DOI: 10.1111/j.1462-2920.2009.02005.x. Type VI secretion modulates quorum sensing and stress response in <i>Vibrio anguillarum</i>

Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum

10.1111/j.1462-2920.2009.02005.x

Crossref journal-article

Wiley

Environmental Microbiology (311)

Abstract

SummaryType VI protein secretion systems (T6SS) are essential for virulence of several Gram‐negative bacteria. In this study, we identified a T6SS in Vibrio anguillarum, a marine bacterium that causes a hemorrhagic septicemia in fish. A partial operon vtsA‐H (vibrio type six secretion) was sequenced and shown to encode eight proteins. VtsE‐H are signature proteins found in other T6SSs, while VtsA‐D are not associated with T6SS studied so far. In‐frame deletions were made in each gene. Secretion of a haemolysin‐co‐regulated‐like protein (Hcp), a protein secreted by all studied T6SSs, was decreased in VtsE‐H. Unexpectedly, VtsA, VtsC and VtsD activated while VtsB and VtsE‐H repressed hcp expression. The T6SS proteins also regulated expression of two extracellular proteases, EmpA and PrtV, but inversely to Hcp expression. This regulation was indirect as T6S positively regulated expression of the stress‐response regulator RpoS and the quorum‐sensing regulator VanT, which positively regulate protease expression. Moreover, VtsA‐H proteins were not needed for virulence but did play a role in various stress responses. Thus, these data characterize a new role for T6S in the ecology of bacteria and we hypothesize this role to be a signal sensing mechanism that modulates the expression of regulators of the general stress response.

Bibliography

Weber, B., Hasic, M., Chen, C., Wai, S. N., & Milton, D. L. (2009). Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environmental Microbiology, 11(12), 3018â3028. Portico.

Authors 5

Barbara Weber (first)
Medisa Hasic (additional)
Chang Chen (additional)
Sun Nyunt Wai (additional)
Debra L. Milton (additional)

References 32 Referenced 120

10.1128/JB.00945-08
{'key': 'e_1_2_6_3_1', 'first-page': '272', 'volume-title': 'Bacterial Fish Pathogens: Disease of Farmed and Wild Fish', 'author': 'Austin B.', 'year': '1999'} / Bacterial Fish Pathogens: Disease of Farmed and Wild Fish by Austin B. (1999)
10.1111/j.1574-6976.2008.00104.x
10.1016/j.mib.2008.01.006
10.1038/emboj.2008.269
10.1038/embor.2008.131
10.1128/JB.184.6.1617-1629.2002
10.1111/j.1365-2958.2004.04083.x
10.1111/j.1462-2920.2006.01147.x
10.1093/nar/12.1Part1.387
10.1099/mic.0.2008/016840-0
10.1128/MMBR.66.3.373-395.2002
10.1128/jb.178.17.5188-5198.1996
10.1016/j.ijmm.2006.01.044
10.1128/jb.174.22.7235-7244.1992
10.1128/jb.178.5.1310-1319.1996
10.1126/science.1128393
10.1038/ncb1605
10.1128/AEM.55.6.1400-1405.1989
10.1128/MMBR.62.1.1-34.1998
10.1046/j.1365-2958.2003.03469.x
10.1073/pnas.0510322103
10.1073/pnas.0706532104
10.1128/IAI.66.5.2245-2255.1998
{'key': 'e_1_2_6_26_1', 'volume-title': 'Molecular Cloning: a Laboratory Manual', 'author': 'Sambrook J.', 'year': '1989'} / Molecular Cloning: a Laboratory Manual by Sambrook J. (1989)
10.1111/j.1365-2958.2007.05734.x
10.1515/BC.2005.128
10.1111/j.1742-4658.2008.06470.x
10.1128/JB.184.6.1630-1639.2002
10.1146/annurev.cellbio.21.012704.131001
10.1099/mic.0.2007/014167-0
10.1016/S1534-5807(03)00295-8

Dates

Type	When
Created	16 years, 1 month ago (July 14, 2009, 5:36 a.m.)
Deposited	1 year, 10 months ago (Oct. 15, 2023, 6:27 a.m.)
Indexed	1 month, 1 week ago (July 19, 2025, 11:42 p.m.)
Issued	15 years, 9 months ago (Dec. 1, 2009)
Published	15 years, 9 months ago (Dec. 1, 2009)
Published Online	15 years, 9 months ago (Dec. 1, 2009)
Published Print	15 years, 9 months ago (Dec. 1, 2009)

Funders 0

None

BibTeX

@article{Weber_2009, title={Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum}, volume={11}, ISSN={1462-2920}, url={http://dx.doi.org/10.1111/j.1462-2920.2009.02005.x}, DOI={10.1111/j.1462-2920.2009.02005.x}, number={12}, journal={Environmental Microbiology}, publisher={Wiley}, author={Weber, Barbara and Hasic, Medisa and Chen, Chang and Wai, Sun Nyunt and Milton, Debra L.}, year={2009}, month=dec, pages={3018–3028} }

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