Formation and maintenance of nitrogen-fixing cell patterns in filamentous cyanobacteria

Abstract

Cyanobacteria forming one-dimensional filaments are paradigmaticmodel organisms of the transition between unicellular andmulticellular living forms. Under nitrogen-limiting conditions, infilaments of the genus Anabaena, some cells differentiate into heterocysts,which lose the possibility to divide but are able to fixenvironmental nitrogen for the colony. These heterocysts form aquasiregular pattern in the filament, representing a prototype ofpatterning and morphogenesis in prokaryotes. Recent years haveseen advances in the identification of the molecular mechanism regulatingthis pattern. We use these data to build a theory on heterocystpattern formation, for which both genetic regulation and theeffects of cell division and filament growth are key components. Thetheory is based on the interplay of three generic mechanisms: localautoactivation, early long-range inhibition, and late long-range inhibition.These mechanisms can be identified with the dynamics ofhetR, patS, and hetN expression. Our theory reproduces quantitativelythe experimental dynamics of pattern formation and maintenancefor wild type and mutants. We find that hetN alone is notenough to play the role as the late inhibitory mechanism: a secondmechanism, hypothetically the products of nitrogen fixation suppliedby heterocysts, must also play a role in late long-range inhibition.The preponderance of even intervals between heterocysts arisesnaturally as a result of the interplay between the timescales of geneticregulation and cell division.We also find that a purely stochasticinitiation of the pattern, without a two-stage process, is enoughto reproduce experimental observations.