Characterization of Proteus mirabilis and associated plasmids isolated from anaerobic dairy cattle manure digesters
Proteus mirabilis is an opportunistic pathogen associated with a variety of human infections, including urinary tract infections. The prevalence of P. mirabilis in foods of animal origin and in the manure by-products created in animal production is not well documented. Further, the prevalence and pe...
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description | Proteus mirabilis is an opportunistic pathogen associated with a variety of human infections, including urinary tract infections. The prevalence of P. mirabilis in foods of animal origin and in the manure by-products created in animal production is not well documented. Further, the prevalence and persistence of extended-spectrum cephalosporin (ESC) resistant P. mirabilis is largely unknown. In this study, we characterized ESC-resistant P. mirabilis recovered from various stages of dairy manure anaerobic digestion. Isolates were screened by PCR for blaCTX-M, blaCMY and blaSHV, and antimicrobial susceptibility testing was performed. Fifty-six P. mirabilis carrying CTX-M were sequenced with short and long read sequencing technologies, and the assembled chromosomes and plasmids were compared. ESC-resistant Proteus was found in four of the six manure digesters, an indication that not all digesters were colonized with resistant strains. Both CTX-M-1 and CTX-M-15 plasmids were found in P. mirabilis isolates. Transfer of plasmid DNA by conjugation was also explored, with ESC-resistance plasmids able to transfer to Escherichia coli at high frequency. We concluded that P. mirabilis can harbour and transfer ESC-resistance genes and plasmids, and may be an overlooked reservoir of antimicrobial resistance. |
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The prevalence of P. mirabilis in foods of animal origin and in the manure by-products created in animal production is not well documented. Further, the prevalence and persistence of extended-spectrum cephalosporin (ESC) resistant P. mirabilis is largely unknown. In this study, we characterized ESC-resistant P. mirabilis recovered from various stages of dairy manure anaerobic digestion. Isolates were screened by PCR for blaCTX-M, blaCMY and blaSHV, and antimicrobial susceptibility testing was performed. Fifty-six P. mirabilis carrying CTX-M were sequenced with short and long read sequencing technologies, and the assembled chromosomes and plasmids were compared. ESC-resistant Proteus was found in four of the six manure digesters, an indication that not all digesters were colonized with resistant strains. Both CTX-M-1 and CTX-M-15 plasmids were found in P. mirabilis isolates. Transfer of plasmid DNA by conjugation was also explored, with ESC-resistance plasmids able to transfer to Escherichia coli at high frequency. We concluded that P. mirabilis can harbour and transfer ESC-resistance genes and plasmids, and may be an overlooked reservoir of antimicrobial resistance.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0289703</identifier><identifier>PMID: 37561682</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anaerobic digestion ; Anaerobiosis ; Animal production ; Animals ; Anti-Bacterial Agents - pharmacology ; Anti-Infective Agents ; Antimicrobial agents ; Antimicrobial resistance ; Bacteria ; Bar codes ; beta-Lactamases - genetics ; Biology and Life Sciences ; Cattle ; Cattle manure ; Cephaloridine ; Cephalosporins ; Chromosomes ; Complications and side effects ; Computer and Information Sciences ; Conjugation ; Dairy cattle ; Deoxyribonucleic acid ; Digesters ; DNA ; Drug resistance ; Drug resistance in microorganisms ; E coli ; Escherichia coli - genetics ; Farms ; Genes ; Genomes ; Health aspects ; Humans ; Infections ; Manure ; Manures ; Medicine and Health Sciences ; Moxalactam ; Opportunist infection ; Patient outcomes ; Plasmids ; Plasmids - genetics ; Proteus mirabilis ; Proteus mirabilis - genetics ; Research and Analysis Methods ; Tetracycline ; Tetracyclines ; Urinary tract ; Urinary tract infections</subject><ispartof>PloS one, 2023-08, Vol.18 (8), p.e0289703-e0289703</ispartof><rights>Copyright: © 2023 Chalmers 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 2023 Public Library of Science</rights><rights>2023 Chalmers 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>2023 Chalmers et al 2023 Chalmers et al</rights><rights>2023 Chalmers 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-c576t-8c4b475adf798fad32645653ced0a48a8b7c8917ac59e405afd41550642af7963</cites><orcidid>0000-0002-6651-4253 ; 0000-0002-9411-5153</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/PMC10414651/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10414651/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37561682$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Aworh, Mabel Kamweli</contributor><creatorcontrib>Chalmers, Gabhan</creatorcontrib><creatorcontrib>Anderson, Rebecca E V</creatorcontrib><creatorcontrib>Murray, Roger</creatorcontrib><creatorcontrib>Topp, Edward</creatorcontrib><creatorcontrib>Boerlin, Patrick</creatorcontrib><title>Characterization of Proteus mirabilis and associated plasmids isolated from anaerobic dairy cattle manure digesters</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Proteus mirabilis is an opportunistic pathogen associated with a variety of human infections, including urinary tract infections. The prevalence of P. mirabilis in foods of animal origin and in the manure by-products created in animal production is not well documented. Further, the prevalence and persistence of extended-spectrum cephalosporin (ESC) resistant P. mirabilis is largely unknown. In this study, we characterized ESC-resistant P. mirabilis recovered from various stages of dairy manure anaerobic digestion. Isolates were screened by PCR for blaCTX-M, blaCMY and blaSHV, and antimicrobial susceptibility testing was performed. Fifty-six P. mirabilis carrying CTX-M were sequenced with short and long read sequencing technologies, and the assembled chromosomes and plasmids were compared. ESC-resistant Proteus was found in four of the six manure digesters, an indication that not all digesters were colonized with resistant strains. Both CTX-M-1 and CTX-M-15 plasmids were found in P. mirabilis isolates. Transfer of plasmid DNA by conjugation was also explored, with ESC-resistance plasmids able to transfer to Escherichia coli at high frequency. We concluded that P. mirabilis can harbour and transfer ESC-resistance genes and plasmids, and may be an overlooked reservoir of antimicrobial resistance.</description><subject>Anaerobic digestion</subject><subject>Anaerobiosis</subject><subject>Animal production</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Infective Agents</subject><subject>Antimicrobial agents</subject><subject>Antimicrobial resistance</subject><subject>Bacteria</subject><subject>Bar codes</subject><subject>beta-Lactamases - genetics</subject><subject>Biology and Life Sciences</subject><subject>Cattle</subject><subject>Cattle manure</subject><subject>Cephaloridine</subject><subject>Cephalosporins</subject><subject>Chromosomes</subject><subject>Complications and side effects</subject><subject>Computer and Information Sciences</subject><subject>Conjugation</subject><subject>Dairy cattle</subject><subject>Deoxyribonucleic acid</subject><subject>Digesters</subject><subject>DNA</subject><subject>Drug resistance</subject><subject>Drug resistance in microorganisms</subject><subject>E coli</subject><subject>Escherichia coli - 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pharmacology</topic><topic>Anti-Infective Agents</topic><topic>Antimicrobial agents</topic><topic>Antimicrobial resistance</topic><topic>Bacteria</topic><topic>Bar codes</topic><topic>beta-Lactamases - genetics</topic><topic>Biology and Life Sciences</topic><topic>Cattle</topic><topic>Cattle manure</topic><topic>Cephaloridine</topic><topic>Cephalosporins</topic><topic>Chromosomes</topic><topic>Complications and side effects</topic><topic>Computer and Information Sciences</topic><topic>Conjugation</topic><topic>Dairy cattle</topic><topic>Deoxyribonucleic acid</topic><topic>Digesters</topic><topic>DNA</topic><topic>Drug resistance</topic><topic>Drug resistance in microorganisms</topic><topic>E coli</topic><topic>Escherichia coli - genetics</topic><topic>Farms</topic><topic>Genes</topic><topic>Genomes</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Infections</topic><topic>Manure</topic><topic>Manures</topic><topic>Medicine and Health Sciences</topic><topic>Moxalactam</topic><topic>Opportunist infection</topic><topic>Patient outcomes</topic><topic>Plasmids</topic><topic>Plasmids - 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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>Chalmers, Gabhan</au><au>Anderson, Rebecca E V</au><au>Murray, Roger</au><au>Topp, Edward</au><au>Boerlin, Patrick</au><au>Aworh, Mabel Kamweli</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of Proteus mirabilis and associated plasmids isolated from anaerobic dairy cattle manure digesters</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-08-10</date><risdate>2023</risdate><volume>18</volume><issue>8</issue><spage>e0289703</spage><epage>e0289703</epage><pages>e0289703-e0289703</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Proteus mirabilis is an opportunistic pathogen associated with a variety of human infections, including urinary tract infections. The prevalence of P. mirabilis in foods of animal origin and in the manure by-products created in animal production is not well documented. Further, the prevalence and persistence of extended-spectrum cephalosporin (ESC) resistant P. mirabilis is largely unknown. In this study, we characterized ESC-resistant P. mirabilis recovered from various stages of dairy manure anaerobic digestion. Isolates were screened by PCR for blaCTX-M, blaCMY and blaSHV, and antimicrobial susceptibility testing was performed. Fifty-six P. mirabilis carrying CTX-M were sequenced with short and long read sequencing technologies, and the assembled chromosomes and plasmids were compared. ESC-resistant Proteus was found in four of the six manure digesters, an indication that not all digesters were colonized with resistant strains. Both CTX-M-1 and CTX-M-15 plasmids were found in P. mirabilis isolates. Transfer of plasmid DNA by conjugation was also explored, with ESC-resistance plasmids able to transfer to Escherichia coli at high frequency. We concluded that P. mirabilis can harbour and transfer ESC-resistance genes and plasmids, and may be an overlooked reservoir of antimicrobial resistance.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37561682</pmid><doi>10.1371/journal.pone.0289703</doi><tpages>e0289703</tpages><orcidid>https://orcid.org/0000-0002-6651-4253</orcidid><orcidid>https://orcid.org/0000-0002-9411-5153</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anaerobic digestion Anaerobiosis Animal production Animals Anti-Bacterial Agents - pharmacology Anti-Infective Agents Antimicrobial agents Antimicrobial resistance Bacteria Bar codes beta-Lactamases - genetics Biology and Life Sciences Cattle Cattle manure Cephaloridine Cephalosporins Chromosomes Complications and side effects Computer and Information Sciences Conjugation Dairy cattle Deoxyribonucleic acid Digesters DNA Drug resistance Drug resistance in microorganisms E coli Escherichia coli - genetics Farms Genes Genomes Health aspects Humans Infections Manure Manures Medicine and Health Sciences Moxalactam Opportunist infection Patient outcomes Plasmids Plasmids - genetics Proteus mirabilis Proteus mirabilis - genetics Research and Analysis Methods Tetracycline Tetracyclines Urinary tract Urinary tract infections |
title | Characterization of Proteus mirabilis and associated plasmids isolated from anaerobic dairy cattle manure digesters |
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