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

Abstract

Multicellularity in Cyanobacteria 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 Gloeocapsopsis 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 Gloeocapsopsis 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 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 among 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. 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 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 the ecological relevance of this transient behavior are discussed.

Two novel heteropolymer‐forming proteins maintain the multicellular shape of the cyanobacterium Anabaena sp. PCC 7120

“…(C) The presence of homologs of ZicK/ZacK in cyanobacteria main types (total number of genomes in the analysis is shown in the legend). Note that the presence of ZicK/ZacK homologs in baeocystous cyanobacteria is in accordance with a recent suggestion of a multicellular ancestry of species in that group [96]. (D) Genomic neighbourhood of ZicK/ZacK in cyanobacterial genomes.…”

The order of trait emergence in the evolution of cyanobacterial multicellularity

“…Notably, baeocyte-forming cyanobacteria, that have been traditionally grouped together with unicellular cyanobacteria (Rippka et al 1979), appear to immediately predate the evolution of spore-like AKINETES and nitrogen-fixing HETEROCYSTS and thus emerge much later than filamentous forms. Indeed, a recent study suggested that Gloeocapsopsis sp., a baeocytous cyanobacterium, harbors several characteristics that are in common with filamentous cyanobacteria, including mechanisms of cell-cell communication (Urrejola et al 2020).…”

Use of a Thermophile Desiccation-Tolerant Cyanobacterial Culture and Os Redox Polymer for the Preparation of Photocurrent Producing Anodes

“…UTEXB3054 is a unicellular cyanobacterium originally isolated from Atacama, the driest warm desert on Earth, with an impressive ability to tolerate desiccation periods based on unique genetic features associated to desiccation tolerance (Urrejola et al, 2019). Because of these properties, its genome and sugar biosynthesis pathways have been studied (Urrejola et al, 2019(Urrejola et al, , 2020. In this work, for the first time, we explored the use of Gloeocapsopsis sp.…”