Robert M Cooper Lev Tsimring Jeff Hasty |
| author_sort | Robert M Cooper |
| collection | DOAJ |
| description | Horizontal gene transfer (HGT) plays a major role in the spread of antibiotic resistance. Of particular concern are Acinetobacter baumannii bacteria, which recently emerged as global pathogens, with nosocomial mortality rates reaching 19–54% (Centers for Disease Control and Prevention, 2013; Joly Guillou, 2005; Talbot et al., 2006). Acinetobacter gains antibiotic resistance remarkably rapidly (Antunes et al., 2014; Joly Guillou, 2005), with multi drug-resistance (MDR) rates exceeding 60% (Antunes et al., 2014; Centers for Disease Control and Prevention, 2013). Despite growing concern (Centers for Disease Control and Prevention, 2013; Talbot et al., 2006), the mechanisms underlying this extensive HGT remain poorly understood (Adams et al., 2008; Fournier et al., 2006; Imperi et al., 2011; Ramirez et al., 2010; Wilharm et al., 2013). Here, we show bacterial predation by Acinetobacter baylyi increases cross-species HGT by orders of magnitude, and we observe predator cells functionally acquiring adaptive resistance genes from adjacent prey. We then develop a population-dynamic model quantifying killing and HGT on solid surfaces. We show DNA released via cell lysis is readily available for HGT and may be partially protected from the environment, describe the effects of cell density, and evaluate potential environmental inhibitors. These findings establish a framework for understanding, quantifying, and combating HGT within the microbiome and the emergence of MDR super-bugs. |
| first_indexed | 2024-04-12T16:43:10Z |
| format | Article |
| id | doaj.art-4c212fb0cd164ace928b766eaaf8b60a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:43:10Z |
| publishDate | 2017-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-4c212fb0cd164ace928b766eaaf8b60a2022-12-22T03:24:42ZengeLife Sciences Publications LtdeLife2050-084X2017-11-01610.7554/eLife.25950Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistanceRobert M Cooper0https://orcid.org/0000-0003-2136-0403Lev Tsimring1Jeff Hasty2BioCircuits Institute, University of California, San Diego, San Diego, United StatesBioCircuits Institute, University of California, San Diego, San Diego, United States; San Diego Center for Systems Biology, University of California, San Diego, San Diego, United StatesBioCircuits Institute, University of California, San Diego, San Diego, United States; San Diego Center for Systems Biology, University of California, San Diego, San Diego, United States; Molecular Biology Section, Division of Biological Science, University of California, San Diego, San Diego, United States; Department of Bioengineering, University of California, San Diego, San Diego, United StatesHorizontal gene transfer (HGT) plays a major role in the spread of antibiotic resistance. Of particular concern are Acinetobacter baumannii bacteria, which recently emerged as global pathogens, with nosocomial mortality rates reaching 19–54% (Centers for Disease Control and Prevention, 2013; Joly Guillou, 2005; Talbot et al., 2006). Acinetobacter gains antibiotic resistance remarkably rapidly (Antunes et al., 2014; Joly Guillou, 2005), with multi drug-resistance (MDR) rates exceeding 60% (Antunes et al., 2014; Centers for Disease Control and Prevention, 2013). Despite growing concern (Centers for Disease Control and Prevention, 2013; Talbot et al., 2006), the mechanisms underlying this extensive HGT remain poorly understood (Adams et al., 2008; Fournier et al., 2006; Imperi et al., 2011; Ramirez et al., 2010; Wilharm et al., 2013). Here, we show bacterial predation by Acinetobacter baylyi increases cross-species HGT by orders of magnitude, and we observe predator cells functionally acquiring adaptive resistance genes from adjacent prey. We then develop a population-dynamic model quantifying killing and HGT on solid surfaces. We show DNA released via cell lysis is readily available for HGT and may be partially protected from the environment, describe the effects of cell density, and evaluate potential environmental inhibitors. These findings establish a framework for understanding, quantifying, and combating HGT within the microbiome and the emergence of MDR super-bugs.https://elifesciences.org/articles/25950Acinetobacter baylyihorizontal gene transferantibiotic resistancenatural competencemulti-drug resistancemicrobial population dynamics |
| spellingShingle | Robert M Cooper Lev Tsimring Jeff Hasty Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance eLife Acinetobacter baylyi horizontal gene transfer antibiotic resistance natural competence multi-drug resistance microbial population dynamics |
| title | Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| title_full | Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| title_fullStr | Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| title_full_unstemmed | Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| title_short | Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| title_sort | inter species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance |
| topic | Acinetobacter baylyi horizontal gene transfer antibiotic resistance natural competence multi-drug resistance microbial population dynamics |
| url | https://elifesciences.org/articles/25950 |
| work_keys_str_mv | AT robertmcooper interspeciespopulationdynamicsenhancemicrobialhorizontalgenetransferandspreadofantibioticresistance AT levtsimring interspeciespopulationdynamicsenhancemicrobialhorizontalgenetransferandspreadofantibioticresistance AT jeffhasty interspeciespopulationdynamicsenhancemicrobialhorizontalgenetransferandspreadofantibioticresistance |