Abstract

Cyanobacteria are among the most morphologically diverse prokaryotic phyla on Earth. Their morphotypes range from unicellular to multicellular filaments, yet mechanisms underlying the evolution of filamentous morphologies remain unknown. Here, we implement phylogenomic, Bayesian molecular clock and gene-tree-species-tree reconciliation analyses to estimate when genes encoding cell-cell joining structures first evolved. We also characterise septal structures and measure intercellular communication rates in non-model and early-branching filamentous strains. Our results suggest that genes encoding septal proteins (namely sepJ, sepI, and fraE) and potentially pattern formation (hetR) evolved in the Neoarchaean [~]2.6-2.7 billion years (Ga) ago. Later, at the start of the Great Oxygenation Event [~]2.5 Ga, genes involved in cellular differentiation (namely hetZ, patU3 and hglK) appeared. Our results predict that early-branching lineages like Pseudanabaena were capable of intercellular communication, but further innovations in cellular differentiation were needed to drive ecological expansion on a scale large enough to permanently oxygenate Earths atmosphere.