Loss of Filamentous Multicellularity in : the Extremophile Sp. Strain UTEX B3054 Retained Multicellular Features at the Genomic and Behavioral Levels

Multicellularity in played a key role in their habitat expansion, contributing to the Great Oxidation Event around 2.45 billion to 2.32 billion years ago. Evolutionary studies have indicated that some unicellular cyanobacteria emerged from multicellular ancestors, yet little is known about how the emergence of new unicellular morphotypes from multicellular ancestors occurred. Our results give new insights into the evolutionary reversion from which the lineage emerged. Flow cytometry and microscopy results revealed morphological plasticity involving the patterned formation of multicellular morphotypes sensitive to environmental stimuli. Genomic analyses unveiled the presence of multicellularity-associated genes in its genome. Calcein-fluorescence recovery after photobleaching (FRAP) experiments confirmed that sp. strain UTEX B3054 carries out cell-to-cell communication in multicellular morphotypes but at slower time scales than filamentous cyanobacteria. Although traditionally classified as unicellular, our results suggest that displays facultative multicellularity, a condition that may have conferred ecological advantages for thriving as an extremophile for more than 1.6 billion years. are among the few prokaryotes that evolved multicellularity. The early emergence of multicellularity in (2.5 billion years ago) entails that some unicellular cyanobacteria reverted from multicellular ancestors. We tested this evolutionary hypothesis by studying the unicellular strain sp. UTEX B3054 using flow cytometry, genomics, and cell-to-cell communication experiments. We demonstrate the existence of a well-defined patterned organization of cells in clusters during growth, which might change triggered by environmental stimuli. Moreover, we found genomic signatures of multicellularity in the genome, giving new insights into the evolutionary history of a cyanobacterial lineage that has thrived in extreme environments since the early Earth. The potential benefits in terms of resource acquisition and the ecological relevance of this transient behavior are discussed.