Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress

Agostoni, Marco; Logan-Jackson, Alshaé R.; Heinz, Emily R.; Severin, Geoffrey B.; Bruger, Eric L.; Waters, Christopher M.; Montgomery, Beronda L.

doi:10.3389/fmicb.2018.01121

Title: Homeostasis of Second Messenger Cyclic-di-AMP Is Critical for Cyanobacterial Fitness and Acclimation to Abiotic Stress

Journal Article · Tue May 29 00:00:00 EDT 2018 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.01121· OSTI ID:1439352

Agostoni, Marco; Logan-Jackson, Alshaé R.; Heinz, Emily R.; Severin, Geoffrey B.; Bruger, Eric L.; Waters, Christopher M.; Montgomery, Beronda L.

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.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Laboratory

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

Grant/Contract Number:: FG02-91ER20021; GM109259; AI130554; MCB-1243983; T32-GM110523

OSTI ID:: 1439352

Alternate ID(s):: OSTI ID: 1510459; OSTI ID: 1603486

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: Switzerland

Language:: English

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Cited by: 13 works

Citation information provided by
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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 Zhu, Yan; Pham, Thi Huong; Nhiep, Thi Hanh Nguyen Molecular Microbiology, Vol. 99, Issue 6 https://doi.org/10.1111/mmi.13281	journal	December 2015
STING-Dependent Recognition of Cyclic di-AMP Mediates Type I Interferon Responses during Chlamydia trachomatis Infection Barker, Jeffrey R.; Koestler, Benjamin J.; Carpenter, Victoria K. mBio, Vol. 4, Issue 3 https://doi.org/10.1128/mBio.00018-13	journal	April 2013
The protein Slr1143 is an active diguanylate cyclase in Synechocystis sp. PCC 6803 and interacts with the photoreceptor Cph2 Angerer, Veronika; Schwenk, Philipp; Wallner, Thomas Microbiology, Vol. 163, Issue 6 https://doi.org/10.1099/mic.0.000475	journal	June 2017
NaCl enhances cellular cAMP and upregulates genes related to heterocyst development in the cyanobacterium, Anabaena sp. strain PCC 7120 Imashimizu, Masahiko; Yoshimura, Hidehisa; Katoh, Hiroshi FEMS Microbiology Letters, Vol. 252, Issue 1 https://doi.org/10.1016/j.femsle.2005.08.035	journal	November 2005

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cyanobacteria
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