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Temporal dynamics of bacteria-plasmid coevolution under antibiotic selection
Horizontally acquired genes can be costly to express even if they encode useful traits, such as antibiotic resistance. We previously showed that when selected with tetracycline, Escherichia coli carrying the tetracycline-resistance plasmid RK2 evolved mutations on both replicons that together provid...
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| Published in: | The ISME Journal 2019-02, Vol.13 (2), p.559-562 |
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| creator | Bottery, Michael J. Wood, A. Jamie Brockhurst, Michael A. |
| description | Horizontally acquired genes can be costly to express even if they encode useful traits, such as antibiotic resistance. We previously showed that when selected with tetracycline,
Escherichia coli
carrying the tetracycline-resistance plasmid RK2 evolved mutations on both replicons that together provided increased tetracycline resistance at reduced cost. Here we investigate the temporal dynamics of this intragenomic coevolution. Using genome sequencing we show that the order of adaptive mutations was highly repeatable across three independently evolving populations. Each population first gained a chromosomal mutation in
ompF
which shortened lag phase and increased tetracycline resistance. This was followed by mutations impairing the plasmid-encoded tetracycline efflux pump, and finally, additional resistance-associated chromosomal mutations. Thus, reducing the cost of the horizontally acquired tetracycline resistance was contingent on first evolving a degree of chromosomally encoded resistance. We conclude therefore that the trajectory of bacteria-plasmid coevolution was constrained to a single repeatable path. |
| doi_str_mv | 10.1038/s41396-018-0276-9 |
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Escherichia coli
carrying the tetracycline-resistance plasmid RK2 evolved mutations on both replicons that together provided increased tetracycline resistance at reduced cost. Here we investigate the temporal dynamics of this intragenomic coevolution. Using genome sequencing we show that the order of adaptive mutations was highly repeatable across three independently evolving populations. Each population first gained a chromosomal mutation in
ompF
which shortened lag phase and increased tetracycline resistance. This was followed by mutations impairing the plasmid-encoded tetracycline efflux pump, and finally, additional resistance-associated chromosomal mutations. Thus, reducing the cost of the horizontally acquired tetracycline resistance was contingent on first evolving a degree of chromosomally encoded resistance. We conclude therefore that the trajectory of bacteria-plasmid coevolution was constrained to a single repeatable path.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-018-0276-9</identifier><identifier>PMID: 30209344</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>45/23 ; 631/181/735 ; 631/326/22/1290 ; Adaptation, Physiological - drug effects ; Adaptation, Physiological - genetics ; Antibiotic resistance ; Antibiotics ; Bacteria ; Biological Coevolution ; Biomedical and Life Sciences ; Brief Communication ; Coevolution ; E coli ; Ecology ; Efflux ; Escherichia coli - drug effects ; Escherichia coli - genetics ; Evolution ; Evolutionary Biology ; Gene sequencing ; Gene Transfer, Horizontal ; Genomes ; Lag phase ; Life Sciences ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Mutation ; Penicillin ; Plasmids - genetics ; Replicon ; Selection, Genetic ; Tetracycline - pharmacology ; Tetracycline Resistance - genetics</subject><ispartof>The ISME Journal, 2019-02, Vol.13 (2), p.559-562</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-7e58db177c9b785302f1ce5a0870f87ca927e0576f5fc0ac2e4ec1e386879e983</citedby><cites>FETCH-LOGICAL-c470t-7e58db177c9b785302f1ce5a0870f87ca927e0576f5fc0ac2e4ec1e386879e983</cites><orcidid>0000-0003-0362-820X ; 0000-0001-5790-1756</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6330079/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6330079/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30209344$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bottery, Michael J.</creatorcontrib><creatorcontrib>Wood, A. Jamie</creatorcontrib><creatorcontrib>Brockhurst, Michael A.</creatorcontrib><title>Temporal dynamics of bacteria-plasmid coevolution under antibiotic selection</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Horizontally acquired genes can be costly to express even if they encode useful traits, such as antibiotic resistance. We previously showed that when selected with tetracycline,
Escherichia coli
carrying the tetracycline-resistance plasmid RK2 evolved mutations on both replicons that together provided increased tetracycline resistance at reduced cost. Here we investigate the temporal dynamics of this intragenomic coevolution. Using genome sequencing we show that the order of adaptive mutations was highly repeatable across three independently evolving populations. Each population first gained a chromosomal mutation in
ompF
which shortened lag phase and increased tetracycline resistance. This was followed by mutations impairing the plasmid-encoded tetracycline efflux pump, and finally, additional resistance-associated chromosomal mutations. Thus, reducing the cost of the horizontally acquired tetracycline resistance was contingent on first evolving a degree of chromosomally encoded resistance. We conclude therefore that the trajectory of bacteria-plasmid coevolution was constrained to a single repeatable path.</description><subject>45/23</subject><subject>631/181/735</subject><subject>631/326/22/1290</subject><subject>Adaptation, Physiological - drug effects</subject><subject>Adaptation, Physiological - genetics</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Biological Coevolution</subject><subject>Biomedical and Life Sciences</subject><subject>Brief Communication</subject><subject>Coevolution</subject><subject>E coli</subject><subject>Ecology</subject><subject>Efflux</subject><subject>Escherichia coli - drug effects</subject><subject>Escherichia coli - genetics</subject><subject>Evolution</subject><subject>Evolutionary Biology</subject><subject>Gene sequencing</subject><subject>Gene Transfer, Horizontal</subject><subject>Genomes</subject><subject>Lag phase</subject><subject>Life Sciences</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Mutation</subject><subject>Penicillin</subject><subject>Plasmids - genetics</subject><subject>Replicon</subject><subject>Selection, Genetic</subject><subject>Tetracycline - pharmacology</subject><subject>Tetracycline Resistance - genetics</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp1kc1q3DAUhUVJaZJpHyCbYsimG7f6sXWlTSGENi0MdJOuhSxfJwq2NJHsQN4-MpNO00BXEtxPR-fcQ8gZo58ZFepLbpjQsqZM1ZSDrPUbcsKgZTUIoEeHu-TH5DTnO0pbkBLekWNBOdWiaU7I9hqnXUx2rPrHYCfvchWHqrNuxuRtvRttnnxfuYgPcVxmH0O1hB5TZcPsOx9n76qMI7p19J68HeyY8cPzuSG_v3-7vvxRb39d_by82NauATrXgK3qOwbgdAeqLWYG5rC1VAEdFDirOeDqdWgHR63j2KBjKJRUoFErsSFf97q7pZuwdxjmksDskp9sejTRevPvJPhbcxMfjBSCUtBF4NOzQIr3C-bZTD47HEcbMC7Z8LJeCZxrWtDzV-hdXFIo8QoloSxSlhY2hO0pl2LOCYeDGUbN2pXZd2VKV2btyqwmPr5McXjxp5wC8D2QyyjcYPr79f9VnwA0pqBO</recordid><startdate>20190201</startdate><enddate>20190201</enddate><creator>Bottery, Michael J.</creator><creator>Wood, A. 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Jamie ; Brockhurst, Michael A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c470t-7e58db177c9b785302f1ce5a0870f87ca927e0576f5fc0ac2e4ec1e386879e983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>45/23</topic><topic>631/181/735</topic><topic>631/326/22/1290</topic><topic>Adaptation, Physiological - drug effects</topic><topic>Adaptation, Physiological - genetics</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Biological Coevolution</topic><topic>Biomedical and Life Sciences</topic><topic>Brief Communication</topic><topic>Coevolution</topic><topic>E coli</topic><topic>Ecology</topic><topic>Efflux</topic><topic>Escherichia coli - drug effects</topic><topic>Escherichia coli - genetics</topic><topic>Evolution</topic><topic>Evolutionary Biology</topic><topic>Gene sequencing</topic><topic>Gene Transfer, Horizontal</topic><topic>Genomes</topic><topic>Lag phase</topic><topic>Life Sciences</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Mutation</topic><topic>Penicillin</topic><topic>Plasmids - genetics</topic><topic>Replicon</topic><topic>Selection, Genetic</topic><topic>Tetracycline - pharmacology</topic><topic>Tetracycline Resistance - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bottery, Michael J.</creatorcontrib><creatorcontrib>Wood, A. Jamie</creatorcontrib><creatorcontrib>Brockhurst, Michael A.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>ProQuest - Health & Medical Complete保健、医学与药学数据库</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bottery, Michael J.</au><au>Wood, A. Jamie</au><au>Brockhurst, Michael A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Temporal dynamics of bacteria-plasmid coevolution under antibiotic selection</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2019-02-01</date><risdate>2019</risdate><volume>13</volume><issue>2</issue><spage>559</spage><epage>562</epage><pages>559-562</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Horizontally acquired genes can be costly to express even if they encode useful traits, such as antibiotic resistance. We previously showed that when selected with tetracycline,
Escherichia coli
carrying the tetracycline-resistance plasmid RK2 evolved mutations on both replicons that together provided increased tetracycline resistance at reduced cost. Here we investigate the temporal dynamics of this intragenomic coevolution. Using genome sequencing we show that the order of adaptive mutations was highly repeatable across three independently evolving populations. Each population first gained a chromosomal mutation in
ompF
which shortened lag phase and increased tetracycline resistance. This was followed by mutations impairing the plasmid-encoded tetracycline efflux pump, and finally, additional resistance-associated chromosomal mutations. Thus, reducing the cost of the horizontally acquired tetracycline resistance was contingent on first evolving a degree of chromosomally encoded resistance. We conclude therefore that the trajectory of bacteria-plasmid coevolution was constrained to a single repeatable path.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30209344</pmid><doi>10.1038/s41396-018-0276-9</doi><tpages>4</tpages><orcidid>https://orcid.org/0000-0003-0362-820X</orcidid><orcidid>https://orcid.org/0000-0001-5790-1756</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 45/23 631/181/735 631/326/22/1290 Adaptation, Physiological - drug effects Adaptation, Physiological - genetics Antibiotic resistance Antibiotics Bacteria Biological Coevolution Biomedical and Life Sciences Brief Communication Coevolution E coli Ecology Efflux Escherichia coli - drug effects Escherichia coli - genetics Evolution Evolutionary Biology Gene sequencing Gene Transfer, Horizontal Genomes Lag phase Life Sciences Microbial Ecology Microbial Genetics and Genomics Microbiology Mutation Penicillin Plasmids - genetics Replicon Selection, Genetic Tetracycline - pharmacology Tetracycline Resistance - genetics |
| title | Temporal dynamics of bacteria-plasmid coevolution under antibiotic selection |
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