Agnete Kirstine Karlsmose , Mirena Ivanova , Martin Laage Kragh , Jette Sejer Kjeldgaard , Saria Otani , Christina Aaby Svendsen , Bojan Papić , Irena Zdovc , Taurai Tasara , Roger Stephan , Even Heir , Solveig Langsrud , Trond Møretrø , Paw Dalgaard , Annette Fagerlund , Lisbeth Truelstrup Hansen , Frank M. Aarestrup , Pimlapas Leekitcharoenphon
{"title":"新型元基因组学方法发现噬菌体基因是混合李斯特菌群落对消毒剂耐受性增强的标志。","authors":"Agnete Kirstine Karlsmose , Mirena Ivanova , Martin Laage Kragh , Jette Sejer Kjeldgaard , Saria Otani , Christina Aaby Svendsen , Bojan Papić , Irena Zdovc , Taurai Tasara , Roger Stephan , Even Heir , Solveig Langsrud , Trond Møretrø , Paw Dalgaard , Annette Fagerlund , Lisbeth Truelstrup Hansen , Frank M. Aarestrup , Pimlapas Leekitcharoenphon","doi":"10.1016/j.meegid.2024.105582","DOIUrl":null,"url":null,"abstract":"<div><p><em>Listeria monocytogenes</em> is an important human pathogen with a high mortality rate. Consumption of contaminated ready-to-eat food is the main mode of transmission to humans. Disinfectant-tolerant <em>L. monocytogenes</em> have emerged, which are believed to have increased persistence potential. Elucidating the mechanisms of <em>L. monocytogenes</em> disinfectant tolerance has been the focus of previous studies using pure cultures. A limitation of such approach is the difficulty to identify strains with reduced susceptibility due to inter-strain variation and the need to screen large numbers of strains and genes. In this study, we applied a novel metagenomic approach to detect genes associated with disinfectant tolerance in mixed <em>L. monocytogenes</em> planktonic communities. Two communities, consisting of 71 and 80 isolates each, were treated with the food industry disinfectants benzalkonium chloride (BC, 1.75 mg/L) or peracetic acid (PAA, 38 mg/L). The communities were subjected to metagenomic sequencing and differences in individual gene abundances between biocide-free control communities and biocide-treated communities were determined. A significant increase in the abundance of <em>Listeria</em> phage-associated genes was observed in both communities after treatment, suggesting that prophage carriage could lead to an increased disinfectant tolerance in mixed <em>L. monocytogenes</em> planktonic communities. In contrast, a significant decrease in the abundance of a high-copy <em>emrC</em>-harbouring plasmid pLmN12–0935 was observed in both communities after treatment. In PAA-treated community, a putative ABC transporter previously found to be necessary for <em>L. monocytogenes</em> resistance to antimicrobial agents and virulence, was among the genes with the highest weight for differentiating treated from control samples. The undertaken metagenomic approach in this study can be applied to identify genes associated with increased tolerance to other antimicrobials in mixed bacterial communities.</p></div>","PeriodicalId":54986,"journal":{"name":"Infection Genetics and Evolution","volume":null,"pages":null},"PeriodicalIF":2.6000,"publicationDate":"2024-03-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1567134824000339/pdfft?md5=d29bdf734f1f64e625b2ad9f51504162&pid=1-s2.0-S1567134824000339-main.pdf","citationCount":"0","resultStr":"{\"title\":\"A novel metagenomic approach uncovers phage genes as markers for increased disinfectant tolerance in mixed Listeria monocytogenes communities\",\"authors\":\"Agnete Kirstine Karlsmose , Mirena Ivanova , Martin Laage Kragh , Jette Sejer Kjeldgaard , Saria Otani , Christina Aaby Svendsen , Bojan Papić , Irena Zdovc , Taurai Tasara , Roger Stephan , Even Heir , Solveig Langsrud , Trond Møretrø , Paw Dalgaard , Annette Fagerlund , Lisbeth Truelstrup Hansen , Frank M. Aarestrup , Pimlapas Leekitcharoenphon\",\"doi\":\"10.1016/j.meegid.2024.105582\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><p><em>Listeria monocytogenes</em> is an important human pathogen with a high mortality rate. Consumption of contaminated ready-to-eat food is the main mode of transmission to humans. Disinfectant-tolerant <em>L. monocytogenes</em> have emerged, which are believed to have increased persistence potential. Elucidating the mechanisms of <em>L. monocytogenes</em> disinfectant tolerance has been the focus of previous studies using pure cultures. A limitation of such approach is the difficulty to identify strains with reduced susceptibility due to inter-strain variation and the need to screen large numbers of strains and genes. In this study, we applied a novel metagenomic approach to detect genes associated with disinfectant tolerance in mixed <em>L. monocytogenes</em> planktonic communities. Two communities, consisting of 71 and 80 isolates each, were treated with the food industry disinfectants benzalkonium chloride (BC, 1.75 mg/L) or peracetic acid (PAA, 38 mg/L). The communities were subjected to metagenomic sequencing and differences in individual gene abundances between biocide-free control communities and biocide-treated communities were determined. A significant increase in the abundance of <em>Listeria</em> phage-associated genes was observed in both communities after treatment, suggesting that prophage carriage could lead to an increased disinfectant tolerance in mixed <em>L. monocytogenes</em> planktonic communities. In contrast, a significant decrease in the abundance of a high-copy <em>emrC</em>-harbouring plasmid pLmN12–0935 was observed in both communities after treatment. In PAA-treated community, a putative ABC transporter previously found to be necessary for <em>L. monocytogenes</em> resistance to antimicrobial agents and virulence, was among the genes with the highest weight for differentiating treated from control samples. 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A novel metagenomic approach uncovers phage genes as markers for increased disinfectant tolerance in mixed Listeria monocytogenes communities
Listeria monocytogenes is an important human pathogen with a high mortality rate. Consumption of contaminated ready-to-eat food is the main mode of transmission to humans. Disinfectant-tolerant L. monocytogenes have emerged, which are believed to have increased persistence potential. Elucidating the mechanisms of L. monocytogenes disinfectant tolerance has been the focus of previous studies using pure cultures. A limitation of such approach is the difficulty to identify strains with reduced susceptibility due to inter-strain variation and the need to screen large numbers of strains and genes. In this study, we applied a novel metagenomic approach to detect genes associated with disinfectant tolerance in mixed L. monocytogenes planktonic communities. Two communities, consisting of 71 and 80 isolates each, were treated with the food industry disinfectants benzalkonium chloride (BC, 1.75 mg/L) or peracetic acid (PAA, 38 mg/L). The communities were subjected to metagenomic sequencing and differences in individual gene abundances between biocide-free control communities and biocide-treated communities were determined. A significant increase in the abundance of Listeria phage-associated genes was observed in both communities after treatment, suggesting that prophage carriage could lead to an increased disinfectant tolerance in mixed L. monocytogenes planktonic communities. In contrast, a significant decrease in the abundance of a high-copy emrC-harbouring plasmid pLmN12–0935 was observed in both communities after treatment. In PAA-treated community, a putative ABC transporter previously found to be necessary for L. monocytogenes resistance to antimicrobial agents and virulence, was among the genes with the highest weight for differentiating treated from control samples. The undertaken metagenomic approach in this study can be applied to identify genes associated with increased tolerance to other antimicrobials in mixed bacterial communities.
期刊介绍:
(aka Journal of Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases -- MEEGID)
Infectious diseases constitute one of the main challenges to medical science in the coming century. The impressive development of molecular megatechnologies and of bioinformatics have greatly increased our knowledge of the evolution, transmission and pathogenicity of infectious diseases. Research has shown that host susceptibility to many infectious diseases has a genetic basis. Furthermore, much is now known on the molecular epidemiology, evolution and virulence of pathogenic agents, as well as their resistance to drugs, vaccines, and antibiotics. Equally, research on the genetics of disease vectors has greatly improved our understanding of their systematics, has increased our capacity to identify target populations for control or intervention, and has provided detailed information on the mechanisms of insecticide resistance.
However, the genetics and evolutionary biology of hosts, pathogens and vectors have tended to develop as three separate fields of research. This artificial compartmentalisation is of concern due to our growing appreciation of the strong co-evolutionary interactions among hosts, pathogens and vectors.
Infection, Genetics and Evolution and its companion congress [MEEGID](http://www.meegidconference.com/) (for Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases) are the main forum acting for the cross-fertilization between evolutionary science and biomedical research on infectious diseases.
Infection, Genetics and Evolution is the only journal that welcomes articles dealing with the genetics and evolutionary biology of hosts, pathogens and vectors, and coevolution processes among them in relation to infection and disease manifestation. All infectious models enter the scope of the journal, including pathogens of humans, animals and plants, either parasites, fungi, bacteria, viruses or prions. The journal welcomes articles dealing with genetics, population genetics, genomics, postgenomics, gene expression, evolutionary biology, population dynamics, mathematical modeling and bioinformatics. We also provide many author benefits, such as free PDFs, a liberal copyright policy, special discounts on Elsevier publications and much more. Please click here for more information on our author services .