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Biological N2 fixation is an important nitrogen source for surface ocean microbial communities. However, nearly all information on the diversity and gene expression of organisms responsible for oceanic N2 fixation in the environment has come from targeted approaches that assay only a small number of genes and organisms. Using genomes of diazotrophic cyanobacteria to extract reads from extensive meta-genomic and -transcriptomic libraries, we examined diazotroph diversity and gene expression from the Amazon River plume, an area characterized by salinity and nutrient gradients. Diazotroph genome and transcript sequences were most abundant in the transitional waters compared with lower salinity or oceanic water masses. We were able to distinguish two genetically divergent phylotypes within the Hemiaulus-associated Richelia sequences, which were the most abundant diazotroph sequences in the data set. Photosystem (PS)-II transcripts in Richelia populations were much less abundant than those in Trichodesmium, and transcripts from several Richelia PS-II genes were absent, indicating a prominent role for cyclic electron transport in Richelia. In addition, there were several abundant regulatory transcripts, including one that targets a gene involved in PS-I cyclic electron transport in Richelia. High sequence coverage of the Richelia transcripts, as well as those from Trichodesmium populations, allowed us to identify expressed regions of the genomes that had been overlooked by genome annotations. High-coverage genomic and transcription analysis enabled the characterization of distinct phylotypes within diazotrophic populations, revealed a distinction in a core process between dominant populations and provided evidence for a prominent role for noncoding RNAs in microbial communities.

Diatoms with symbiotic N₂-fixing cyanobacteria are often abundant in the oligotrophic open ocean gyres. The most abundant cyanobacterial symbionts form heterocysts (specialized cells for N₂ fixation) and provide nitrogen (N) to their hosts, but their morphology, cellular locations and abundances differ depending on the host. Here we show that the location of the symbiont and its dependency on the host are linked to the evolution of the symbiont genome. The genome of Richelia (found inside the siliceous frustule of Hemiaulus) is reduced and lacks ammonium transporters, nitrate/nitrite reductases and glutamine:2-oxoglutarate aminotransferase. In contrast, the genome of the closely related Calothrix (found outside the frustule of Chaetoceros) is more similar to those of free-living heterocyst-forming cyanobacteria. The genome of Richelia is an example of metabolic streamlining that has implications for the evolution of N₂-fixing symbiosis and potentially for manipulating plant-cyanobacterial interactions.