Abstract

BackgroundFilamentous cyanobacteria that differentiate multiple cell types are considered the peak of prokaryotic complexity and their evolution has been studied in the context of multicellularity origins. Species that form true-branching filaments exemplify the most complex cyanobacteria. However, the mechanisms underlying the true-branching morphology remain poorly understood despite of several investigations that focused on the identification of novel genes or pathways. An alternative route for the evolution of novel traits is based on existing phenotypic plasticity. According to that scenario – termed genetic assimilation – the fixation of a novel phenotype precedes the fixation of the genotype.ResultsHere we show that the evolution of transcriptional regulatory elements constitutes a major mechanism for the evolution of new traits. We found that supplementation with sucrose reconstitutes the ancestral branchless phenotype of two true-branching Fischerella species and compared the transcription start sites (TSSs) between the two phenotypic states. Our analysis uncovers several orthologous TSSs whose transcription level is correlated with the true-branching phenotype. These TSSs are found in genes that encode components of the septosome and elongasome (e.g., fraC and mreB).ConclusionsThe concept of genetic assimilation supplies a tenable explanation for the evolution of novel traits but testing its feasibility is hindered by the inability to recreate and study the evolution of present-day traits. We present a novel approach to examine transcription data for the plasticity first route and provide evidence for its occurrence during the evolution of complex colony morphology in true-branching cyanobacteria. Our results reveal a route for evolution of the true-branching phenotype in cyanobacteria via modification of the transcription level of pre-existing genes. Our study supplies evidence for the ‘plasticity-first’ hypothesis and highlights the importance of transcriptional regulation in the evolution of novel traits.

Highlights

  • Filamentous cyanobacteria that differentiate multiple cell types are considered the peak of prokaryotic complexity and their evolution has been studied in the context of multicellularity origins

  • Phenotypic plasticity of the true-branching colony morphology To screen for conditions that generate an ancestor-like filamentous and branchless phenotype, we cultured the true-branching cyanobacteria F. muscicola Pasteur culture collection of Cyanobacteria (PCC) 7414 and F. thermalis PCC 7521 under different conditions

  • In Nostoc punctiforme, the importance of sucrose has been highlighted by recent findings suggesting that it serves as a hormogonium-repressing-factor (HRF)

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Summary

Introduction

Filamentous cyanobacteria that differentiate multiple cell types are considered the peak of prokaryotic complexity and their evolution has been studied in the context of multicellularity origins. An alternative route for the evolution of novel traits is based on existing phenotypic plasticity. Explaining the evolution of novel phenotypic traits has been a long-standing challenge in biology [1]. A major conundrum is whether the origin of a novel trait can evolve via adaptive genetic change alone or whether it could be initiated by a plastic phenotype that is induced in direct response to an environmental cue. We propose to make use of the traces of past evolution in genomes of contemporary organisms by searching for molecular signatures of the ‘plasticity-first’ hypothesis for the trait of interest. We test this proposal by investigating the underlying genetic mechanisms of the complex trait ‘true-branching’ in a prokaryotic system – the cyanobacteria

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