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

J. Muñoz-García,Saúl Ares

Published 2016 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Cyanobacteria produce an important fraction of oxygen on Earth and, together with archaea, fix atmospheric nitrogen used by all other organisms. Some types live in colonies with specialized cells that perform different functions. In particular, the genus Anabaena forms filaments in which some cells differentiate, forming patterns to effectively provide nitrogen for the colony. We present a theory that combines genetic, metabolic, and morphological aspects to understand this prokaryotic example of multicellularity. Our results quantitatively reproduce the appearance and dynamics of this pattern and are used to learn how different aspects, like fixed-nitrogen diffusion, cell division, or stochasticity, affect it. Cyanobacteria forming one-dimensional filaments are paradigmatic model organisms of the transition between unicellular and multicellular living forms. Under nitrogen-limiting conditions, in filaments of the genus Anabaena, some cells differentiate into heterocysts, which lose the possibility to divide but are able to fix environmental nitrogen for the colony. These heterocysts form a quasiregular pattern in the filament, representing a prototype of patterning and morphogenesis in prokaryotes. Recent years have seen advances in the identification of the molecular mechanism regulating this pattern. We use these data to build a theory on heterocyst pattern formation, for which both genetic regulation and the effects of cell division and filament growth are key components. The theory is based on the interplay of three generic mechanisms: local autoactivation, early long-range inhibition, and late long-range inhibition. These mechanisms can be identified with the dynamics of hetR, patS, and hetN expression. Our theory reproduces quantitatively the experimental dynamics of pattern formation and maintenance for wild type and mutants. We find that hetN alone is not enough to play the role as the late inhibitory mechanism: a second mechanism, hypothetically the products of nitrogen fixation supplied by heterocysts, must also play a role in late long-range inhibition. The preponderance of even intervals between heterocysts arises naturally as a result of the interplay between the timescales of genetic regulation and cell division. We also find that a purely stochastic initiation of the pattern, without a two-stage process, is enough to reproduce experimental observations.

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