U.S. Department of EnergyOffice of Scientific and Technical Information
Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress
Abstract
Second messengers are intracellular molecules regulated by external stimuli known as first messengers that are used for rapid organismal responses to dynamic environmental changes. Cyclic di-AMP (c-di-AMP) is a relatively newly discovered second messenger implicated in cell wall homeostasis in many pathogenic bacteria. C-di-AMP is synthesized from ATP by diadenylyl cyclases (DAC) and degraded by specific c-di-AMP phosphodiesterases (PDE). C-di-AMP DACs and PDEs are present in all sequenced cyanobacteria, suggesting roles for c-di-AMP in the physiology and/or development of these organisms. Despite conservation of these genes across numerous cyanobacteria, the functional roles of c-di-AMP in cyanobacteria have not been well-investigated. In a unique feature of cyanobacteria, phylogenetic analysis indicated that the broadly conserved DAC, related to CdaA/DacA, is always co-associated in an operon with genes critical for controlling cell wall synthesis. To investigate phenotypes regulated by c-di-AMP in cyanobacteria, we overexpressed native DAC (sll0505) and c-di-AMP PDE (slr0104) genes in the cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis) to increase and decrease intracellular c-di-AMP levels, respectively. DAC- and PDE-overexpression strains, showed abnormal aggregation phenotypes, suggesting functional roles for regulating c-di-AMP homeostasis in vivo. As c-di-AMP may be implicated in osmotic responses in cyanobacteria, we tested whether sorbitol and NaCl stressesmore »
- Authors:
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1439352
- Alternate Identifier(s):
- OSTI ID: 1510459; OSTI ID: 1603486
- Grant/Contract Number:
- FG02-91ER20021; GM109259; AI130554; MCB-1243983; T32-GM110523
- Resource Type:
- Journal Article: Published Article
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; abiotic stresses; c-di-AMP; c-di-GMP; cyanobacteria; ionic stress; osmotic stress; salt stress; second messengers
Citation Formats
Agostoni, Marco, Logan-Jackson, Alshaé R., Heinz, Emily R., Severin, Geoffrey B., Bruger, Eric L., Waters, Christopher M., and Montgomery, Beronda L. Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress. Switzerland: N. p., 2018.
Web. doi:10.3389/fmicb.2018.01121.
Agostoni, Marco, Logan-Jackson, Alshaé R., Heinz, Emily R., Severin, Geoffrey B., Bruger, Eric L., Waters, Christopher M., & Montgomery, Beronda L. Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress. Switzerland. https://doi.org/10.3389/fmicb.2018.01121
Agostoni, Marco, Logan-Jackson, Alshaé R., Heinz, Emily R., Severin, Geoffrey B., Bruger, Eric L., Waters, Christopher M., and Montgomery, Beronda L. 2018.
"Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress". Switzerland. https://doi.org/10.3389/fmicb.2018.01121.
@article{osti_1439352,
title = {Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress},
author = {Agostoni, Marco and Logan-Jackson, Alshaé R. and Heinz, Emily R. and Severin, Geoffrey B. and Bruger, Eric L. and Waters, Christopher M. and Montgomery, Beronda L.},
abstractNote = {Second messengers are intracellular molecules regulated by external stimuli known as first messengers that are used for rapid organismal responses to dynamic environmental changes. Cyclic di-AMP (c-di-AMP) is a relatively newly discovered second messenger implicated in cell wall homeostasis in many pathogenic bacteria. C-di-AMP is synthesized from ATP by diadenylyl cyclases (DAC) and degraded by specific c-di-AMP phosphodiesterases (PDE). C-di-AMP DACs and PDEs are present in all sequenced cyanobacteria, suggesting roles for c-di-AMP in the physiology and/or development of these organisms. Despite conservation of these genes across numerous cyanobacteria, the functional roles of c-di-AMP in cyanobacteria have not been well-investigated. In a unique feature of cyanobacteria, phylogenetic analysis indicated that the broadly conserved DAC, related to CdaA/DacA, is always co-associated in an operon with genes critical for controlling cell wall synthesis. To investigate phenotypes regulated by c-di-AMP in cyanobacteria, we overexpressed native DAC (sll0505) and c-di-AMP PDE (slr0104) genes in the cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis) to increase and decrease intracellular c-di-AMP levels, respectively. DAC- and PDE-overexpression strains, showed abnormal aggregation phenotypes, suggesting functional roles for regulating c-di-AMP homeostasis in vivo. As c-di-AMP may be implicated in osmotic responses in cyanobacteria, we tested whether sorbitol and NaCl stresses impacted expression of sll0505 and slr0104 or intracellular c-di-AMP levels in Synechocystis. Additionally, to determine the range of cyanobacteria in which c-di-AMP may function, we assessed c-di-AMP levels in two unicellular cyanobacteria, i.e., Synechocystis and Synechococcus elongatus PCC 7942, and two filamentous cyanobacteria, i.e., Fremyella diplosiphon and Anabaena sp. PCC 7120. C-di-AMP levels responded differently to abiotic stress signals in distinct cyanobacteria strains, whereas salt stress uniformly impacted another second messenger cyclic di-GMP in cyanobacteria. Together, these results suggest regulation of c-di-AMP homeostasis in cyanobacteria and implicate a role for the second messenger in maintaining cellular fitness in response to abiotic stress.},
doi = {10.3389/fmicb.2018.01121},
url = {https://www.osti.gov/biblio/1439352},
journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 9,
place = {Switzerland},
year = {Tue May 29 00:00:00 EDT 2018},
month = {Tue May 29 00:00:00 EDT 2018}
}
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- Oppenheimer-Shaanan, Yaara; Wexselblatt, Ezequiel; Katzhendler, Jehoshua
- EMBO reports, Vol. 12, Issue 6
Salinity impacts photosynthetic pigmentation and cellular morphology changes by distinct mechanisms in Fremyella diplosiphon
journal, March 2013
- Singh, Shailendra P.; Montgomery, Beronda L.
- Biochemical and Biophysical Research Communications, Vol. 433, Issue 1
Five Histidine Kinases Perceive Osmotic Stress and Regulate Distinct Sets of Genes in Synechocystis
journal, October 2004
- Paithoonrangsarid, Kalyanee; Shoumskaya, Maria A.; Kanesaki, Yu
- Journal of Biological Chemistry, Vol. 279, Issue 51
Bacillus subtilis DisA helps to circumvent replicative stress during spore revival
journal, November 2017
- Raguse, Marina; Torres, Rubén; Seco, Elena M.
- DNA Repair, Vol. 59
Characterization of Genes Encoding Multi-domain Proteins in the Genome of the Filamentous Nitrogen-fixing Cyanobacterium Anabaena sp. Strain PCC 7120
journal, January 2001
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- DNA Research, Vol. 8, Issue 6
A Turquoise Mutant Genetically Separates Expression of Genes Encoding Phycoerythrin and Its Associated Linker Peptides
journal, February 2002
- Seib, L. O.; Kehoe, D. M.
- Journal of Bacteriology, Vol. 184, Issue 4
Cyclic-di-AMP synthesis by the diadenylate cyclase CdaA is modulated by the peptidoglycan biosynthesis enzyme GlmM in L actococcus lactis : GlmM modulates c-di-AMP synthesis in
journal, December 2015
- Zhu, Yan; Pham, Thi Huong; Nhiep, Thi Hanh Nguyen
- Molecular Microbiology, Vol. 99, Issue 6
STING-Dependent Recognition of Cyclic di-AMP Mediates Type I Interferon Responses during Chlamydia trachomatis Infection
journal, April 2013
- Barker, Jeffrey R.; Koestler, Benjamin J.; Carpenter, Victoria K.
- mBio, Vol. 4, Issue 3
The protein Slr1143 is an active diguanylate cyclase in Synechocystis sp. PCC 6803 and interacts with the photoreceptor Cph2
journal, June 2017
- Angerer, Veronika; Schwenk, Philipp; Wallner, Thomas
- Microbiology, Vol. 163, Issue 6
NaCl enhances cellular cAMP and upregulates genes related to heterocyst development in the cyanobacterium, Anabaena sp. strain PCC 7120
journal, November 2005
- Imashimizu, Masahiko; Yoshimura, Hidehisa; Katoh, Hiroshi
- FEMS Microbiology Letters, Vol. 252, Issue 1