Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control
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Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control. / Ozaki, Shogo; Schalch-Moser, Annina; Zumthor, Ludwig; Manfredi, Pablo; Ebbensgaard, Anna; Schirmer, Tilman; Jenal, Urs.
In: Molecular Microbiology, Vol. 94, No. 3, 11.2014, p. 580-94.Research output: Contribution to journal › Journal article › Research › peer-review
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T1 - Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control
AU - Ozaki, Shogo
AU - Schalch-Moser, Annina
AU - Zumthor, Ludwig
AU - Manfredi, Pablo
AU - Ebbensgaard, Anna
AU - Schirmer, Tilman
AU - Jenal, Urs
N1 - © 2014 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
PY - 2014/11
Y1 - 2014/11
N2 - When Caulobacter crescentus enters S-phase the replication initiation inhibitor CtrA dynamically positions to the old cell pole to be degraded by the polar ClpXP protease. Polar delivery of CtrA requires PopA and the diguanylate cyclase PleD that positions to the same pole. Here we present evidence that PopA originated through gene duplication from its paralogue response regulator PleD and subsequent co-option as c-di-GMP effector protein. While the C-terminal catalytic domain (GGDEF) of PleD is activated by phosphorylation of the N-terminal receiver domain, functional adaptation has reversed signal transduction in PopA with the GGDEF domain adopting input function and the receiver domain serving as regulatory output. We show that the N-terminal receiver domain of PopA specifically interacts with RcdA, a component required for CtrA degradation. In contrast, the GGDEF domain serves to target PopA to the cell pole in response to c-di-GMP binding. In agreement with the divergent activation and targeting mechanisms, distinct markers sequester PleD and PopA to the old cell pole upon S-phase entry. Together these data indicate that PopA adopted a novel role as topology specificity factor to help recruit components of the CtrA degradation pathway to the protease specific old cell pole of C. crescentus.
AB - When Caulobacter crescentus enters S-phase the replication initiation inhibitor CtrA dynamically positions to the old cell pole to be degraded by the polar ClpXP protease. Polar delivery of CtrA requires PopA and the diguanylate cyclase PleD that positions to the same pole. Here we present evidence that PopA originated through gene duplication from its paralogue response regulator PleD and subsequent co-option as c-di-GMP effector protein. While the C-terminal catalytic domain (GGDEF) of PleD is activated by phosphorylation of the N-terminal receiver domain, functional adaptation has reversed signal transduction in PopA with the GGDEF domain adopting input function and the receiver domain serving as regulatory output. We show that the N-terminal receiver domain of PopA specifically interacts with RcdA, a component required for CtrA degradation. In contrast, the GGDEF domain serves to target PopA to the cell pole in response to c-di-GMP binding. In agreement with the divergent activation and targeting mechanisms, distinct markers sequester PleD and PopA to the old cell pole upon S-phase entry. Together these data indicate that PopA adopted a novel role as topology specificity factor to help recruit components of the CtrA degradation pathway to the protease specific old cell pole of C. crescentus.
KW - Bacterial Proteins/genetics
KW - Caulobacter crescentus/cytology
KW - Cell Cycle Checkpoints
KW - Cyclic GMP/analogs & derivatives
KW - Models, Molecular
KW - Phosphorylation
KW - Protein Binding
KW - Protein Conformation
KW - Protein Interaction Domains and Motifs
KW - Protein Processing, Post-Translational
U2 - 10.1111/mmi.12777
DO - 10.1111/mmi.12777
M3 - Journal article
C2 - 25171231
VL - 94
SP - 580
EP - 594
JO - Molecular Microbiology
JF - Molecular Microbiology
SN - 0950-382X
IS - 3
ER -
ID: 202067620