Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>
ABSTRACT Biofilms usually form when the density of bacteria increases during the middle to late periods of growth in culture, commonly induced by quorum-sensing systems. Biofilms attach to the surfaces of either living or nonliving objects and protect bacteria against antibiotics and a host’s immune...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-06-01
|
| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00336-20 |
| _version_ | 1818754580236730368 |
|---|---|
| author | Yan Liu Chao Pan Lijun Ye Yue Si Changhao Bi Xiaoting Hua Yunsong Yu Li Zhu Hengliang Wang |
| author_facet | Yan Liu Chao Pan Lijun Ye Yue Si Changhao Bi Xiaoting Hua Yunsong Yu Li Zhu Hengliang Wang |
| author_sort | Yan Liu |
| collection | DOAJ |
| description | ABSTRACT Biofilms usually form when the density of bacteria increases during the middle to late periods of growth in culture, commonly induced by quorum-sensing systems. Biofilms attach to the surfaces of either living or nonliving objects and protect bacteria against antibiotics and a host’s immune system. Here, a novel type of biofilm (the “R-biofilm”) is reported. These biofilms were formed by clinically isolated Klebsiella pneumoniae strains following double-stranded-DNA breaks (DSBs), while undamaged bacteria did not form classic biofilms even in the later stages of growth. R-biofilms had a fixed ring-like or discoid shape with good ductility and could protect many living bacterial cells within. We show that extracellular proteins and DNAs released, probably by dead bacteria, were the core structural materials of R-biofilms. We anticipate that novel signaling pathways besides the bacterial SOS response are involved in R-biofilm formation. The observations in this study suggest a limitation to the use of the currently popular Cas9-mediated bactericidal tools to eliminate certain bacteria because the resulting DSBs may lead to the formation of these protective R-biofilms. IMPORTANCE Many pathogenic bacteria can form biofilm matrices that consist of complex molecules such as polysaccharides, proteins, and DNA. These biofilms help the bacteria to infect and colonize a host. Such biofilms may attach and develop on the surfaces of indwelling medical devices or other supportive environments. This study found that following double-strand breaks in their DNA, Klebsiella pneumoniae cells can form a novel type of biofilm with ring-like or discoid morphology. This biofilm structure, named the “R-biofilm,” helps protect the bacteria against adverse conditions such as exposure to ethanol, hydrogen peroxide, and UV radiation. |
| first_indexed | 2024-12-18T05:25:31Z |
| format | Article |
| id | doaj.art-df34a7b95dc948f184016311122ef599 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-18T05:25:31Z |
| publishDate | 2020-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-df34a7b95dc948f184016311122ef5992022-12-21T21:19:34ZengAmerican Society for MicrobiologymSphere2379-50422020-06-015310.1128/mSphere.00336-20Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>Yan Liu0Chao Pan1Lijun Ye2Yue Si3Changhao Bi4Xiaoting Hua5Yunsong Yu6Li Zhu7Hengliang Wang8State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Biotechnology, Beijing, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Biotechnology, Beijing, ChinaTianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Biotechnology, Beijing, ChinaTianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, College of Medicine, Zhejiang University, Hangzhou, ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, College of Medicine, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Biotechnology, Beijing, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Biotechnology, Beijing, ChinaABSTRACT Biofilms usually form when the density of bacteria increases during the middle to late periods of growth in culture, commonly induced by quorum-sensing systems. Biofilms attach to the surfaces of either living or nonliving objects and protect bacteria against antibiotics and a host’s immune system. Here, a novel type of biofilm (the “R-biofilm”) is reported. These biofilms were formed by clinically isolated Klebsiella pneumoniae strains following double-stranded-DNA breaks (DSBs), while undamaged bacteria did not form classic biofilms even in the later stages of growth. R-biofilms had a fixed ring-like or discoid shape with good ductility and could protect many living bacterial cells within. We show that extracellular proteins and DNAs released, probably by dead bacteria, were the core structural materials of R-biofilms. We anticipate that novel signaling pathways besides the bacterial SOS response are involved in R-biofilm formation. The observations in this study suggest a limitation to the use of the currently popular Cas9-mediated bactericidal tools to eliminate certain bacteria because the resulting DSBs may lead to the formation of these protective R-biofilms. IMPORTANCE Many pathogenic bacteria can form biofilm matrices that consist of complex molecules such as polysaccharides, proteins, and DNA. These biofilms help the bacteria to infect and colonize a host. Such biofilms may attach and develop on the surfaces of indwelling medical devices or other supportive environments. This study found that following double-strand breaks in their DNA, Klebsiella pneumoniae cells can form a novel type of biofilm with ring-like or discoid morphology. This biofilm structure, named the “R-biofilm,” helps protect the bacteria against adverse conditions such as exposure to ethanol, hydrogen peroxide, and UV radiation.https://journals.asm.org/doi/10.1128/mSphere.00336-20Klebsiella pneumoniaebiofilmCas9double-strand break |
| spellingShingle | Yan Liu Chao Pan Lijun Ye Yue Si Changhao Bi Xiaoting Hua Yunsong Yu Li Zhu Hengliang Wang Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> mSphere Klebsiella pneumoniae biofilm Cas9 double-strand break |
| title | Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> |
| title_full | Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> |
| title_fullStr | Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> |
| title_full_unstemmed | Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> |
| title_short | Nonclassical Biofilms Induced by DNA Breaks in <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> |
| title_sort | nonclassical biofilms induced by dna breaks in named content content type genus species klebsiella pneumoniae named content |
| topic | Klebsiella pneumoniae biofilm Cas9 double-strand break |
| url | https://journals.asm.org/doi/10.1128/mSphere.00336-20 |
| work_keys_str_mv | AT yanliu nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT chaopan nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT lijunye nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT yuesi nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT changhaobi nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT xiaotinghua nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT yunsongyu nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT lizhu nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent AT hengliangwang nonclassicalbiofilmsinducedbydnabreaksinnamedcontentcontenttypegenusspeciesklebsiellapneumoniaenamedcontent |