Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon
ABSTRACT The type IX secretion system (T9SS) transports cargo proteins through the outer membrane of Bacteroidetes and attaches them to the cell surface for functions including pathogenesis, gliding motility, and degradation of carbon sources. The T9SS comprises at least 20 different proteins and in...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01602-21 |
| _version_ | 1819279610324451328 |
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| author | Dhana G. Gorasia Ignacio Lunar Silva Catherine A. Butler Maïalène Chabalier Thierry Doan Eric Cascales Paul D. Veith Eric C. Reynolds |
| author_facet | Dhana G. Gorasia Ignacio Lunar Silva Catherine A. Butler Maïalène Chabalier Thierry Doan Eric Cascales Paul D. Veith Eric C. Reynolds |
| author_sort | Dhana G. Gorasia |
| collection | DOAJ |
| description | ABSTRACT The type IX secretion system (T9SS) transports cargo proteins through the outer membrane of Bacteroidetes and attaches them to the cell surface for functions including pathogenesis, gliding motility, and degradation of carbon sources. The T9SS comprises at least 20 different proteins and includes several modules: the trans-envelope core module comprising the PorL/M motor and the PorK/N ring, the outer membrane Sov translocon, and the cell attachment complex. However, the spatial organization of these modules is unknown. We have characterized the protein interactome of the Sov translocon in Porphyromonas gingivalis and identified Sov-PorV-PorA as well as Sov-PorW-PorN-PorK to be novel networks. PorW also interacted with PGN_1783 (PorD), which was required for maximum secretion efficiency. The identification of PorW as the missing link completes a continuous interaction network from the PorL/M motor to the Sov translocon, providing a pathway for cargo delivery and energy transduction from the inner membrane to the secretion pore. IMPORTANCE The T9SS is a newly identified protein secretion system of the Fibrobacteres-Chlorobi-Bacteroidetes superphylum used by pathogens associated with diseases of humans, fish, and poultry for the secretion and cell surface attachment of virulence factors. The T9SS comprises three known modules: (i) the trans-envelope core module comprising the PorL/M motor and the PorK/N ring, (ii) the outer membrane Sov translocon, and (iii) the cell surface attachment complex. The spatial organization and interaction of these modules have been a mystery. Here, we describe the protein interactome of the Sov translocon in the human pathogen Porphyromonas gingivalis and have identified PorW as the missing link which bridges PorN with Sov and so completes a continuous interaction network from the PorL/M motor to the Sov translocon, providing, for the first time, a pathway for cargo delivery and energy transduction from the inner membrane to the secretion pore. |
| first_indexed | 2024-12-24T00:30:38Z |
| format | Article |
| id | doaj.art-abed47ec460f4e9db9bc60e34b2f2206 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-24T00:30:38Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-abed47ec460f4e9db9bc60e34b2f22062022-12-21T17:24:16ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-02-0110110.1128/spectrum.01602-21Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov TransloconDhana G. Gorasia0Ignacio Lunar Silva1Catherine A. Butler2Maïalène Chabalier3Thierry Doan4Eric Cascales5Paul D. Veith6Eric C. Reynolds7Oral Health Cooperative Research Centre, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Parkville, Victoria, AustraliaLaboratoire d’Ingénierie des Systémes Macromoléculaires (LISM - UMR7255), Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), CNRS - Aix-Marseille Universite, Marseille, FranceOral Health Cooperative Research Centre, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Parkville, Victoria, AustraliaLaboratoire d’Ingénierie des Systémes Macromoléculaires (LISM - UMR7255), Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), CNRS - Aix-Marseille Universite, Marseille, FranceLaboratoire d’Ingénierie des Systémes Macromoléculaires (LISM - UMR7255), Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), CNRS - Aix-Marseille Universite, Marseille, FranceLaboratoire d’Ingénierie des Systémes Macromoléculaires (LISM - UMR7255), Institut de Microbiologie, Bioénergies et Biotechnologie (IM2B), CNRS - Aix-Marseille Universite, Marseille, FranceOral Health Cooperative Research Centre, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Parkville, Victoria, AustraliaOral Health Cooperative Research Centre, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Parkville, Victoria, AustraliaABSTRACT The type IX secretion system (T9SS) transports cargo proteins through the outer membrane of Bacteroidetes and attaches them to the cell surface for functions including pathogenesis, gliding motility, and degradation of carbon sources. The T9SS comprises at least 20 different proteins and includes several modules: the trans-envelope core module comprising the PorL/M motor and the PorK/N ring, the outer membrane Sov translocon, and the cell attachment complex. However, the spatial organization of these modules is unknown. We have characterized the protein interactome of the Sov translocon in Porphyromonas gingivalis and identified Sov-PorV-PorA as well as Sov-PorW-PorN-PorK to be novel networks. PorW also interacted with PGN_1783 (PorD), which was required for maximum secretion efficiency. The identification of PorW as the missing link completes a continuous interaction network from the PorL/M motor to the Sov translocon, providing a pathway for cargo delivery and energy transduction from the inner membrane to the secretion pore. IMPORTANCE The T9SS is a newly identified protein secretion system of the Fibrobacteres-Chlorobi-Bacteroidetes superphylum used by pathogens associated with diseases of humans, fish, and poultry for the secretion and cell surface attachment of virulence factors. The T9SS comprises three known modules: (i) the trans-envelope core module comprising the PorL/M motor and the PorK/N ring, (ii) the outer membrane Sov translocon, and (iii) the cell surface attachment complex. The spatial organization and interaction of these modules have been a mystery. Here, we describe the protein interactome of the Sov translocon in the human pathogen Porphyromonas gingivalis and have identified PorW as the missing link which bridges PorN with Sov and so completes a continuous interaction network from the PorL/M motor to the Sov translocon, providing, for the first time, a pathway for cargo delivery and energy transduction from the inner membrane to the secretion pore.https://journals.asm.org/doi/10.1128/spectrum.01602-21Porpyromonas gingivalisT9SSgingipainssecretion |
| spellingShingle | Dhana G. Gorasia Ignacio Lunar Silva Catherine A. Butler Maïalène Chabalier Thierry Doan Eric Cascales Paul D. Veith Eric C. Reynolds Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon Microbiology Spectrum Porpyromonas gingivalis T9SS gingipains secretion |
| title | Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon |
| title_full | Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon |
| title_fullStr | Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon |
| title_full_unstemmed | Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon |
| title_short | Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon |
| title_sort | protein interactome analysis of the type ix secretion system identifies porw as the missing link between the pork n ring complex and the sov translocon |
| topic | Porpyromonas gingivalis T9SS gingipains secretion |
| url | https://journals.asm.org/doi/10.1128/spectrum.01602-21 |
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