Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium

Symbiotic N-2-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments(1-3). Particularly among land plants, N-2-fixing symbionts occur in a variety of distantly related plant lineages and often involve an intimate association between host and symbiont2,4. Descriptions of such intimate symbioses are lacking for seagrasses, which evolved around 100 million years ago from terrestrial flowering plants that migrated back to the sea(5). Here we describe an N-2-fixing symbiont, 'Candidatus Celerinatantimonas neptuna', that lives inside seagrass root tissue, where it provides ammonia and amino acids to its host in exchange for sugars. As such, this symbiosis is reminiscent of terrestrial N-2-fixing plant symbioses. The symbiosis between Ca. C. neptuna and its host Posidonia oceanica enables highly productive seagrass meadows to thrive in the nitrogen-limited Mediterranean Sea. Relatives of Ca. C. neptuna occur worldwide in coastal ecosystems, in which they may form similar symbioses with other seagrasses and saltmarsh plants. Just like N-2-fixing microorganisms might have aided the colonization of nitrogen-poor soils by early land plants(6), the ancestors of Ca. C. neptuna and its relatives probably enabled flowering plants to invade nitrogen-poor marine habitats, where they formed extremely efficient blue carbon ecosystems(7).

Automated summary

Symbiotic N-2-fixing microorganisms play a crucial role in nitrogen assimilation by eukaryotes in nitrogen-limited environments. The symbiotic relationship between 'Candidatus Celerinatantimonas neptuna' and its host Posidonia oceanica allows highly productive seagrass meadows to thrive in the Mediterranean Sea. This symbiosis is similar to that of terrestrial N-2-fixing plant symbioses and may have enabled flowering plants to thrive in nitrogen-poor marine habitats.