Survival strategies in the aquatic and terrestrial world: the impact of second messengers on cyanobacterial processes

Abstract

Second messengers are intracellular substances regulated by specific external stimuli globally known as first messengers. Cells rely on second messengers to generate rapid responses to environmental changes and the importance of their roles is becoming increasingly realized in cellular signaling research. Cyanobacteria are photooxygenic bacteria that inhabit most of Earth's environments. The ability of cyanobacteria to survive in ecologically diverse habitats is due to their capacity to adapt and respond to environmental changes. This article reviews known second messenger-controlled physiological processes in cyanobacteria. Second messengers used in these systems include the element calcium (Ca2+), nucleotide-based guanosine tetraphosphate or pentaphosphate (ppGpp or pppGpp, represented as (p)ppGpp), cyclic adenosine 3',5'-monophosphate (cAMP), cyclic dimeric GMP (c-di-GMP), cyclic guanosine 3',5'-monophosphate (cGMP), and cyclic dimeric AMP (c-di-AMP), and the gaseous nitric oxide (NO). The discussion focuses on processes central to cyanobacteria, such as nitrogen fixation, light perception, photosynthesis-related processes, and gliding motility. In addition, we address future research trajectories needed to better understand the signaling networks and cross talk in the signaling pathways of these molecules in cyanobacteria. Second messengers have significant potential to be adapted as technological tools and we highlight possible novel and practical applications based on our understanding of these molecules and the signaling networks that they control.

Figure 1

Specific second messengers are regulated by an external stimulus (i.e., first messenger) and will bind specific effectors. In turn, the effector will initiate a signal cascade, which leads to organism-specific outputs (examples shown for cyanobacteria). This mechanism is common for all known second messengers.

Figure 2

External signals controlling free intracellular Ca²⁺ levels and phenotypes or processes that are controlled by Ca²⁺ in cyanobacteria. Levels of free intracellular Ca²⁺ are regulated externally by influx(es) of extracellular Ca²⁺ through ion channels or internally by release of Ca²⁺ from Ca²⁺-binding proteins. Green arrow from free [Ca²⁺] indicates increased Ca²⁺ levels from external sources leads to noted phenotypes, whereas the red arrow indicates that increased Ca²⁺ levels from internal sources leads to the noted phenotypes. Blue arrow indicates that referenced studies did not demonstrate whether the noted phenotypes are under external or internal control. +, indicates process promoted by increased cellular Ca²⁺ levels; −, indicates process inhibited by increased intracellular Ca²⁺ levels.

Figure 3

External factors controlling intracellular levels of (p)ppGpp and phenotypes or processes that are controlled by (p)ppGpp in cyanobacteria. (p)ppGpp is synthesized from GDP or GTP together with ATP by RelA or SpoT proteins and degraded to GDP or GTP and the by-product pyrophosphate (PPi) by SpoT. Dashed lines denote hypothetical or suggested role of cyanophages under nutrient-deficient growth conditions in controlling internal (p)ppGpp levels. Green arrow indicates that increased synthesis of (p)ppGpp leads to noted phenotypes, whereas red arrow indicates that degradation of (p)ppGpp leads to noted phenotypes. +, indicates process promoted by increased (p)ppGpp synthesis; −, indicates process inhibited by increased (p)ppGpp levels.

Figure 4

External factors controlling intracellular levels of cAMP and phenotypes or processes that are controlled by cAMP in cyanobacteria. Cyclic AMP is synthesized from ATP by adenylate cyclases (AC) and degraded to AMP by cAMP-specific phosphodiesterases. Green arrow indicates that increased synthesis of cAMP leads to noted phenotypes. +, indicates process promoted by increased cAMP levels.

Figure 5

External factors controlling intracellular levels of cGMP and phenotypes or processes that are controlled by cGMP in cyanobacteria. Cyclic GMP is synthesized by guanylyl cyclases and degraded by cGMP-specific phosphodiesterases. −, indicates process inhibited by increased cGMP levels.

Figure 6

External factors controlling intracellular levels of c-di-GMP and phenotypes or processes that are controlled by c-di-GMP in cyanobacteria. Cyclic di-GMP is synthesized from two GTP by diguanylate cyclases and degraded to two GMP or pGpG by phosphodiesterases (PDE). Dashed lines denote hypothetical or suggested roles of light in activating PDEs and resulting phenotypes; these relationships between light absorption and c-di-GMP degradation are proposed as PDEs are often associated with photoreceptors in cyanobacteria [16] and this class of proteins induces motility and promotes dispersion in several pathogenic bacteria [6]. Green arrow indicates that increased c-di-GMP synthesis supports the noted phenotypes, whereas a red arrow indicates that increased degradation of c-di-GMP is associated with the noted phenotypes. +, indicates process promoted by altered c-di-GMP levels; −, indicates process inhibited by altered c-di-GMP levels.

Figure 7

External factors controlling intracellular levels of nitric oxide (NO) and phenotypes or processes that are controlled by NO in cyanobacteria. NO is synthesized from nitrite (NO₂) by nitrite reductase (and/or NO synthase) during denitrification and reduced to nitrous oxide (N₂O) by nitric oxide reductase. Dashed lines denote hypothetical roles of NO synthase in controlling NO concentration. Green arrow pointing to the dashed green box indicates that cell proliferation could be induced (+) by high intracellular levels of NO [96].

Figure 8

Suggested external factors controlling intracellular levels of c-di-AMP and phenotypes or processes that are proposed to be controlled by c-di-AMP in cyanobacteria. Cyclic di-AMP is synthesized from two ATP by diadenylyl cyclases and degraded to pApA by a putative phosphodiesterase. Green arrow pointing to the dashed green box indicates that the production of osmoprotectants could be induced (+) by increased c-di-AMP synthesis.