Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis
Gastrointestinal carriage of multidrug-resistant (MDR) bacteria is one of the main risk factors for developing serious, difficult-to-treat infections. Given that there is currently no all-round solution to eliminate colonization with MDR bacteria, it is particularly important to understand the dynam...
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| Format: | Article |
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MDPI AG
2021-03-01
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| Series: | Antibiotics |
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| Online Access: | https://www.mdpi.com/2079-6382/10/3/268 |
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| author | János Juhász Balázs Ligeti Márió Gajdács Nóra Makra Eszter Ostorházi Ferenc Balázs Farkas Balázs Stercz Ákos Tóth Judit Domokos Sándor Pongor Dóra Szabó |
| author_facet | János Juhász Balázs Ligeti Márió Gajdács Nóra Makra Eszter Ostorházi Ferenc Balázs Farkas Balázs Stercz Ákos Tóth Judit Domokos Sándor Pongor Dóra Szabó |
| author_sort | János Juhász |
| collection | DOAJ |
| description | Gastrointestinal carriage of multidrug-resistant (MDR) bacteria is one of the main risk factors for developing serious, difficult-to-treat infections. Given that there is currently no all-round solution to eliminate colonization with MDR bacteria, it is particularly important to understand the dynamic process of colonization to aid the development of novel decolonization strategies. The aim of our present study was to perform metataxonomic analyses of gut microbiota dynamics during colonization with an extended-spectrum β-lactamase (ESBL)- and carbapenemase-producing <i>Klebsiella pneumoniae</i> (ECKP) strain in mice; additionally, to ascertain the effects of antibiotic administration (ampicillin, ceftazidime, and ciprofloxacin) on the establishment and elimination of ECKP intestinal colonization. We have found that the phyla Bacteroidetes and Firmicutes were most dominant in all of the treatment groups; however, Bacteroidetes was more common in the groups treated with antibiotics compared to the control group. Significant differences were observed among the different antibiotic-treated groups in beta but not alpha diversity, implying that the difference is the relative abundance of some bacterial community members. Bacteria from the <i>Lachnospiraceae</i> family (including <i>Agathobacter</i>, <i>Anaerostipes</i>, <i>Lachnoclostridium</i> 11308, <i>Lachnospiraceae</i> UCG-004, <i>Lachnospiraceae</i> NK3A20 group 11318, <i>Lachnospiraceae</i> NK4A136 group 11319, <i>Roseburia,</i> and <i>Tyzzerella</i>) showed an inverse relationship with the carriage rate of the ECKP strain, whereas members of Enterobacteriaceae and the ECKP strain have shown a correlational relationship. Our results suggest that the composition of the microbial community plays a primary role in the MDR-colonization rate, whereas the antibiotic susceptibility of individual MDR strains affects this process to a lesser extent. Distinct bacterial families have associated into microbial clusters, collecting taxonomically close species to produce survival benefits in the gut. These associations do not develop at random, as they may be attributed to the presence of specific metabolomic networks. A new concept should be introduced in designing future endeavors for MDR decolonization, supplemented by knowledge of the composition of the host bacterial community and the identification of bacterial clusters capable of suppressing or enhancing the invader species. |
| first_indexed | 2024-03-09T05:07:20Z |
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| id | doaj.art-c5af822280454e1d939d99a20733189a |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-09T05:07:20Z |
| publishDate | 2021-03-01 |
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| series | Antibiotics |
| spelling | doaj.art-c5af822280454e1d939d99a20733189a2023-12-03T12:53:54ZengMDPI AGAntibiotics2079-63822021-03-0110326810.3390/antibiotics10030268Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic AnalysisJános Juhász0Balázs Ligeti1Márió Gajdács2Nóra Makra3Eszter Ostorházi4Ferenc Balázs Farkas5Balázs Stercz6Ákos Tóth7Judit Domokos8Sándor Pongor9Dóra Szabó10Institute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryDepartment of Bacteriology, Mycology and Parasitology, National Public Health Centre, Albert Flórián út 2-6, 1097 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryFaculty of Information Technology and Bionics, Pázmány Péter Catholic University, Práter utca 50/A, 1083 Budapest, HungaryInstitute of Medical Microbiology, Faculty of Medicine, Semmelweis University, Nagyvárad tér 4., 1089 Budapest, HungaryGastrointestinal carriage of multidrug-resistant (MDR) bacteria is one of the main risk factors for developing serious, difficult-to-treat infections. Given that there is currently no all-round solution to eliminate colonization with MDR bacteria, it is particularly important to understand the dynamic process of colonization to aid the development of novel decolonization strategies. The aim of our present study was to perform metataxonomic analyses of gut microbiota dynamics during colonization with an extended-spectrum β-lactamase (ESBL)- and carbapenemase-producing <i>Klebsiella pneumoniae</i> (ECKP) strain in mice; additionally, to ascertain the effects of antibiotic administration (ampicillin, ceftazidime, and ciprofloxacin) on the establishment and elimination of ECKP intestinal colonization. We have found that the phyla Bacteroidetes and Firmicutes were most dominant in all of the treatment groups; however, Bacteroidetes was more common in the groups treated with antibiotics compared to the control group. Significant differences were observed among the different antibiotic-treated groups in beta but not alpha diversity, implying that the difference is the relative abundance of some bacterial community members. Bacteria from the <i>Lachnospiraceae</i> family (including <i>Agathobacter</i>, <i>Anaerostipes</i>, <i>Lachnoclostridium</i> 11308, <i>Lachnospiraceae</i> UCG-004, <i>Lachnospiraceae</i> NK3A20 group 11318, <i>Lachnospiraceae</i> NK4A136 group 11319, <i>Roseburia,</i> and <i>Tyzzerella</i>) showed an inverse relationship with the carriage rate of the ECKP strain, whereas members of Enterobacteriaceae and the ECKP strain have shown a correlational relationship. Our results suggest that the composition of the microbial community plays a primary role in the MDR-colonization rate, whereas the antibiotic susceptibility of individual MDR strains affects this process to a lesser extent. Distinct bacterial families have associated into microbial clusters, collecting taxonomically close species to produce survival benefits in the gut. These associations do not develop at random, as they may be attributed to the presence of specific metabolomic networks. A new concept should be introduced in designing future endeavors for MDR decolonization, supplemented by knowledge of the composition of the host bacterial community and the identification of bacterial clusters capable of suppressing or enhancing the invader species.https://www.mdpi.com/2079-6382/10/3/268colonizationdecolonizationgut microbiotamicrobiota-clusterantibiotic-induced microbiota alterationmetataxonomic analysis |
| spellingShingle | János Juhász Balázs Ligeti Márió Gajdács Nóra Makra Eszter Ostorházi Ferenc Balázs Farkas Balázs Stercz Ákos Tóth Judit Domokos Sándor Pongor Dóra Szabó Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis Antibiotics colonization decolonization gut microbiota microbiota-cluster antibiotic-induced microbiota alteration metataxonomic analysis |
| title | Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis |
| title_full | Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis |
| title_fullStr | Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis |
| title_full_unstemmed | Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis |
| title_short | Colonization Dynamics of Multidrug-Resistant <i>Klebsiella pneumoniae</i> Are Dictated by Microbiota-Cluster Group Behavior over Individual Antibiotic Susceptibility: A Metataxonomic Analysis |
| title_sort | colonization dynamics of multidrug resistant i klebsiella pneumoniae i are dictated by microbiota cluster group behavior over individual antibiotic susceptibility a metataxonomic analysis |
| topic | colonization decolonization gut microbiota microbiota-cluster antibiotic-induced microbiota alteration metataxonomic analysis |
| url | https://www.mdpi.com/2079-6382/10/3/268 |
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