Metagenome-amplified genome (MAG) covariation uncovers the genome of the algal host of the marine nitrogen-fixing cyanobacterium UCYN-A

The uncultivated unicellular cyanobacterium UCYN-A is a key nitrogen fixer in the open ocean. Unveiling the symbiotic lifestyle of UCYN-A was crucial for understanding the unusual streamlining of its metabolic capacities. However, still little is known about the metabolic potential of its prymnesiophyte host, a single-celled alga for which there is no genetic information available. Here, we identify the partial genome of the prymnesiophyte host of UCYN-A among nearly 1,000 non-redundant metagenome-amplified genomes (MAGs) reconstructed from a subset of the TARA Oceans metagenomic dataset. Only one of these MAGs showed highly significant covariation with the abundance of the UCYN-A1 genome across 63 globally distributed open ocean stations, suggesting that UCYN-A1 is hosted by a single prymnesiophyte genomic lineage (A1-Host). Moreover, the genome comparison of the A1-Host MAG with several A1-Host single-amplified genomes (SAGs) obtained from the North Pacific Ocean (Station ALOHA) points to a low genetic divergence among geographically distant A1-Host populations, as previously shown for its UCYN-A1 symbiotic partner. Finally, based on metatranscriptomic analysis, we observed that a high affinity ammonium transporter (amt) gene was among the highest transcribed genes during the morning hours, suggesting that the timing of amt transcription may be coordinated with UCYN-A1 nitrogen fixation for effective transfer of ammonium from UCYN-A1. These results provide new insights into the metabolic coupling between UCYN-A and its host, a symbiotic system key in the carbon and nitrogen marine cycles that remains elusive to cultivation.