Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i>
Carboxy-terminal processing protease (Ctp) is a serine protease that controls multiple cellular processes through posttranslational modification of proteins. <i>Acinetobacter baumannii</i> ATCC 17978 <i>ctp</i> mutant, namely MR14, is known to cause cell wall defects and auto...
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MDPI AG
2021-06-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/9/6/1336 |
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| author | Rakesh Roy Ren-In You Chan-Hua Chang Chiou-Ying Yang Nien-Tsung Lin |
| author_facet | Rakesh Roy Ren-In You Chan-Hua Chang Chiou-Ying Yang Nien-Tsung Lin |
| author_sort | Rakesh Roy |
| collection | DOAJ |
| description | Carboxy-terminal processing protease (Ctp) is a serine protease that controls multiple cellular processes through posttranslational modification of proteins. <i>Acinetobacter baumannii</i> ATCC 17978 <i>ctp</i> mutant, namely MR14, is known to cause cell wall defects and autolysis. The objective of this study was to investigate the role of <i>ctp</i> mutation–driven autolysis in regulating biofilms in <i>A. baumannii</i> and to evaluate the vesiculation caused by cell wall defects. We found that in <i>A. baumannii</i>, Ctp is localized in the cytoplasmic membrane, and loss of Ctp function enhances the biofilm-forming ability of <i>A. baumannii</i>. Quantification of the matrix components revealed that extracellular DNA (eDNA) and proteins were the chief constituents of MR14 biofilm, and the transmission electron microscopy further indicated the presence of numerous dead cells compared with ATCC 17978. The large number of MR14 dead cells is potentially the result of compromised outer membrane integrity, as demonstrated by its high sensitivity to sodium dodecyl sulfate (SDS) and ethylenediaminetetraacetic acid (EDTA). MR14 also exhibited the hypervesiculation phenotype, producing outer-membrane vesicles (OMVs) of large mean size. The MR14 OMVs were more cytotoxic toward A549 cells than ATCC 17978 OMVs. Our overall results indicate that <i>A. baumannii</i><i>ctp</i> negatively controls pathogenic traits through autolysis and OMV biogenesis. |
| first_indexed | 2024-03-10T10:15:04Z |
| format | Article |
| id | doaj.art-d6ae913d21ed4bbfb11d8807fe3e0804 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T10:15:04Z |
| publishDate | 2021-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-d6ae913d21ed4bbfb11d8807fe3e08042023-11-22T00:55:50ZengMDPI AGMicroorganisms2076-26072021-06-0196133610.3390/microorganisms9061336Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i>Rakesh Roy0Ren-In You1Chan-Hua Chang2Chiou-Ying Yang3Nien-Tsung Lin4Institute of Medical Sciences, Tzu Chi University, No. 701, Sec. 3, Zhongyang Rd., Hualien 97004, TaiwanDepartment of Laboratory Medicine and Biotechnology, Tzu Chi University, No. 701, Sec. 3, Zhongyang Rd., Hualien 97004, TaiwanInstitute of Molecular Biology, National Chung Hsing University, Taichung 40227, TaiwanInstitute of Molecular Biology, National Chung Hsing University, Taichung 40227, TaiwanInstitute of Medical Sciences, Tzu Chi University, No. 701, Sec. 3, Zhongyang Rd., Hualien 97004, TaiwanCarboxy-terminal processing protease (Ctp) is a serine protease that controls multiple cellular processes through posttranslational modification of proteins. <i>Acinetobacter baumannii</i> ATCC 17978 <i>ctp</i> mutant, namely MR14, is known to cause cell wall defects and autolysis. The objective of this study was to investigate the role of <i>ctp</i> mutation–driven autolysis in regulating biofilms in <i>A. baumannii</i> and to evaluate the vesiculation caused by cell wall defects. We found that in <i>A. baumannii</i>, Ctp is localized in the cytoplasmic membrane, and loss of Ctp function enhances the biofilm-forming ability of <i>A. baumannii</i>. Quantification of the matrix components revealed that extracellular DNA (eDNA) and proteins were the chief constituents of MR14 biofilm, and the transmission electron microscopy further indicated the presence of numerous dead cells compared with ATCC 17978. The large number of MR14 dead cells is potentially the result of compromised outer membrane integrity, as demonstrated by its high sensitivity to sodium dodecyl sulfate (SDS) and ethylenediaminetetraacetic acid (EDTA). MR14 also exhibited the hypervesiculation phenotype, producing outer-membrane vesicles (OMVs) of large mean size. The MR14 OMVs were more cytotoxic toward A549 cells than ATCC 17978 OMVs. Our overall results indicate that <i>A. baumannii</i><i>ctp</i> negatively controls pathogenic traits through autolysis and OMV biogenesis.https://www.mdpi.com/2076-2607/9/6/1336<i>Acinetobacter baumannii</i>carboxy-terminal processing protease (Ctp)outer-membrane vesicles (OMVs)extracellular DNA (eDNA)capsular polysaccharides (CPSs) |
| spellingShingle | Rakesh Roy Ren-In You Chan-Hua Chang Chiou-Ying Yang Nien-Tsung Lin Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> Microorganisms <i>Acinetobacter baumannii</i> carboxy-terminal processing protease (Ctp) outer-membrane vesicles (OMVs) extracellular DNA (eDNA) capsular polysaccharides (CPSs) |
| title | Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> |
| title_full | Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> |
| title_fullStr | Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> |
| title_full_unstemmed | Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> |
| title_short | Carboxy-Terminal Processing Protease Controls Production of Outer Membrane Vesicles and Biofilm in <i>Acinetobacter baumannii</i> |
| title_sort | carboxy terminal processing protease controls production of outer membrane vesicles and biofilm in i acinetobacter baumannii i |
| topic | <i>Acinetobacter baumannii</i> carboxy-terminal processing protease (Ctp) outer-membrane vesicles (OMVs) extracellular DNA (eDNA) capsular polysaccharides (CPSs) |
| url | https://www.mdpi.com/2076-2607/9/6/1336 |
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