Symbiont regulation of nitrogen metabolism and excretion in tropical planktonic foraminifera

Abstract

Dissolved inorganic nitrogen (DIN) is one of the key major nutrients crucial for regulating marine productivity. Photosynthetic endosymbiosis, as seen in organisms like stony corals and foraminifera, appear to alleviate nutrient limitations in surface ocean waters through its symbiotic relationship with the host. Recent advancements in understanding the nitrogen isotopic compositions (¹⁵N/¹⁴N) of planktonic foraminifera reveal notably lower ¹⁵N/¹⁴N ratios in species harboring dinoflagellate symbionts compared to those without symbionts or with different types of symbionts. This species differentiation is hypothesized to arise from more efficient internal nitrogen cycling in dinoflagellate-bearing species, resulting in reduced nitrogen loss to the environment and thus diminished trophic enrichment. In our investigation, we monitored nitrogen excretion in incubation experiments involving several planktonic foraminifera species, including dinoflagellate-bearing Globigerinoides ruber, Trilobatus sacculifer, Orbulina universa, and chrysophyte-bearing Globigerinella siphonifera. G. siphonifera exhibited distinct diel cycles of ammonium production at night and uptake during the day, with its trophic enrichment in biomass ¹⁵N/¹⁴N increasing in tandem with ammonium loss. Conversely, no measurable excreted ammonium was detected from any of the three dinoflagellate-bearing species. These findings align with earlier observations indicating a tight interaction wherein hosts likely supply excess non-carbon nutrients to their symbionts via prey ingestion and digestion, in exchange for organic carbon. Our research underscores the pivotal role of symbiosis in shaping nutrient dynamics between planktonic foraminifera and the surrounding environment, with implications for using the species ¹⁵N/¹⁴N difference to reconstruct upper ocean nutrient conditions.