Quorum Sensing Controls Multicellular Aggregate Formation

Overview

Journal Elife

Specialty Biology

Date 2018 Dec 25

PMID 30582742

Citations 26

Authors

Matthew Jemielita

Ned S Wingreen

Bonnie L Bassler

Affiliations

Soon will be listed here.

Abstract

Bacteria communicate and collectively regulate gene expression using a process called quorum sensing (QS). QS relies on group-wide responses to signal molecules called autoinducers. Here, we show that QS activates a new program of multicellularity in . This program, which we term aggregation, is distinct from the canonical surface-biofilm formation program, which QS represses. Aggregation is induced by autoinducers, occurs rapidly in cell suspensions, and does not require cell division, features strikingly dissimilar from those characteristic of biofilm formation. Extracellular DNA limits aggregate size, but is not sufficient to drive aggregation. A mutagenesis screen identifies genes required for aggregate formation, revealing proteins involved in intestinal colonization, stress response, and a protein that distinguishes the current pandemic strain from earlier pandemic strains. We suggest that QS-controlled aggregate formation is important for to successfully transit between the marine niche and the human host.

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References

Freeman J, Bassler B . A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol. 1999; 31(2):665-77. DOI: 10.1046/j.1365-2958.1999.01208.x. View

Watnick P, Fullner K, Kolter R . A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol. 1999; 181(11):3606-9. PMC: 93833. DOI: 10.1128/JB.181.11.3606-3609.1999. View

Shimkets L . Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol. 1999; 53:525-49. DOI: 10.1146/annurev.micro.53.1.525. View

Kirn T, Lafferty M, Sandoe C, Taylor R . Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol. 2000; 35(4):896-910. DOI: 10.1046/j.1365-2958.2000.01764.x. View

McCarter L . Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J Bacteriol. 2000; 182(19):5513-20. PMC: 110996. DOI: 10.1128/JB.182.19.5513-5520.2000. View

Yildiz F, Dolganov N, Schoolnik G . VpsR, a Member of the Response Regulators of the Two-Component Regulatory Systems, Is Required for Expression of vps Biosynthesis Genes and EPS(ETr)-Associated Phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol. 2001; 183(5):1716-26. PMC: 95057. DOI: 10.1128/JB.183.5.1716-1726.2001. View

Schauder S, Shokat K, Surette M, Bassler B . The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol. 2001; 41(2):463-76. DOI: 10.1046/j.1365-2958.2001.02532.x. View

Dziejman M, Balon E, Boyd D, Fraser C, Heidelberg J, Mekalanos J . Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci U S A. 2002; 99(3):1556-61. PMC: 122229. DOI: 10.1073/pnas.042667999. View

Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler B . Structural identification of a bacterial quorum-sensing signal containing boron. Nature. 2002; 415(6871):545-9. DOI: 10.1038/415545a. View

10.

Zhu J, Miller M, Vance R, Dziejman M, Bassler B, Mekalanos J . Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A. 2002; 99(5):3129-34. PMC: 122484. DOI: 10.1073/pnas.052694299. View

11.

Merrell D, Hava D, Camilli A . Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol Microbiol. 2002; 43(6):1471-91. DOI: 10.1046/j.1365-2958.2002.02857.x. View

12.

Miller M, Skorupski K, Lenz D, Taylor R, Bassler B . Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell. 2002; 110(3):303-14. DOI: 10.1016/s0092-8674(02)00829-2. View

13.

Colwell R, Huq A, Islam M, Aziz K, Yunus M, Khan N . Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci U S A. 2003; 100(3):1051-5. PMC: 298724. DOI: 10.1073/pnas.0237386100. View

14.

Rickard A, Gilbert P, High N, Kolenbrander P, Handley P . Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 2003; 11(2):94-100. DOI: 10.1016/s0966-842x(02)00034-3. View

15.

Brinkman A, Ettema T, de Vos W, van der Oost J . The Lrp family of transcriptional regulators. Mol Microbiol. 2003; 48(2):287-94. DOI: 10.1046/j.1365-2958.2003.03442.x. View

16.

Silva A, Pham K, Benitez J . Haemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae. Microbiology (Reading). 2003; 149(Pt 7):1883-1891. DOI: 10.1099/mic.0.26086-0. View

17.

Kierek K, Watnick P . Environmental determinants of Vibrio cholerae biofilm development. Appl Environ Microbiol. 2003; 69(9):5079-88. PMC: 194957. DOI: 10.1128/AEM.69.9.5079-5088.2003. View

18.

LANKFORD C . Factors of virulence of Vibrio cholerae. Ann N Y Acad Sci. 1960; 88:1203-12. DOI: 10.1111/j.1749-6632.1960.tb20111.x. View

19.

Hammer B, Bassler B . Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol. 2003; 50(1):101-4. DOI: 10.1046/j.1365-2958.2003.03688.x. View

20.

Zhu J, Mekalanos J . Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell. 2003; 5(4):647-56. DOI: 10.1016/s1534-5807(03)00295-8. View