Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae

Severin, Geoffrey B.; Ramliden, Miriam S.; Hawver, Lisa A.; Wang, Kun; Pell, Macy E.; Kieninger, Ann-Katrin; Khataokar, Atul; O’Hara, Brendan J.; Behrmann, Lara V.; Neiditch, Matthew B.; Benning, Christoph; Waters, Christopher M.; Ng, Wai-Leung

doi:10.1073/pnas.1801233115

Title: Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae

Journal Article · 11 June 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1801233115 · OSTI ID:1441128

Severin, Geoffrey B. ^[1]; Ramliden, Miriam S. ^[2]; Hawver, Lisa A. ^[2];

^[1]; Pell, Macy E. ^[1]; Kieninger, Ann-Katrin ^[1]; Khataokar, Atul ^[3]; O’Hara, Brendan J. ^[2]; Behrmann, Lara V. ^[1]; Neiditch, Matthew B. ^[3];

^[1]; Waters, Christopher M. ^[1];

^[2]

Michigan State Univ., East Lansing, MI (United States)
Tufts Univ., Boston, MA (United States)
State Univ. of New Jersey, Newark, NJ (United States)

Sensing and responding to environmental changes is critical for bacteria to adapt and thrive, and nucleotide-derived second messengers are central signaling systems in this process. The most recently identified bacterial cyclic dinucleotide second messenger, 3', 3'-cyclic GMP-AMP (cGAMP), was first discovered in the El Tor biotype of Vibrio cholerae. The cGAMP synthase, DncV, is encoded on the VSP-1 pathogenicity island, which is found in all El Tor isolates that are responsible for the current seventh pandemic of cholera but not in the classical biotype. We determined that unregulated production of DncV inhibits growth in El TorV. choleraebut has no effect on the classical biotype. This cGAMP-dependent phenotype can be suppressed by null mutations invc0178immediately 5' ofdncVin VSP-1. VC0178 [renamed as cGAMP-activated phospholipase in Vibrio (CapV)] is predicted to be a patatin-like phospholipase, and coexpression of capVand dncVis sufficient to induce growth inhibition in classicalV. choleraeandEscherichia coli. Furthermore, cGAMP binds to CapV and directly activates its hydrolase activity in vitro. CapV activated by cGAMP in vivo degrades phospholipids in the cell membrane, releasing 16:1 and 18:1 free fatty acids. Together, we demonstrate that cGAMP activates CapV phospholipase activity to target the cell membrane and imply that acquisition of this second messenger signaling pathway may contribute to the emergence of the El Tor biotype as the etiological agent behind the seventh cholera pandemic.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); USDOE

Grant/Contract Number:: FG02-91ER20021; FG02-98ER20305

OSTI ID:: 1441128

Alternate ID(s):: OSTI ID: 1547352

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 26; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
second messengers
cyclic dinucleotides
phospholipid metabolism
pathogenicity island
cGAMP

Title: Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae

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