Secreted Proteases Control the Timing of Aggregative Community Formation in Vibrio cholerae

TY - JOUR

T1 - Secreted Proteases Control the Timing of Aggregative Community Formation in Vibrio cholerae

AU - Jemielita, Matthew

AU - Mashruwala, Ameya A.

AU - Valastyan, Julie S.

AU - Wingreen, Ned S.

AU - Bassler, Bonnie L.

N1 - Publisher Copyright: © 2021 American Society for Microbiology. All rights reserved.

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Bacteria orchestrate collective behaviors using the cell-cell communication process called quorum sensing (QS). QS relies on the synthesis, release, and group-wide detection of small molecules called autoinducers. In Vibrio cholerae, a multicellular community aggregation program occurs in liquid, during the stationary phase, and in the high-cell-density QS state. Here, we demonstrate that this aggregation program consists of two subprograms. In one subprogram, which we call void formation, structures form that contain few cells but provide a scaffold within which cells can embed. The other subprogram relies on flagellar machinery and enables cells to enter voids. A genetic screen for factors contributing to void formation, coupled with companion molecular analyses, showed that four extracellular proteases, Vca0812, Vca0813, HapA, and PrtV, control the onset timing of both void formation and aggregation; moreover, proteolytic activity is required. These proteases, or their downstream products, can be shared between void-producing and nonvoid- forming cells and can elicit aggregation in a normally nonaggregating V. cholerae strain. Employing multiple proteases to control void formation and aggregation timing could provide a redundant and irreversible path to commitment to this community lifestyle.

AB - Bacteria orchestrate collective behaviors using the cell-cell communication process called quorum sensing (QS). QS relies on the synthesis, release, and group-wide detection of small molecules called autoinducers. In Vibrio cholerae, a multicellular community aggregation program occurs in liquid, during the stationary phase, and in the high-cell-density QS state. Here, we demonstrate that this aggregation program consists of two subprograms. In one subprogram, which we call void formation, structures form that contain few cells but provide a scaffold within which cells can embed. The other subprogram relies on flagellar machinery and enables cells to enter voids. A genetic screen for factors contributing to void formation, coupled with companion molecular analyses, showed that four extracellular proteases, Vca0812, Vca0813, HapA, and PrtV, control the onset timing of both void formation and aggregation; moreover, proteolytic activity is required. These proteases, or their downstream products, can be shared between void-producing and nonvoid- forming cells and can elicit aggregation in a normally nonaggregating V. cholerae strain. Employing multiple proteases to control void formation and aggregation timing could provide a redundant and irreversible path to commitment to this community lifestyle.

KW - Aggregation

KW - Biofilms

KW - Proteases

KW - Quorum sensing

KW - Vibrio cholerae

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UR - http://www.scopus.com/inward/citedby.url?scp=85121990017&partnerID=8YFLogxK

U2 - 10.1128/mBio.01518-21

DO - 10.1128/mBio.01518-21

M3 - Article

C2 - 34809464

SN - 2161-2129

VL - 12

JO - mBio

JF - mBio

IS - 6

M1 - e01518-21

ER -