Loss of filamentous multicellularity in Cyanobacteria - the extremophile Gloeocapsopsis sp. UTEX B3054 retained multicellular features at the genomic and behavioral level

Multicellularity in Cyanobacteria played a key role in their habitat expansion contributing to the Great Oxidation Event around 2.45-2.32 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 Gloeocapsopsis lineage emerged. Flow cytometry and microscopy results revealed morphological plasticity, involving patterned formation of multicellular morphotypes sensitive to environmental stimuli. Genomic analyses unveiled the presence of multicellular-associated genes in its genome. Calcein-FRAP experiments confirmed that Gloeocapsopsis sp. UTEXB3054 carry out cell-to-cell communication in multicellular morphotypes, but in slower timescales than filamentous cyanobacteria. Although traditionally classified as unicellular, our results suggest that Gloeocapsopsis displays facultative multicellularity, a condition that may have conferred ecological advantages for thriving as an extremophile for more than 1.6 billion years.Importance Cyanobacteria are amongst the few prokaryotes that evolved multicellularity. The early emergence of multicellularity in Cyanobacteria (2.5 billion years ago) entails that some unicellular cyanobacteria reverted from multicellular ancestors. We tested this evolutionary hypothesis by studying the unicellular strain Gloeocapsopsis sp. UTEXB3054, using flow cytometry, genomics and cell-to-cell communication experiments. We demonstrated 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 Gloeocapsopsis 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 ecological relevance of this transient behavior are discussed.