The small Ca2+-binding protein CSE links Ca2+ signalling with nitrogen metabolism and filament integrity in Anabaena sp. PCC 7120

Abstract

Background: Filamentous cyanobacteria represent model organisms for investigating multicellularity. For many species, nitrogen-fixing heterocysts are formed from photosynthetic vegetative cells under nitrogen limitation. Intracellular Ca 2+ has been implicated in the highly regulated process of heterocyst differentiation but its role remains unclear. Ca 2+ is known to operate more broadly in metabolic signalling in cyanobacteria, although the signalling mechanisms are virtually unknown. A Ca 2+-binding protein called the Ca 2+ Sensor EF-hand (CSE) is found almost exclusively in filamentous cyanobacteria. Expression of asr1131 encoding the CSE protein in Anabaena sp. PCC 7120 was strongly induced by low CO 2 conditions, and rapidly downregulated during nitrogen step-down. A previous study suggests a role for CSE and Ca 2+ in regulation of photosynthetic activity in response to changes in carbon and nitrogen availability. Results: In the current study, a mutant Anabaena sp. PCC 7120 strain lacking asr1131 (Δcse) was highly prone to filament fragmentation, leading to a striking phenotype of very short filaments and poor growth under nitrogendepleted conditions. Transcriptomics analysis under nitrogen-replete conditions revealed that genes involved in heterocyst differentiation and function were downregulated in Δcse, while heterocyst inhibitors were upregulated, compared to the wild-type. Conclusions: These results indicate that CSE is required for filament integrity and for proper differentiation and function of heterocysts upon changes in the cellular carbon/nitrogen balance. A role for CSE in transmitting Ca 2+ signals during the first response to changes in metabolic homeostasis is discussed.

Roles of second messengers in the regulation of cyanobacterial physiology: the carbon-concentrating mechanism and beyond

“…Physiological analysis revealed that the Ca 2+ signaling via the CSE protein is required for the regulation of photosynthesis, the correct assembly of phycobilisomes, and downstream energy and electron transfer routes, thereby affecting the overall cell fitness. Moreover, CSE is needed for proper differentiation and full function of heterocysts (Walter et al 2020 ).…”

Unveiling the Secrets of Calcium-Dependent Proteins in Plant Growth-Promoting Rhizobacteria: An Abundance of Discoveries Awaits

“…Although the importance of Ca 2+ for heterocyst formation is clear, the signaling mechanisms remain unknown. Physiological and biochemical studies indicate that a low nitrogen/high carbon signal triggers high intracellular [Ca 2+ ] that are detected by a Ca 2+ sensor with two EF-hand domains (CSE), a protein that is found almost exclusively in filamentous cyanobacteria [194]. The CSE-encoding gene is downregulated during nitrogen limitation and upregulated during CO 2 limitation, the conditions that induce heterocyst differentiation [195].…”

Setting the Stage: Genes Controlling Mechanosensation and Ca 2+ Signaling in Escherichia coli

“…Later, during the evolution of on December 1, 2020 by guest http://jb.asm.org/ Downloaded from eukarya, the chemical properties of Ca 2+ were also adapted for structural roles (8). Ca 2+ ions also play important structural roles in bacterial spores (9), and there are correlative data indicating roles for calcium in chemotaxis (10), differentiation (11), and pathogenicity (12).…”