Uncovering the Unusual Long Chains of Vegetative Cells within Single Colonies of the Dryland Nitrogen-Fixing Cyanobacterium Nostoc flagelliforme

Heterocyst-forming cyanobacteria that colonize the drylands contribute to carbon and nitrogen supplies in nutrient-poor soils. As one of the representative cyanobacteria, Nostoc flagelliforme adapts well to the arid environment in the form of filamentous colonies (or filaments). To date, the adaptive changes, either genetic or micromorphological, that occur within single colonies of dryland cyanobacteria remain largely unclear. In this study, unusual long chains or trichomes of vegetative cells (not containing heterocysts) were observed within N. flagelliforme filaments. And the overall heterocyst frequency in the trichomes was counted to be 1.3–2.7%, different from the usually observed 5–10% heterocyst frequency in model Nostoc strains when grown in nitrogen-deprived medium. Thus, these phenomena seem contradictory to our usual recognition of Nostoc strains. Related transcriptional and heterocyst frequency analyses suggested no genetically significant alteration in heterocyst formation and nitrogen fixation in this strain. Also, the amounts of nitrogen sources in the extracellular polysaccharide (EPS) matrix released by N. flagelliforme cells that may cause the low heterocyst frequency were assessed to be equivalent to 0.28–1.10 mM NaNO3. When combining these findings with the habitat characters, it can be envisaged that the released nitrogen sources from cells are confined, accumulated, and re-utilized in the EPS matrix, thereby leading to the formation of reduced heterocyst frequency and long-chained vegetative cells. This study will contribute to our understanding of the distinctive adaptation properties of colonial cyanobacteria in dryland areas.