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

Abstract

Symbiotic N2-fixing microorganisms have a crucial role in the assimilation of nitrogen by eukaryotes in nitrogen-limited environments1–3. Particularly among land plants, N2-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 sea5. Here we describe an N2-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 N2-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 N2-fixing microorganisms might have aided the colonization of nitrogen-poor soils by early land plants6, 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 ecosystems7.

The Diversity and Functional Capacity of Microbes Associated with Coastal Macrophytes

“…Blades of kelp and surfgrass were a locus of microbial diversity and function, a finding that is similar to many recent studies of macroalgal and seagrass microbiomes reporting high microbial diversity ( 6 , 8 , 9 , 51 – 53 ). The functional attributes of microbial taxa associated with marine macrophytes include pathogen resistance ( 54 ), the ability to provision the host with B vitamins ( 11 ), and enhanced host algal fitness ( 55 ), perhaps through some of the nitrogen or sulfur metabolisms we documented here ( 5 , 13 ).…”

“…These microbial associations are nearly ubiquitous, spanning a diversity of hosts across ecosystems. In coastal marine environments, marine angiosperms and macroalgae show high productivity ( 2 ), are a critical component of the carbon ( 3 ) and nitrogen cycles ( 4 , 5 ), and host a wide range of microbial organisms. Different macroalgal species ( 6 , 7 ) and their different tissues ( 8 , 9 ) host distinct microbial communities which number in the millions per cm 2 of host tissue ( 10 ).…”

“…Yet, bacteria can supply B vitamins ( 11 ) and affect the development of their seaweed hosts ( 12 ). Seagrasses have been shown to have microbial associates that help the host access inorganic nitrogen, including bacteria that can ammonify ( 13 ) and bacteria that can fix atmospheric nitrogen ( 5 ). Though many seaweeds and seagrasses are foundational species in the coastal ocean, our understanding of the diversity and roles of their associated microbes is nascent, even as we discover that environmental change affects these communities ( 14 ).…”

Sand supplementation favors tropical seagrass Thalassia hemprichii in eutrophic bay: implications for seagrass restoration and management

“…Seagrasses are marine ecosystem engineers that provide important ecological services including nutrient uptake, carbon sequestration, food and habitat for marine animals, and shoreline and sediment stabilization [1][2][3]. However, global climate change and sustained pressures from coastal development, including dredging and eutrophication (nutrient enrichment), have weakened the capacity of seagrass meadows to support coastal productivity [4,5].…”

Microbiota-mediated nitrogen fixation and homeostasis in aerial root-mucilage

“…This is consistent with previous observations in seagrass. The nitrogen-fixing symbionts live within the seagrass root tissue, where it supplies amino acids and ammonia to the host in exchange for sugars (Mohr et al, 2021).…”