The Type IX Secretion System and Its Role in Bacterial Function and Pathogenesis

, and species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors. These virulence factors are then released on outer membrane vesicles (OMVs), which penetrate the host to dysregulate the immune response to est...

Full description

Saved in:
Bibliographic Details
Published in:Journal of dental research Vol. 101; no. 4; p. 374
Main Authors: Veith, P D, Glew, M D, Gorasia, D G, Cascales, E, Reynolds, E C
Format: Journal Article
Language:English
Published: United States 01.04.2022
Subjects:
ISSN:1544-0591, 1544-0591
Online Access:Get more information
Tags: Add Tag
No Tags, Be the first to tag this record!
Abstract , and species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors. These virulence factors are then released on outer membrane vesicles (OMVs), which penetrate the host to dysregulate the immune response to establish a positive feedback loop of chronic, inflammatory destruction of the tooth's supporting tissues. In this review, we present the latest information on the molecular architecture of the T9SS and provide mechanistic insight into its role in secretion and attachment of cargo proteins to produce a virulence coat on cells and OMVs. The recent molecular structures of the T9SS motor comprising PorL and PorM as well as the secretion pore Sov, together with advances in the overall interactome, have provided insight into the possible mechanisms of secretion. We propose the presence of PorL/M motors arranged in a circle at the inner membrane with bent periplasmic rotors interacting with the PorN protein. At the outer membrane, we envisage a slide carousel model where the PorN protein is driven around a circular track composed of PorK. Cargo proteins are transported by PorN to PorW and the Sov translocon just as slides are rotated to the projection window. Secreted proteins are proposed to then be shuttled along highways consisting of the PorV shuttle protein to an array of attachment complexes distributed around the cell. The cell surface attachment of cargo is a hallmark of the T9SS, and in and , this attachment is achieved via covalent bonding to a linking sugar synthesized by the Wbp/Vim pathway. The cell-surface attached cargo are enriched on OMVs, which are then released from the cell.
AbstractList , and species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors. These virulence factors are then released on outer membrane vesicles (OMVs), which penetrate the host to dysregulate the immune response to establish a positive feedback loop of chronic, inflammatory destruction of the tooth's supporting tissues. In this review, we present the latest information on the molecular architecture of the T9SS and provide mechanistic insight into its role in secretion and attachment of cargo proteins to produce a virulence coat on cells and OMVs. The recent molecular structures of the T9SS motor comprising PorL and PorM as well as the secretion pore Sov, together with advances in the overall interactome, have provided insight into the possible mechanisms of secretion. We propose the presence of PorL/M motors arranged in a circle at the inner membrane with bent periplasmic rotors interacting with the PorN protein. At the outer membrane, we envisage a slide carousel model where the PorN protein is driven around a circular track composed of PorK. Cargo proteins are transported by PorN to PorW and the Sov translocon just as slides are rotated to the projection window. Secreted proteins are proposed to then be shuttled along highways consisting of the PorV shuttle protein to an array of attachment complexes distributed around the cell. The cell surface attachment of cargo is a hallmark of the T9SS, and in and , this attachment is achieved via covalent bonding to a linking sugar synthesized by the Wbp/Vim pathway. The cell-surface attached cargo are enriched on OMVs, which are then released from the cell.
Porphyromonas, Tannerella, and Prevotella species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors. These virulence factors are then released on outer membrane vesicles (OMVs), which penetrate the host to dysregulate the immune response to establish a positive feedback loop of chronic, inflammatory destruction of the tooth's supporting tissues. In this review, we present the latest information on the molecular architecture of the T9SS and provide mechanistic insight into its role in secretion and attachment of cargo proteins to produce a virulence coat on cells and OMVs. The recent molecular structures of the T9SS motor comprising PorL and PorM as well as the secretion pore Sov, together with advances in the overall interactome, have provided insight into the possible mechanisms of secretion. We propose the presence of PorL/M motors arranged in a circle at the inner membrane with bent periplasmic rotors interacting with the PorN protein. At the outer membrane, we envisage a slide carousel model where the PorN protein is driven around a circular track composed of PorK. Cargo proteins are transported by PorN to PorW and the Sov translocon just as slides are rotated to the projection window. Secreted proteins are proposed to then be shuttled along highways consisting of the PorV shuttle protein to an array of attachment complexes distributed around the cell. The cell surface attachment of cargo is a hallmark of the T9SS, and in Porphyromonas gingivalis and Tannerella forsythia, this attachment is achieved via covalent bonding to a linking sugar synthesized by the Wbp/Vim pathway. The cell-surface attached cargo are enriched on OMVs, which are then released from the cell.Porphyromonas, Tannerella, and Prevotella species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors. These virulence factors are then released on outer membrane vesicles (OMVs), which penetrate the host to dysregulate the immune response to establish a positive feedback loop of chronic, inflammatory destruction of the tooth's supporting tissues. In this review, we present the latest information on the molecular architecture of the T9SS and provide mechanistic insight into its role in secretion and attachment of cargo proteins to produce a virulence coat on cells and OMVs. The recent molecular structures of the T9SS motor comprising PorL and PorM as well as the secretion pore Sov, together with advances in the overall interactome, have provided insight into the possible mechanisms of secretion. We propose the presence of PorL/M motors arranged in a circle at the inner membrane with bent periplasmic rotors interacting with the PorN protein. At the outer membrane, we envisage a slide carousel model where the PorN protein is driven around a circular track composed of PorK. Cargo proteins are transported by PorN to PorW and the Sov translocon just as slides are rotated to the projection window. Secreted proteins are proposed to then be shuttled along highways consisting of the PorV shuttle protein to an array of attachment complexes distributed around the cell. The cell surface attachment of cargo is a hallmark of the T9SS, and in Porphyromonas gingivalis and Tannerella forsythia, this attachment is achieved via covalent bonding to a linking sugar synthesized by the Wbp/Vim pathway. The cell-surface attached cargo are enriched on OMVs, which are then released from the cell.
Author Reynolds, E C
Gorasia, D G
Glew, M D
Cascales, E
Veith, P D
Author_xml – sequence: 1
  givenname: P D
  surname: Veith
  fullname: Veith, P D
  organization: Oral Health CRC, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Victoria, Australia
– sequence: 2
  givenname: M D
  surname: Glew
  fullname: Glew, M D
  organization: Oral Health CRC, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Victoria, Australia
– sequence: 3
  givenname: D G
  surname: Gorasia
  fullname: Gorasia, D G
  organization: Oral Health CRC, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Victoria, Australia
– sequence: 4
  givenname: E
  surname: Cascales
  fullname: Cascales, E
  organization: Laboratoire d'Ingénierie des Syst èmes Macromol éculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique (CNRS), UMR7255, Marseille Cedex, France
– sequence: 5
  givenname: E C
  surname: Reynolds
  fullname: Reynolds, E C
  organization: Oral Health CRC, Melbourne Dental School, Bio21 Institute, The University of Melbourne, Victoria, Australia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34889148$$D View this record in MEDLINE/PubMed
BookMark eNpNkD1PwzAYhC1URD_gB7AgjywBv47t2CNUFCpVoqJFYotc5w0NSpwSJ0P-PQGKxHQ3PDrd3ZSMfO2RkEtgNwBJcssY5ywWkgMwCdKYEzIBKUTEpIHRPz8m0xA-GAPDdXxGxrHQ2oDQE7Le7pFu-wPS5RvdoGuwLWpPN31osaLWZ3TZBvpSl0gLT--ta7EpbEkXnXc_5Deytu2-fkePoQjn5DS3ZcCLo87I6-JhO3-KVs-Py_ndKnISoI0sg1jnKomH2s6aXMRKZIk1InOSgWVqp412icwVRy2swsRmyvKdGrZqxzM-I9e_uYem_uwwtGlVBIdlaT3WXUi5YlqKYTEM6NUR7XYVZumhKSrb9OnfC_wLF5Be_g
CitedBy_id crossref_primary_10_1111_omi_12380
crossref_primary_10_1080_1040841X_2022_2163613
crossref_primary_10_1002_mbo3_1401
crossref_primary_10_1099_mic_0_001320
crossref_primary_10_1128_iai_00207_24
crossref_primary_10_1098_rsob_240335
crossref_primary_10_1073_pnas_2119907119
crossref_primary_10_1094_PHYTO_12_24_0417_R
crossref_primary_10_1016_j_gene_2024_149182
crossref_primary_10_1038_s42003_023_04472_3
crossref_primary_10_1111_omi_12426
crossref_primary_10_3389_fmicb_2022_1006609
crossref_primary_10_1038_s41429_024_00790_8
crossref_primary_10_1128_mbio_01799_25
crossref_primary_10_3390_ijms23105681
crossref_primary_10_1128_jb_00068_24
crossref_primary_10_3390_ijms25010281
crossref_primary_10_1111_mmi_15363
crossref_primary_10_1038_s41598_024_57089_9
crossref_primary_10_1038_s41598_024_72451_7
crossref_primary_10_1016_j_crmicr_2025_100404
crossref_primary_10_1038_s41564_024_01644_7
crossref_primary_10_3389_fcimb_2025_1569544
crossref_primary_10_1038_s41467_025_63163_1
crossref_primary_10_3389_fmicb_2025_1555868
crossref_primary_10_1002_adfm_202314024
ContentType Journal Article
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1177/00220345211051599
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE
MEDLINE - Academic
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Dentistry
EISSN 1544-0591
ExternalDocumentID 34889148
Genre Research Support, Non-U.S. Gov't
Journal Article
Review
GroupedDBID ---
-TM
.2E
.2J
.2N
.55
01A
0R~
18M
1~K
29K
2WC
31R
31U
31X
31Z
34H
3V.
4.4
53G
54M
5GY
5RE
5VS
7RQ
7RV
7X7
88E
8AO
8FE
8FH
8FI
8FJ
8FW
8R4
8R5
AABMB
AABOD
AACMV
AACTG
AADUE
AAEWN
AAGGD
AAGMC
AAITX
AAJPV
AAKGS
AANSI
AAOVH
AAPEO
AAQXH
AAQXI
AARDL
AARDX
AARIX
AATAA
AATBZ
AAUAS
AAWTL
AAXOT
AAZBJ
ABAWP
ABCCA
ABCJG
ABDWY
ABEIX
ABFWQ
ABHKI
ABKRH
ABLUO
ABPGX
ABPNF
ABQKF
ABQXT
ABRHV
ABUJY
ABUWG
ABVFX
ABYTW
ACARO
ACDSZ
ACDXX
ACFEJ
ACFMA
ACGBL
ACGFO
ACGFS
ACGZU
ACJER
ACJTF
ACLFY
ACLHI
ACLZU
ACOFE
ACOXC
ACPRK
ACROE
ACSBE
ACSIQ
ACSVP
ACTQU
ACUAV
ACUIR
ACXKE
ACXMB
ADBBV
ADEIA
ADMPF
ADNON
ADRRZ
ADTBJ
ADUKL
ADVBO
ADZZY
AECGH
AEDTQ
AEILP
AEKYL
AENEX
AEPTA
AEQLS
AERKM
AESZF
AEUHG
AEUIJ
AEWDL
AEWHI
AEXFG
AEXNY
AFEET
AFFNX
AFGYO
AFKRA
AFKRG
AFMOU
AFOSN
AFQAA
AFUIA
AGHKR
AGKLV
AGNHF
AGPXR
AGWFA
AHDMH
AHJOV
AHMBA
AI.
AIGRN
AIOMO
AJEFB
AJMMQ
AJUZI
AJXAJ
ALIPV
ALKWR
ALMA_UNASSIGNED_HOLDINGS
ALTZF
AMCVQ
ANDLU
ARTOV
AUTPY
AUVAJ
AYAKG
B3H
B8M
B8R
B8Z
B94
BBNVY
BBRGL
BDDNI
BENPR
BHPHI
BKEYQ
BKIIM
BKSCU
BPACV
BPHCQ
BSEHC
BVXVI
BWJAD
BYIEH
CAG
CBRKF
CCPQU
CDWPY
CFDXU
CGR
COF
CORYS
CQQTX
CUTAK
CUY
CVF
D-I
DB0
DC-
DF0
DO-
DOPDO
DU5
DV7
DWQXO
E3Z
EBD
EBS
ECM
EIF
EJD
EX3
F5P
FHBDP
FYUFA
GROUPED_SAGE_PREMIER_JOURNAL_COLLECTION
GX1
H13
HCIFZ
HF~
HMCUK
HZ~
J8X
K.F
LK8
M1P
M4V
M7P
N9A
NAPCQ
NPM
O9-
OHT
P.9
P.B
P2P
PKN
PQQKQ
PROAC
PSQYO
Q1R
Q2X
Q7L
Q7U
Q83
ROL
S01
S0X
SAUOL
SCNPE
SFC
SGO
SGR
SGV
SGZ
SHG
SPQ
SPV
TDR
UKHRP
VH1
W8F
WOQ
WOW
X7M
ZE2
ZGI
ZONMY
ZPPRI
ZRKOI
ZSSAH
7X8
AAPII
ABIDT
ABJZC
ADDLC
ADEBD
AJGYC
AJHME
AJVBE
SASJQ
ID FETCH-LOGICAL-c511t-a0138f673159ca9f4364d7a94dc501a06b898c75f62e84a6e7ad6a2b62118c2d2
IEDL.DBID 7X8
ISICitedReferencesCount 35
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000730163300001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1544-0591
IngestDate Sun Sep 28 12:03:30 EDT 2025
Wed Feb 19 02:27:32 EST 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 4
Keywords microbiology
bacterial virulence
host pathogen interactions
periodontal disease(s)/periodontitis
outer membrane vesicles
ultrastructure
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c511t-a0138f673159ca9f4364d7a94dc501a06b898c75f62e84a6e7ad6a2b62118c2d2
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
ObjectType-Review-3
content type line 23
OpenAccessLink https://amu.hal.science/hal-03654995
PMID 34889148
PQID 2608540191
PQPubID 23479
ParticipantIDs proquest_miscellaneous_2608540191
pubmed_primary_34889148
PublicationCentury 2000
PublicationDate 2022-04-01
PublicationDateYYYYMMDD 2022-04-01
PublicationDate_xml – month: 04
  year: 2022
  text: 2022-04-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Journal of dental research
PublicationTitleAlternate J Dent Res
PublicationYear 2022
SSID ssj0019283
Score 2.5232737
SecondaryResourceType review_article
Snippet , and species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface with an array of virulence factors....
Porphyromonas, Tannerella, and Prevotella species found in severe periodontitis use the Type IX Secretion System (T9SS) to load their outer membrane surface...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 374
SubjectTerms Bacterial Proteins - metabolism
Bacterial Secretion Systems - metabolism
Porphyromonas gingivalis
Tannerella forsythia
Virulence Factors
Title The Type IX Secretion System and Its Role in Bacterial Function and Pathogenesis
URI https://www.ncbi.nlm.nih.gov/pubmed/34889148
https://www.proquest.com/docview/2608540191
Volume 101
WOSCitedRecordID wos000730163300001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1LS8QwEA7qCnrx_VhfRPAa7LZpkp7E1-IeXIoP6K2kaSIL0q529fc7k3bZmwheekpDO5nMfJOZfEPIBaypEZHTzMU2ZDxRlqkk0MyYQMpSlNwZ5ZtNyPFYZVmSdgduTVdWObeJ3lCXtcEz8kvA3QrQBYQXV9MPhl2jMLvatdBYJr0IoAxqtcwWWYQk9DScSDjDAEYMuqymJ1zCG6YRjzH-QZf-C8L0nma4-d9v3CIbHcak161SbJMlW-2QtTusC8LWbrskBeWgGIHSUUafETji8tCWvZzqqqSjWUOf6ndLJxW9aQmdYcYhOEE_EoekgB3rNzSVk2aPvA7vX24fWNdagRlAWDOmMUHphIzg141OHI8EL6VOeGniYKADUahEGRk7EVrFtbBSl0KHhQB5KROW4T5ZqerKHhIK-1bHauAAaBQcwIZ2VlhQAFFYoYoB75PzubByUF3MR-jK1l9NvhBXnxy0Es-nLcdGHoFhSSBUO_rD28dkPcRLCb6e5oT0HGxce0pWzTeI9fPM6wQ8x-njD5PHvto
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+Type+IX+Secretion+System+and+Its+Role+in+Bacterial+Function+and+Pathogenesis&rft.jtitle=Journal+of+dental+research&rft.au=Veith%2C+P+D&rft.au=Glew%2C+M+D&rft.au=Gorasia%2C+D+G&rft.au=Cascales%2C+E&rft.date=2022-04-01&rft.issn=1544-0591&rft.eissn=1544-0591&rft.volume=101&rft.issue=4&rft.spage=374&rft_id=info:doi/10.1177%2F00220345211051599&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1544-0591&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1544-0591&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1544-0591&client=summon