Acquired resistance of Stenotrophomonas maltophilia to antimicrobials induced by herbicide paraquat dichloride
Stenotrophomonas maltophilia, a ubiquitous environmental bacterium, is an important cause of nosocomial infections. Although banned in some countries, paraquat (PQ) is commonly used to control weeds. In this study, we investigated the effects of increasing concentrations of PQ on S. maltophilia and...
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| Veröffentlicht in: | PloS one 2024-08, Vol.19 (8), p.e0309525 |
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| creator | Vanitshavit, Veerakit Charoenlap, Nisanart Sallabhan, Ratiboot Whangsuk, Wirongrong Bhinija, Kisana Dulyayangkul, Punyawee Mongkolsuk, Skorn Vattanavibooon, Paiboon |
| description | Stenotrophomonas maltophilia, a ubiquitous environmental bacterium, is an important cause of nosocomial infections. Although banned in some countries, paraquat (PQ) is commonly used to control weeds. In this study, we investigated the effects of increasing concentrations of PQ on S. maltophilia and its antimicrobial resistance. The sequential exposure of S. maltophilia K279a to increasing concentrations of PQ induces the formation of strains with increased resistance to PQ. Among the 400 PQ-resistant isolates tested, 70 clones were resistant to 16 μg/ml ciprofloxacin (CIP), and around 18% of the PQ/CIP-resistant isolates showed increased resistance to all the tested antimicrobials including, the aminoglycosides, quinolones, cephalosporin, chloramphenicol, and co-trimoxazole. The results of the expression analysis of the antimicrobial resistance genes in the five selected PQ/CIP-resistant isolates demonstrated the high expression of genes encoding efflux pumps (smeYZ, smaAB, smaCDEF, smeDEF, smeVWX, and smtcrA) and the enzymes aph(3')-IIc, blaL1, and blaL2. However, expression of the genes known for PQ resistance (i.e., mfsA and sod) were not altered relative to the wild-type levels. Whole genome sequence analysis identified gene mutations that could account for the antimicrobial resistance, namely, smeT (TetR family regulatory protein), rplA (ribosomal protein L1), and acnA (aconitase A). Ectopic expression of wild-type AcnA partially complemented the fluoroquinolone-resistant phenotype of the mutant with mutated acnA, which suggests the role of aconitase A in antimicrobial susceptibility. Exposure of S. maltophilia to PQ thus induces the development of strains that increase resistance to multiple antimicrobials. |
| doi_str_mv | 10.1371/journal.pone.0309525 |
| format | Article |
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Although banned in some countries, paraquat (PQ) is commonly used to control weeds. In this study, we investigated the effects of increasing concentrations of PQ on S. maltophilia and its antimicrobial resistance. The sequential exposure of S. maltophilia K279a to increasing concentrations of PQ induces the formation of strains with increased resistance to PQ. Among the 400 PQ-resistant isolates tested, 70 clones were resistant to 16 μg/ml ciprofloxacin (CIP), and around 18% of the PQ/CIP-resistant isolates showed increased resistance to all the tested antimicrobials including, the aminoglycosides, quinolones, cephalosporin, chloramphenicol, and co-trimoxazole. The results of the expression analysis of the antimicrobial resistance genes in the five selected PQ/CIP-resistant isolates demonstrated the high expression of genes encoding efflux pumps (smeYZ, smaAB, smaCDEF, smeDEF, smeVWX, and smtcrA) and the enzymes aph(3')-IIc, blaL1, and blaL2. However, expression of the genes known for PQ resistance (i.e., mfsA and sod) were not altered relative to the wild-type levels. Whole genome sequence analysis identified gene mutations that could account for the antimicrobial resistance, namely, smeT (TetR family regulatory protein), rplA (ribosomal protein L1), and acnA (aconitase A). Ectopic expression of wild-type AcnA partially complemented the fluoroquinolone-resistant phenotype of the mutant with mutated acnA, which suggests the role of aconitase A in antimicrobial susceptibility. Exposure of S. maltophilia to PQ thus induces the development of strains that increase resistance to multiple antimicrobials.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0309525</identifier><identifier>PMID: 39196988</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acid sequence ; Aminoglycosides ; Analysis ; Anti-Bacterial Agents - pharmacology ; Antibiotics ; Antimicrobial agents ; Antimicrobial resistance ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biology and Life Sciences ; Blood proteins ; Cephalosporins ; Chloramphenicol ; Chloromycetin ; Ciprofloxacin ; Ciprofloxacin - pharmacology ; Cotrimoxazole ; Dichlorides ; Drug resistance ; Drug resistance in microorganisms ; Drug Resistance, Bacterial - drug effects ; Drug Resistance, Bacterial - genetics ; Drug Resistance, Multiple, Bacterial - genetics ; Ectopic expression ; Efflux ; Environmental aspects ; Enzymes ; Genes ; Genetic aspects ; Genomes ; Genomic analysis ; Gram-negative bacteria ; Health aspects ; Herbicide resistance ; Herbicides ; Herbicides - pharmacology ; Influence ; Medicine and Health Sciences ; Microbial Sensitivity Tests ; Microorganisms ; Mutation ; Nosocomial infection ; Nosocomial infections ; Nucleotide sequence ; Paraquat ; Paraquat - pharmacology ; Phenotypes ; Physiological aspects ; Point mutation ; Proteins ; Quinolones ; Regulatory sequences ; Ribosomal protein L1 ; Scientific equipment and supplies industry ; Sequence analysis ; Stenotrophomonas maltophilia ; Stenotrophomonas maltophilia - drug effects ; Stenotrophomonas maltophilia - genetics ; Testing ; Weed control</subject><ispartof>PloS one, 2024-08, Vol.19 (8), p.e0309525</ispartof><rights>Copyright: © 2024 Vanitshavit et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Vanitshavit et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Vanitshavit et al 2024 Vanitshavit et al</rights><rights>2024 Vanitshavit et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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><cites>FETCH-LOGICAL-c506t-93f5faccc170a65ea0b581fbb366171a3997a40718fcf7fd4482a2ce313810343</cites><orcidid>0000-0002-4034-3468 ; 0000-0001-8744-4963</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/PMC11356428/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11356428/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39196988$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Hosseini, Seyed Mostafa</contributor><creatorcontrib>Vanitshavit, Veerakit</creatorcontrib><creatorcontrib>Charoenlap, Nisanart</creatorcontrib><creatorcontrib>Sallabhan, Ratiboot</creatorcontrib><creatorcontrib>Whangsuk, Wirongrong</creatorcontrib><creatorcontrib>Bhinija, Kisana</creatorcontrib><creatorcontrib>Dulyayangkul, Punyawee</creatorcontrib><creatorcontrib>Mongkolsuk, Skorn</creatorcontrib><creatorcontrib>Vattanavibooon, Paiboon</creatorcontrib><title>Acquired resistance of Stenotrophomonas maltophilia to antimicrobials induced by herbicide paraquat dichloride</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Stenotrophomonas maltophilia, a ubiquitous environmental bacterium, is an important cause of nosocomial infections. Although banned in some countries, paraquat (PQ) is commonly used to control weeds. In this study, we investigated the effects of increasing concentrations of PQ on S. maltophilia and its antimicrobial resistance. The sequential exposure of S. maltophilia K279a to increasing concentrations of PQ induces the formation of strains with increased resistance to PQ. Among the 400 PQ-resistant isolates tested, 70 clones were resistant to 16 μg/ml ciprofloxacin (CIP), and around 18% of the PQ/CIP-resistant isolates showed increased resistance to all the tested antimicrobials including, the aminoglycosides, quinolones, cephalosporin, chloramphenicol, and co-trimoxazole. The results of the expression analysis of the antimicrobial resistance genes in the five selected PQ/CIP-resistant isolates demonstrated the high expression of genes encoding efflux pumps (smeYZ, smaAB, smaCDEF, smeDEF, smeVWX, and smtcrA) and the enzymes aph(3')-IIc, blaL1, and blaL2. However, expression of the genes known for PQ resistance (i.e., mfsA and sod) were not altered relative to the wild-type levels. Whole genome sequence analysis identified gene mutations that could account for the antimicrobial resistance, namely, smeT (TetR family regulatory protein), rplA (ribosomal protein L1), and acnA (aconitase A). Ectopic expression of wild-type AcnA partially complemented the fluoroquinolone-resistant phenotype of the mutant with mutated acnA, which suggests the role of aconitase A in antimicrobial susceptibility. 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content 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>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vanitshavit, Veerakit</au><au>Charoenlap, Nisanart</au><au>Sallabhan, Ratiboot</au><au>Whangsuk, Wirongrong</au><au>Bhinija, Kisana</au><au>Dulyayangkul, Punyawee</au><au>Mongkolsuk, Skorn</au><au>Vattanavibooon, Paiboon</au><au>Hosseini, Seyed Mostafa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Acquired resistance of Stenotrophomonas maltophilia to antimicrobials induced by herbicide paraquat dichloride</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2024-08-28</date><risdate>2024</risdate><volume>19</volume><issue>8</issue><spage>e0309525</spage><pages>e0309525-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Stenotrophomonas maltophilia, a ubiquitous environmental bacterium, is an important cause of nosocomial infections. Although banned in some countries, paraquat (PQ) is commonly used to control weeds. In this study, we investigated the effects of increasing concentrations of PQ on S. maltophilia and its antimicrobial resistance. The sequential exposure of S. maltophilia K279a to increasing concentrations of PQ induces the formation of strains with increased resistance to PQ. Among the 400 PQ-resistant isolates tested, 70 clones were resistant to 16 μg/ml ciprofloxacin (CIP), and around 18% of the PQ/CIP-resistant isolates showed increased resistance to all the tested antimicrobials including, the aminoglycosides, quinolones, cephalosporin, chloramphenicol, and co-trimoxazole. The results of the expression analysis of the antimicrobial resistance genes in the five selected PQ/CIP-resistant isolates demonstrated the high expression of genes encoding efflux pumps (smeYZ, smaAB, smaCDEF, smeDEF, smeVWX, and smtcrA) and the enzymes aph(3')-IIc, blaL1, and blaL2. However, expression of the genes known for PQ resistance (i.e., mfsA and sod) were not altered relative to the wild-type levels. Whole genome sequence analysis identified gene mutations that could account for the antimicrobial resistance, namely, smeT (TetR family regulatory protein), rplA (ribosomal protein L1), and acnA (aconitase A). Ectopic expression of wild-type AcnA partially complemented the fluoroquinolone-resistant phenotype of the mutant with mutated acnA, which suggests the role of aconitase A in antimicrobial susceptibility. Exposure of S. maltophilia to PQ thus induces the development of strains that increase resistance to multiple antimicrobials.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39196988</pmid><doi>10.1371/journal.pone.0309525</doi><tpages>e0309525</tpages><orcidid>https://orcid.org/0000-0002-4034-3468</orcidid><orcidid>https://orcid.org/0000-0001-8744-4963</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2024-08, Vol.19 (8), p.e0309525 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_3098198524 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amino acid sequence Aminoglycosides Analysis Anti-Bacterial Agents - pharmacology Antibiotics Antimicrobial agents Antimicrobial resistance Bacterial Proteins - genetics Bacterial Proteins - metabolism Biology and Life Sciences Blood proteins Cephalosporins Chloramphenicol Chloromycetin Ciprofloxacin Ciprofloxacin - pharmacology Cotrimoxazole Dichlorides Drug resistance Drug resistance in microorganisms Drug Resistance, Bacterial - drug effects Drug Resistance, Bacterial - genetics Drug Resistance, Multiple, Bacterial - genetics Ectopic expression Efflux Environmental aspects Enzymes Genes Genetic aspects Genomes Genomic analysis Gram-negative bacteria Health aspects Herbicide resistance Herbicides Herbicides - pharmacology Influence Medicine and Health Sciences Microbial Sensitivity Tests Microorganisms Mutation Nosocomial infection Nosocomial infections Nucleotide sequence Paraquat Paraquat - pharmacology Phenotypes Physiological aspects Point mutation Proteins Quinolones Regulatory sequences Ribosomal protein L1 Scientific equipment and supplies industry Sequence analysis Stenotrophomonas maltophilia Stenotrophomonas maltophilia - drug effects Stenotrophomonas maltophilia - genetics Testing Weed control |
| title | Acquired resistance of Stenotrophomonas maltophilia to antimicrobials induced by herbicide paraquat dichloride |
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