An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins

Jeffrey W. Hall, Bruno P. Lima, Gaetan G. Herbomel, Tata Gopinath, Le Anna McDonald, Michael T. Shyne, John K. Lee, Jens Kreth, Karen F. Ross, Gianluigi Veglia, Mark C. Herzberg

Research output: Contribution to journalArticle

Abstract

Bacterial adhesins mediate adhesion to substrates and biofilm formation. Adhesins of the LPXTG family are posttranslationally processed by the cell membrane-localized peptidase sortase A, which cleaves the LPXTG motif. This generates a short C-terminal peptide (C-pep) that remains in the cell membrane, whereas the mature adhesin is incorporated into the cell wall. Genes encoding adhesins of the oral bacterium Streptococcus gordonii were differentially expressed depending on whether the bacteria were isolated from saliva or dental plaque and appeared to be coordinately regulated. Deletion of sspA and sspB (sspAB), both of which encode LPXTG-containing adhesins, unexpectedly enhanced adhesion and biofilm formation. C-peps produced from a model LPXTG-containing adhesin localized to the cell membrane and bound to and inhibited the intramembrane sensor histidine kinase SGO_1180, thus preventing activation of the cognate response regulator SGO_1181. The absence of SspAB C-peps induced the expression of the scaCBA operon encoding the lipoprotein adhesin ScaA, which was sufficient to preserve and even enhance biofilm formation. This C-pep-driven regulatory circuit also exists in pathogenic streptococci and is likely conserved among Gram-positive bacteria. This quality control mechanism ensures that the bacteria can form biofilms under diverse environmental conditions and may play a role in optimizing adhesion and biofilm formation.

Original languageEnglish (US)
JournalScience signaling
Volume12
Issue number580
DOIs
StatePublished - May 7 2019

Fingerprint

Biofilms
Bacteria
Cell membranes
Networks (circuits)
Processing
Adhesion
Cell Membrane
Streptococcus gordonii
Bacterial Adhesins
Dental Plaque
Peptides
Gene encoding
Gram-Positive Bacteria
Operon
Streptococcus
Saliva
Histidine
Quality Control
Cell Wall
Lipoproteins

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Hall, J. W., Lima, B. P., Herbomel, G. G., Gopinath, T., McDonald, L. A., Shyne, M. T., ... Herzberg, M. C. (2019). An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins. Science signaling, 12(580). https://doi.org/10.1126/scisignal.aas9941

An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins. / Hall, Jeffrey W.; Lima, Bruno P.; Herbomel, Gaetan G.; Gopinath, Tata; McDonald, Le Anna; Shyne, Michael T.; Lee, John K.; Kreth, Jens; Ross, Karen F.; Veglia, Gianluigi; Herzberg, Mark C.

In: Science signaling, Vol. 12, No. 580, 07.05.2019.

Research output: Contribution to journalArticle

Hall, JW, Lima, BP, Herbomel, GG, Gopinath, T, McDonald, LA, Shyne, MT, Lee, JK, Kreth, J, Ross, KF, Veglia, G & Herzberg, MC 2019, 'An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins', Science signaling, vol. 12, no. 580. https://doi.org/10.1126/scisignal.aas9941
Hall, Jeffrey W. ; Lima, Bruno P. ; Herbomel, Gaetan G. ; Gopinath, Tata ; McDonald, Le Anna ; Shyne, Michael T. ; Lee, John K. ; Kreth, Jens ; Ross, Karen F. ; Veglia, Gianluigi ; Herzberg, Mark C. / An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins. In: Science signaling. 2019 ; Vol. 12, No. 580.
@article{d3601fc6a5be4d7dae9d527e38ca4554,
title = "An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins",
abstract = "Bacterial adhesins mediate adhesion to substrates and biofilm formation. Adhesins of the LPXTG family are posttranslationally processed by the cell membrane-localized peptidase sortase A, which cleaves the LPXTG motif. This generates a short C-terminal peptide (C-pep) that remains in the cell membrane, whereas the mature adhesin is incorporated into the cell wall. Genes encoding adhesins of the oral bacterium Streptococcus gordonii were differentially expressed depending on whether the bacteria were isolated from saliva or dental plaque and appeared to be coordinately regulated. Deletion of sspA and sspB (sspAB), both of which encode LPXTG-containing adhesins, unexpectedly enhanced adhesion and biofilm formation. C-peps produced from a model LPXTG-containing adhesin localized to the cell membrane and bound to and inhibited the intramembrane sensor histidine kinase SGO_1180, thus preventing activation of the cognate response regulator SGO_1181. The absence of SspAB C-peps induced the expression of the scaCBA operon encoding the lipoprotein adhesin ScaA, which was sufficient to preserve and even enhance biofilm formation. This C-pep-driven regulatory circuit also exists in pathogenic streptococci and is likely conserved among Gram-positive bacteria. This quality control mechanism ensures that the bacteria can form biofilms under diverse environmental conditions and may play a role in optimizing adhesion and biofilm formation.",
author = "Hall, {Jeffrey W.} and Lima, {Bruno P.} and Herbomel, {Gaetan G.} and Tata Gopinath and McDonald, {Le Anna} and Shyne, {Michael T.} and Lee, {John K.} and Jens Kreth and Ross, {Karen F.} and Gianluigi Veglia and Herzberg, {Mark C.}",
year = "2019",
month = "5",
day = "7",
doi = "10.1126/scisignal.aas9941",
language = "English (US)",
volume = "12",
journal = "Science Signaling",
issn = "1937-9145",
publisher = "American Association for the Advancement of Science",
number = "580",

}

TY - JOUR

T1 - An intramembrane sensory circuit monitors sortase A-mediated processing of streptococcal adhesins

AU - Hall, Jeffrey W.

AU - Lima, Bruno P.

AU - Herbomel, Gaetan G.

AU - Gopinath, Tata

AU - McDonald, Le Anna

AU - Shyne, Michael T.

AU - Lee, John K.

AU - Kreth, Jens

AU - Ross, Karen F.

AU - Veglia, Gianluigi

AU - Herzberg, Mark C.

PY - 2019/5/7

Y1 - 2019/5/7

N2 - Bacterial adhesins mediate adhesion to substrates and biofilm formation. Adhesins of the LPXTG family are posttranslationally processed by the cell membrane-localized peptidase sortase A, which cleaves the LPXTG motif. This generates a short C-terminal peptide (C-pep) that remains in the cell membrane, whereas the mature adhesin is incorporated into the cell wall. Genes encoding adhesins of the oral bacterium Streptococcus gordonii were differentially expressed depending on whether the bacteria were isolated from saliva or dental plaque and appeared to be coordinately regulated. Deletion of sspA and sspB (sspAB), both of which encode LPXTG-containing adhesins, unexpectedly enhanced adhesion and biofilm formation. C-peps produced from a model LPXTG-containing adhesin localized to the cell membrane and bound to and inhibited the intramembrane sensor histidine kinase SGO_1180, thus preventing activation of the cognate response regulator SGO_1181. The absence of SspAB C-peps induced the expression of the scaCBA operon encoding the lipoprotein adhesin ScaA, which was sufficient to preserve and even enhance biofilm formation. This C-pep-driven regulatory circuit also exists in pathogenic streptococci and is likely conserved among Gram-positive bacteria. This quality control mechanism ensures that the bacteria can form biofilms under diverse environmental conditions and may play a role in optimizing adhesion and biofilm formation.

AB - Bacterial adhesins mediate adhesion to substrates and biofilm formation. Adhesins of the LPXTG family are posttranslationally processed by the cell membrane-localized peptidase sortase A, which cleaves the LPXTG motif. This generates a short C-terminal peptide (C-pep) that remains in the cell membrane, whereas the mature adhesin is incorporated into the cell wall. Genes encoding adhesins of the oral bacterium Streptococcus gordonii were differentially expressed depending on whether the bacteria were isolated from saliva or dental plaque and appeared to be coordinately regulated. Deletion of sspA and sspB (sspAB), both of which encode LPXTG-containing adhesins, unexpectedly enhanced adhesion and biofilm formation. C-peps produced from a model LPXTG-containing adhesin localized to the cell membrane and bound to and inhibited the intramembrane sensor histidine kinase SGO_1180, thus preventing activation of the cognate response regulator SGO_1181. The absence of SspAB C-peps induced the expression of the scaCBA operon encoding the lipoprotein adhesin ScaA, which was sufficient to preserve and even enhance biofilm formation. This C-pep-driven regulatory circuit also exists in pathogenic streptococci and is likely conserved among Gram-positive bacteria. This quality control mechanism ensures that the bacteria can form biofilms under diverse environmental conditions and may play a role in optimizing adhesion and biofilm formation.

UR - http://www.scopus.com/inward/record.url?scp=85065780047&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85065780047&partnerID=8YFLogxK

U2 - 10.1126/scisignal.aas9941

DO - 10.1126/scisignal.aas9941

M3 - Article

VL - 12

JO - Science Signaling

JF - Science Signaling

SN - 1937-9145

IS - 580

ER -