Mechanism of intercellular molecular exchange in heterocyst-forming cyanobacteria

Abstract

Heterocyst-forming filamentous cyanobacteria are true multicellular prokaryotes, in which heterocysts and vegetative cells have complementary metabolism and are mutually dependent. The mechanism for metabolite exchange between cells has remained unclear. To gain insight into the mechanism and kinetics of metabolite exchange, we introduced calcein, a 623-Da fluorophore, into the Anabaena cytoplasm. We used fluorescence recovery after photobleaching to quantify rapid diffusion of this molecule between the cytoplasms of all the cells in the filament. This indicates nonspecific intercellular channels allowing the movement of molecules from cytoplasm to cytoplasm. We quantify rates of molecular exchange as filaments adapt to diazotrophic growth. Exchange among vegetative cells becomes faster as filaments differentiate, becoming considerably faster than exchange with heterocysts. Slower exchange is probably a price paid to maintain a microaerobic environment in the heterocyst. We show that the slower exchange is partly due to the presence of cyanophycin polar nodules in heterocysts. The phenotype of a null mutant identifies FraG (SepJ), a membrane protein localised at the cell-cell interface, as a strong candidate for the channel-forming protein.

Nutritional stress induces exchange of cell material and energetic coupling between bacterial species

“…The fact that there is an exchange of molecules between D. vulgaris and E. coli, but not between C. acetobutylicum and E. coli, is compatible with this hypothesis, because E. coli, like C. acetobutylicum, is able to ferment glucose, and is not suffering a nutrient stress condition in the GY medium. The communication between bacteria, which can take several forms [33][34][35][36][37][38] , is essential for coordinating the behaviour of the whole community. Thus, communication between cells in pure culture regulates the population density by emitting, receiving and responding to a chemical signal, that is, quorum sensing 39,40 .…”

The evolutionary path to terminal differentiation and division of labor in cyanobacteria

“…Each cell is in turn also encapsulated by its own cytoplasmic membrane. In addition, there is some evidence for direct exchange between the cytoplasms of adjacent cells through membrane channels [56].…”

Metabolic cross-feeding via intercellular nanotubes among bacteria

“…Such mechanisms include, for example, the production of outer membrane vesicles, as they are used by many bacterial species to deliver cargo to other cells [12][13][14][15][16] . Alternatively, bacterial cells may connect via channels 17 , nanotubes 18 , pili 19 or transiently fuse their outer membrane 20 to transfer cytoplasmic components or outer membrane materials.…”