The Roles of a Multidrug-Resistant Klebsiella pneumoniae High-Risk Clone and Its Resistance Plasmids on the Gastrointestinal Colonization and Host-Defense Effectors in the Gut
The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing ST15 (MDR-KP) strain, as...
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| Published in: | Antibiotics (Basel) Vol. 13; no. 8; p. 698 |
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| Abstract | The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing
ST15 (MDR-KP) strain, as well as
J53 (EC) and
transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the
phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas
was dominant in EC. The
family was significantly more common in the MDR-KP and EC-OXA groups, while the
family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the
family members exhibited a correlation with the IncL plasmid. The detected amounts of the
family indicated the protective role against the high-risk clone and the resistance plasmids' dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut. |
|---|---|
| AbstractList | The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing Klebsiella pneumoniae ST15 (MDR-KP) strain, as well as Escherichia coli J53 (EC) and E. coli transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the Bacteroidota phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas Proteobacteria was dominant in EC. The Muribaculaceae family was significantly more common in the MDR-KP and EC-OXA groups, while the Lachnospiraceae family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the Muribaculaceae family members exhibited a correlation with the IncL plasmid. The detected amounts of the Lachnospiraceae family indicated the protective role against the high-risk clone and the resistance plasmids’ dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut. The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing Klebsiella pneumoniae ST15 (MDR-KP) strain, as well as Escherichia coli J53 (EC) and E. coli transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the Bacteroidota phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas Proteobacteria was dominant in EC. The Muribaculaceae family was significantly more common in the MDR-KP and EC-OXA groups, while the Lachnospiraceae family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the Muribaculaceae family members exhibited a correlation with the IncL plasmid. The detected amounts of the Lachnospiraceae family indicated the protective role against the high-risk clone and the resistance plasmids’ dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut. The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing ST15 (MDR-KP) strain, as well as J53 (EC) and transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas was dominant in EC. The family was significantly more common in the MDR-KP and EC-OXA groups, while the family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the family members exhibited a correlation with the IncL plasmid. The detected amounts of the family indicated the protective role against the high-risk clone and the resistance plasmids' dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut. The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing Klebsiella pneumoniae ST15 (MDR-KP) strain, as well as Escherichia coli J53 (EC) and E. coli transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the Bacteroidota phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas Proteobacteria was dominant in EC. The Muribaculaceae family was significantly more common in the MDR-KP and EC-OXA groups, while the Lachnospiraceae family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the Muribaculaceae family members exhibited a correlation with the IncL plasmid. The detected amounts of the Lachnospiraceae family indicated the protective role against the high-risk clone and the resistance plasmids' dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut.The asymptomatic gastrointestinal colonization of multidrug-resistant (MDR) bacteria can lead to difficult-to-treat infections. We investigated the role of host factors influencing colonization in an orogastrical murine infection model using a CTX-M-15- and OXA-162-producing Klebsiella pneumoniae ST15 (MDR-KP) strain, as well as Escherichia coli J53 (EC) and E. coli transconjugants with an IncFII(K) plasmid carrying CTX-M-15 (EC-CTXM), and with an IncL plasmid carrying OXA-162 (EC-OXA) genes. The fecal bacterial count in colony-forming unit/gram stool (CFU/g) was determined by cultivation, IgA and defensin levels by ELISA, and gut microbiota by 16S rRNA analysis. The CFU was the lowest in EC, followed by EC-OXA and EC-CTXM, and the highest in the MDR-KP group. The IgA level in feces increased in MDR-KP, EC-CTXM, and EC-OXA, and did not change in EC. The beta-defensin 3 level markedly increased in all groups, with the highest values in MDR-KP and EC-CTXM. Alpha-defensin-5 increased in all groups especially in EC. In microbiota, the Bacteroidota phylum was dominant in MDR-KP, EC-CTXM, and EC-OXA, whereas Proteobacteria was dominant in EC. The Muribaculaceae family was significantly more common in the MDR-KP and EC-OXA groups, while the Lachnospiraceae family was dominant in the EC group. While fecal IgA levels positively correlated with colonizing bacterial CFU, the alpha-defensin 5 levels inversely correlated with CFUs and IgA levels. The presence of the IncFII(K) plasmid induced beta-defensin 3 production. The amounts of the Muribaculaceae family members exhibited a correlation with the IncL plasmid. The detected amounts of the Lachnospiraceae family indicated the protective role against the high-risk clone and the resistance plasmids' dissemination. Our results suggest that not only the MDR-KP clone itself but also the resistance plasmids play a primary role in the colonization rate in the gastrointestinal tract. Both the MDR-KP clone as well as the IncFII(K) and IncL resistance plasmids provide survival and colonization benefits in the gut. |
| Audience | Academic |
| Author | Kocsis, Bela Juhasz, Janos Szabo, Dora Ostorhazi, Eszter Stercz, Balazs Domokos, Judit Makra, Nora Dunai, Zsuzsanna A |
| AuthorAffiliation | 1 Institute of Medical Microbiology, Semmelweis University, 1089 Budapest, Hungary; stercz.balazs@semmelweis.hu (B.S.); domokos.judit@semmelweis.hu (J.D.); makra.nora@semmelweis.hu (N.M.); juhaszjanos4@gmail.com (J.J.); ostorhazi.eszter@semmelweis.hu (E.O.); kocsis.bela@semmelweis.hu (B.K.) 3 Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, 1083 Budapest, Hungary 2 HUN-REN-SU Human Microbiota Research Group, 1052 Budapest, Hungary; zsuzsanna.dunai@gmail.com 4 Neurosurgical and Neurointervention Clinic, Semmelweis University, 1083 Budapest, Hungary |
| AuthorAffiliation_xml | – name: 2 HUN-REN-SU Human Microbiota Research Group, 1052 Budapest, Hungary; zsuzsanna.dunai@gmail.com – name: 3 Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, 1083 Budapest, Hungary – name: 4 Neurosurgical and Neurointervention Clinic, Semmelweis University, 1083 Budapest, Hungary – name: 1 Institute of Medical Microbiology, Semmelweis University, 1089 Budapest, Hungary; stercz.balazs@semmelweis.hu (B.S.); domokos.judit@semmelweis.hu (J.D.); makra.nora@semmelweis.hu (N.M.); juhaszjanos4@gmail.com (J.J.); ostorhazi.eszter@semmelweis.hu (E.O.); kocsis.bela@semmelweis.hu (B.K.) |
| Author_xml | – sequence: 1 givenname: Balazs orcidid: 0000-0002-9585-8397 surname: Stercz fullname: Stercz, Balazs organization: HUN-REN-SU Human Microbiota Research Group, 1052 Budapest, Hungary – sequence: 2 givenname: Judit orcidid: 0000-0002-0238-105X surname: Domokos fullname: Domokos, Judit organization: HUN-REN-SU Human Microbiota Research Group, 1052 Budapest, Hungary – sequence: 3 givenname: Zsuzsanna A surname: Dunai fullname: Dunai, Zsuzsanna A organization: HUN-REN-SU Human Microbiota Research Group, 1052 Budapest, Hungary – sequence: 4 givenname: Nora surname: Makra fullname: Makra, Nora organization: Institute of Medical Microbiology, Semmelweis University, 1089 Budapest, Hungary – sequence: 5 givenname: Janos surname: Juhasz fullname: Juhasz, Janos organization: Faculty of Information Technology and Bionics, Pázmány Péter Catholic University, 1083 Budapest, Hungary – sequence: 6 givenname: Eszter orcidid: 0000-0002-9459-7316 surname: Ostorhazi fullname: Ostorhazi, Eszter organization: Institute of Medical Microbiology, Semmelweis University, 1089 Budapest, Hungary – sequence: 7 givenname: Bela orcidid: 0000-0002-7067-7055 surname: Kocsis fullname: Kocsis, Bela organization: Institute of Medical Microbiology, Semmelweis University, 1089 Budapest, Hungary – sequence: 8 givenname: Dora orcidid: 0000-0002-8601-3923 surname: Szabo fullname: Szabo, Dora organization: Neurosurgical and Neurointervention Clinic, Semmelweis University, 1083 Budapest, Hungary |
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| Keywords | CTX-M OXA-carbapenemase multidrug resistance defensins mouse model colonization gut ESBL microbiome |
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