Аннотация:Multicellularity is a form of organization in living systems, in which a group of cells fulfils more complex functions than any individual cell. Filamentous heterocysts-forming cyanobacteria are the prototype of a multicellular organism, because their cells are not just clustered into agglomerates but represent a functional association unified by exchange of metabolic products and regulatory molecules as well as by electrical communications through highly permeable intercellular contacts (PIC) [Potapova and Koksharova, 2020]. The separation of functions between neighboring cells in any tissue allows some cells to receive an “energy subsidy” from neighbor cells by virtue of ion fluxes through PIC. The energy acquired by this means corresponds to the energy needed for the operation of primary ion pumps (up to one-third of the total cell energy production). The cell-to-cell transmission of energy by means of intercellular electrical communication through permeable intercellular contacts should apparently be regarded as one of the oldest natural technologies of biological systems. The hyperpolarization of cell membranes generated by the cyanobacterial photosynthetic apparatus can perform a number of energy-dependent functions: it promotes the functioning of ATP synthases, transport mechanisms, the motor apparatus, etc., both at the point of illumination and at a distance of tens of cells from the illuminated site. In filamentous cyanobacteria featuring the separation of functions between heterocysts and vegetative cells, the intercellular electrical connections within the trichome ensure the operation of plasma-membrane ATP synthases in heterocysts that are lacking photosynthetic systems of their own. Thus, the heterocysts remain functional and well supplied with ATP resources without the increase in oxygen concentration.
Multicellularity is an evolutionary innovation that represents a new level of organization and is a necessary tool for sophisticated adaptation techniques. From the viewpoint of modern molecular genetics, a group of filamentous cyanobacteria featuring separation of functions between neighboring cells is a prototype of multicellular organization and provides a convenient model for elucidating the mechanisms of regulation of multicellularity, which, apparently, appeared more than once during the evolution in different phylogenetic groups. It is highly important that the ability of bioenergetic cooperation in electrically interconnected cells appeared at the dawn of evolution, billions of years ago, as a structural and functional basis for the division of labor in trichomes of filamentous cyanobacteria, the first multicellular organisms of our planet.
Potapova T.V., Koksharova O.A. Filamentous Cyanobacteria as a Prototype of Multicellular Organisms. Russian Journal of Plant Physiology. 2020. 67:1, pp. 17-30, DOI: 10.1134/S102144372001015X