Genomic and transcriptomic insights into the habitat adaptation of the diazotrophic paddy-field cyanobacterium Nostoc sphaeroides

Nitrogen-fixing cyanobacteria are common in paddy fields, one of the most productive wetland ecosystems. Here, we present the complete genome of Nostoc sphaeroides, a paddy-field diazotroph used for food and medicine for more than 1700 years and deciphered the transcriptional regulation during the developmental transition from hormogonia to vegetative filaments with heterocysts. The genome of N. sphaeroides consists of one circular chromosome (6.48 Mb), one of the largest ever reported megaplasmids (2.34 Mb), and seven plasmids. Multiple gene families involved in the adaption to high solar radiation and water fluctuation conditions were found expanded, while genes involved in anoxic adaptation and phosphonate utilization are located on the megaplasmid, suggesting its indispensable role in environmental adaptation. Distinct gene expression patterns were observed during the light-intensity-regulated transition from hormogonia to vegetative filaments, specifically, genes encoding proteins involved in photosynthetic light reaction, carbon fixation, nitrogen metabolism and heterocyst differentiation were significantly upregulated, whereas genes related to cell motility were down-regulated. Our results provide genomic and transcriptomic insights into the adaptation of a filamentous nitrogen-fixing cyanobacterium to the highly dynamic paddy-field habitat, suggesting N. sphaeroides as an excellent system to understand the transition from aquatic to terrestrial habitats and to support sustainable rice production.