Triclosan Tolerance Is Driven by a Conserved Mechanism in Diverse Pseudomonas Species
Perturbation of natural microbial communities by antimicrobials, such as triclosan, can result in selection for antibiotic tolerance, which is of particular concern when pathogens are present. Members of the genus are found in many natural microbial communities and frequently demonstrate increased a...
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creator | McFarland, Alexander G Bertucci, Hanna K Littman, Erica Shen, Jiaxian Huttenhower, Curtis Hartmann, Erica M |
description | Perturbation of natural microbial communities by antimicrobials, such as triclosan, can result in selection for antibiotic tolerance, which is of particular concern when pathogens are present. Members of the genus
are found in many natural microbial communities and frequently demonstrate increased abundance following triclosan exposure. The pathogen and well-studied model organism
exhibits high triclosan tolerance; however, it is unknown if all
species share this trait or if there are susceptible strains. We characterized the triclosan tolerance phenotypes of diverse
isolates obtained from triclosan-exposed built environments and identified both tolerant and sensitive strains. High tolerance is associated with carriage of the enoyl-acyl carrier reductase (ENR) isozyme gene
, compared to the lesser protective effects of efflux or presence of ENRs. Given its unique importance, we examined
distribution throughout
species using large-scale phylogenomic analyses. We find
presence or absence is largely invariant at the species level but demonstrates multiple gain and loss events in its evolutionary history. We further provide evidence of its presence on mobile genetic elements. Our results demonstrate the surprising variability in triclosan tolerance in
and confirm
to be a useful indicator for high triclosan tolerance in
These findings provide a framework for better monitoring of
in triclosan-exposed environments and interpreting effects on species and gene composition.
Closely related species are typically assumed to demonstrate similar phenotypes driven by underlying conserved genotypes. When monitoring for the effect of antimicrobials on the types of species that may be selected for, this assumption may prove to be incorrect, and identification of additional genetic markers may be necessary. We isolated several phylogenetically diverse members of
from indoor environments and tested their phenotypic tolerance toward the commonly used antimicrobial triclosan. Although
isolates are broadly regarded to be highly triclosan tolerant, we demonstrate the presence of both triclosan-tolerant and -susceptible strains, separated by a difference in tolerance of nearly 3 orders of magnitude. Bioinformatic and experimental investigation demonstrated that the presence of the gene
was associated with high tolerance. We demonstrate that
is not evenly distributed in all
species and that its presence could be a useful predictor of high triclosan tolerance suitable for antimicrob |
doi_str_mv | 10.1128/AEM.02924-20 |
format | Article |
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are found in many natural microbial communities and frequently demonstrate increased abundance following triclosan exposure. The pathogen and well-studied model organism
exhibits high triclosan tolerance; however, it is unknown if all
species share this trait or if there are susceptible strains. We characterized the triclosan tolerance phenotypes of diverse
isolates obtained from triclosan-exposed built environments and identified both tolerant and sensitive strains. High tolerance is associated with carriage of the enoyl-acyl carrier reductase (ENR) isozyme gene
, compared to the lesser protective effects of efflux or presence of ENRs. Given its unique importance, we examined
distribution throughout
species using large-scale phylogenomic analyses. We find
presence or absence is largely invariant at the species level but demonstrates multiple gain and loss events in its evolutionary history. We further provide evidence of its presence on mobile genetic elements. Our results demonstrate the surprising variability in triclosan tolerance in
and confirm
to be a useful indicator for high triclosan tolerance in
These findings provide a framework for better monitoring of
in triclosan-exposed environments and interpreting effects on species and gene composition.
Closely related species are typically assumed to demonstrate similar phenotypes driven by underlying conserved genotypes. When monitoring for the effect of antimicrobials on the types of species that may be selected for, this assumption may prove to be incorrect, and identification of additional genetic markers may be necessary. We isolated several phylogenetically diverse members of
from indoor environments and tested their phenotypic tolerance toward the commonly used antimicrobial triclosan. Although
isolates are broadly regarded to be highly triclosan tolerant, we demonstrate the presence of both triclosan-tolerant and -susceptible strains, separated by a difference in tolerance of nearly 3 orders of magnitude. Bioinformatic and experimental investigation demonstrated that the presence of the gene
was associated with high tolerance. We demonstrate that
is not evenly distributed in all
species and that its presence could be a useful predictor of high triclosan tolerance suitable for antimicrobial monitoring efforts involving triclosan.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.02924-20</identifier><identifier>PMID: 33483311</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Anti-Bacterial Agents - pharmacology ; Anti-Infective Agents, Local - pharmacology ; Antibiotic tolerance ; Antibiotics ; Antiinfectives and antibacterials ; Antimicrobial agents ; Drug Resistance, Bacterial - genetics ; Efflux ; Environmental effects ; Evolutionary and Genomic Microbiology ; Exposure ; Genetic markers ; Genotypes ; Geographical distribution ; Indoor environments ; Microbial activity ; Microorganisms ; Monitoring ; Pathogens ; Perturbation ; Phenotypes ; Phylogeny ; Pseudomonas ; Pseudomonas - drug effects ; Pseudomonas - genetics ; Pseudomonas aeruginosa ; Reductases ; Species ; Species Specificity ; Strains (organisms) ; Triclosan ; Triclosan - pharmacology ; Urban areas ; Urban environments</subject><ispartof>Applied and environmental microbiology, 2021-03, Vol.87 (7), p.e02924-20</ispartof><rights>Copyright © 2021 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Apr 2021</rights><rights>Copyright © 2021 American Society for Microbiology. 2021 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a446t-c4999a5de32639af2ef3bfbe83ad2860bb7bd10567568716b94675561762cd8d3</citedby><cites>FETCH-LOGICAL-a446t-c4999a5de32639af2ef3bfbe83ad2860bb7bd10567568716b94675561762cd8d3</cites><orcidid>0000-0002-0966-2014</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/AEM.02924-20$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/AEM.02924-20$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,52751,52752,52753,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33483311$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Drake, Harold L</contributor><contributor>Drake, Harold L.</contributor><creatorcontrib>McFarland, Alexander G</creatorcontrib><creatorcontrib>Bertucci, Hanna K</creatorcontrib><creatorcontrib>Littman, Erica</creatorcontrib><creatorcontrib>Shen, Jiaxian</creatorcontrib><creatorcontrib>Huttenhower, Curtis</creatorcontrib><creatorcontrib>Hartmann, Erica M</creatorcontrib><title>Triclosan Tolerance Is Driven by a Conserved Mechanism in Diverse Pseudomonas Species</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>Perturbation of natural microbial communities by antimicrobials, such as triclosan, can result in selection for antibiotic tolerance, which is of particular concern when pathogens are present. Members of the genus
are found in many natural microbial communities and frequently demonstrate increased abundance following triclosan exposure. The pathogen and well-studied model organism
exhibits high triclosan tolerance; however, it is unknown if all
species share this trait or if there are susceptible strains. We characterized the triclosan tolerance phenotypes of diverse
isolates obtained from triclosan-exposed built environments and identified both tolerant and sensitive strains. High tolerance is associated with carriage of the enoyl-acyl carrier reductase (ENR) isozyme gene
, compared to the lesser protective effects of efflux or presence of ENRs. Given its unique importance, we examined
distribution throughout
species using large-scale phylogenomic analyses. We find
presence or absence is largely invariant at the species level but demonstrates multiple gain and loss events in its evolutionary history. We further provide evidence of its presence on mobile genetic elements. Our results demonstrate the surprising variability in triclosan tolerance in
and confirm
to be a useful indicator for high triclosan tolerance in
These findings provide a framework for better monitoring of
in triclosan-exposed environments and interpreting effects on species and gene composition.
Closely related species are typically assumed to demonstrate similar phenotypes driven by underlying conserved genotypes. When monitoring for the effect of antimicrobials on the types of species that may be selected for, this assumption may prove to be incorrect, and identification of additional genetic markers may be necessary. We isolated several phylogenetically diverse members of
from indoor environments and tested their phenotypic tolerance toward the commonly used antimicrobial triclosan. Although
isolates are broadly regarded to be highly triclosan tolerant, we demonstrate the presence of both triclosan-tolerant and -susceptible strains, separated by a difference in tolerance of nearly 3 orders of magnitude. Bioinformatic and experimental investigation demonstrated that the presence of the gene
was associated with high tolerance. We demonstrate that
is not evenly distributed in all
species and that its presence could be a useful predictor of high triclosan tolerance suitable for antimicrobial monitoring efforts involving triclosan.</description><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Infective Agents, Local - pharmacology</subject><subject>Antibiotic tolerance</subject><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Antimicrobial agents</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>Efflux</subject><subject>Environmental effects</subject><subject>Evolutionary and Genomic Microbiology</subject><subject>Exposure</subject><subject>Genetic markers</subject><subject>Genotypes</subject><subject>Geographical distribution</subject><subject>Indoor environments</subject><subject>Microbial activity</subject><subject>Microorganisms</subject><subject>Monitoring</subject><subject>Pathogens</subject><subject>Perturbation</subject><subject>Phenotypes</subject><subject>Phylogeny</subject><subject>Pseudomonas</subject><subject>Pseudomonas - drug effects</subject><subject>Pseudomonas - genetics</subject><subject>Pseudomonas aeruginosa</subject><subject>Reductases</subject><subject>Species</subject><subject>Species Specificity</subject><subject>Strains (organisms)</subject><subject>Triclosan</subject><subject>Triclosan - pharmacology</subject><subject>Urban areas</subject><subject>Urban environments</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1LAzEQhoMoWqs3zxLwJLg6SXbT5CKU-gmKgvUcsruzutJNatIW_PdGW78OnmZgHp6Z4SVkj8ExY1ydDM9vj4Frnmcc1kiPgVZZIYRcJz0ArTPOc9gi2zG-AEAOUm2SLSFyJQRjPfI4Dm018dE6OvYTDNZVSK8jPQvtAh0t36ilI-8ihgXW9BarZ-va2NHW0bNEhIj0PuK89p13NtKHKVYtxh2y0dhJxN1V7ZPHi_Px6Cq7ubu8Hg1vMpvncpZVudbaFjUKLoW2DcdGlE2JStiaKwllOShrBoUcFFINmCx1ntpCsoHkVa1q0SenS-90XnZYV-hmwU7MNLSdDW_G29b8nbj22Tz5hVGgmQSdBAcrQfCvc4wz8-LnwaWbDS8gLeMJTNTRkqqCjzFg872BgfkIwaQQzGcIhkPCD5e4jR3_Ef7D7v_-4Fv8lZB4B06TjrM</recordid><startdate>20210311</startdate><enddate>20210311</enddate><creator>McFarland, Alexander G</creator><creator>Bertucci, Hanna K</creator><creator>Littman, Erica</creator><creator>Shen, Jiaxian</creator><creator>Huttenhower, Curtis</creator><creator>Hartmann, Erica M</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0966-2014</orcidid></search><sort><creationdate>20210311</creationdate><title>Triclosan Tolerance Is Driven by a Conserved Mechanism in Diverse Pseudomonas Species</title><author>McFarland, Alexander G ; 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Members of the genus
are found in many natural microbial communities and frequently demonstrate increased abundance following triclosan exposure. The pathogen and well-studied model organism
exhibits high triclosan tolerance; however, it is unknown if all
species share this trait or if there are susceptible strains. We characterized the triclosan tolerance phenotypes of diverse
isolates obtained from triclosan-exposed built environments and identified both tolerant and sensitive strains. High tolerance is associated with carriage of the enoyl-acyl carrier reductase (ENR) isozyme gene
, compared to the lesser protective effects of efflux or presence of ENRs. Given its unique importance, we examined
distribution throughout
species using large-scale phylogenomic analyses. We find
presence or absence is largely invariant at the species level but demonstrates multiple gain and loss events in its evolutionary history. We further provide evidence of its presence on mobile genetic elements. Our results demonstrate the surprising variability in triclosan tolerance in
and confirm
to be a useful indicator for high triclosan tolerance in
These findings provide a framework for better monitoring of
in triclosan-exposed environments and interpreting effects on species and gene composition.
Closely related species are typically assumed to demonstrate similar phenotypes driven by underlying conserved genotypes. When monitoring for the effect of antimicrobials on the types of species that may be selected for, this assumption may prove to be incorrect, and identification of additional genetic markers may be necessary. We isolated several phylogenetically diverse members of
from indoor environments and tested their phenotypic tolerance toward the commonly used antimicrobial triclosan. Although
isolates are broadly regarded to be highly triclosan tolerant, we demonstrate the presence of both triclosan-tolerant and -susceptible strains, separated by a difference in tolerance of nearly 3 orders of magnitude. Bioinformatic and experimental investigation demonstrated that the presence of the gene
was associated with high tolerance. We demonstrate that
is not evenly distributed in all
species and that its presence could be a useful predictor of high triclosan tolerance suitable for antimicrobial monitoring efforts involving triclosan.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>33483311</pmid><doi>10.1128/AEM.02924-20</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-0966-2014</orcidid><oa>free_for_read</oa></addata></record> |
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source | American Society for Microbiology; MEDLINE; PubMed Central; Alma/SFX Local Collection |
subjects | Anti-Bacterial Agents - pharmacology Anti-Infective Agents, Local - pharmacology Antibiotic tolerance Antibiotics Antiinfectives and antibacterials Antimicrobial agents Drug Resistance, Bacterial - genetics Efflux Environmental effects Evolutionary and Genomic Microbiology Exposure Genetic markers Genotypes Geographical distribution Indoor environments Microbial activity Microorganisms Monitoring Pathogens Perturbation Phenotypes Phylogeny Pseudomonas Pseudomonas - drug effects Pseudomonas - genetics Pseudomonas aeruginosa Reductases Species Species Specificity Strains (organisms) Triclosan Triclosan - pharmacology Urban areas Urban environments |
title | Triclosan Tolerance Is Driven by a Conserved Mechanism in Diverse Pseudomonas Species |
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