Abstract:
Single cells within the filaments of certain multicellular cyanobacteria exchange molecules through cell-cell connections known as junctions (SJs). These SJs consist of cytoplasmic cap and plug modules and a tube module positioned in nanopores, allowing connection through the septal peptidoglycan. SJs display reversible gating and are analogous to metazoan gap junctions, despite predating them by a billion years. Mutants in the fraD and sepN genes lack structural components of SJs and are therefore impaired in SJ closure. SJ-mediated cell-cell communication is important for differentiation of nitrogen-fixing heterocysts and metabolite exchange during diazotrophic growth. However, its role in the differentiation of other cell types – such as motile hormogonia and dormant akinetes, remains unexplored. Additionally, the coordination mechanism for hormogonia phototaxis, where filaments rapidly change direction in response to light conditions, is not well understood. The importance of gating for stress survival and heterocyst formation has been speculated but lacked strong evidence.
In this work, by studying the communication-impaired fraI mutant of Nostoc punctiforme, we show that, despite highly impaired cell-to-cell communication the differentiation of hormogonia and akinetes is still possible, unlike heterocyst differentiation. The heavily fragmenting fraI mutant filaments showed altered hormogonia formation with significantly reduced motility. However, the loss of SJ-mediated cell-to-cell communication did not affect hormogonia phototaxy, suggesting the need for an alternative hypothesis for the high degree of synchronization among the hormogonia cells.
By studying the gating-impaired fraD and sepN— we showed that the closure of SJs is important for whole-filament survival under stress conditions such as UV-C light treatment, where many individual cells undergo cell death. However, SJ gating was not necessary for heterocyst differentiation. Instead, we suggest the idea that peptidoglycan remodelling is crucial in the heterocyst differentiation process.
This work contributed to the understanding of the mode of action, the function under stress conditions and cell differentiation of SJs, and added new insights in the SJ architecture.