A grazing-driven positive nutrient feedback loop and active sexual reproduction underpin widespread Noctiluca green tides

Abstract

The mixoplankton green Noctiluca scintillans (gNoctiluca) is known to form extensive green tides in tropical coastal ecosystems prone to eutrophication. In the Arabian Sea, their recent appearance and annual recurrence have upended an ecosystem that was once exclusively dominated by diatoms. Despite evidence of strong links to eutrophication, hypoxia and warming, the mechanisms underlying outbreaks of this mixoplanktonic dinoflagellate remain uncertain. Here we have used eco-physiological measurements and transcriptomic profiling to ascribe gNoctiluca’s explosive growth during bloom formation to the form of sexual reproduction that produces numerous gametes. Rapid growth of gNoctiluca coincided with active ammonium and phosphate release from gNoctiluca cells, which exhibited high transcriptional activity of phagocytosis and metabolism generating ammonium. This grazing-driven nutrient flow ostensibly promotes the growth of phytoplankton as prey and offers positive support successively for bloom formation and maintenance. We also provide the first evidence that the host gNoctiluca cell could be manipulating growth of its endosymbiont population in order to exploit their photosynthetic products and meet critical energy needs. These findings illuminate gNoctiluca’s little known nutritional and reproductive strategies that facilitate its ability to form intense and expansive gNoctiluca blooms to the detriment of regional water, food and the socio-economic security in several tropical countries.

Interactions between Noctiluca scintillans and Three Co-Occurring Microalgae in Response to Varying Nutrient Levels

“…However, during N. scintillans red tide, the nitrogen and phosphorus emissions from N. scintillans can potentially meet or even surpass the demands of the phytoplankton [23]. For example, Luo et al [29] conducted an in situ investigation at Seeb Jetty in the Oman Sea, which revealed a significant positive correlation (p < 0.001) between the nutrient concentration in the water and the abundance of green N. scintillans, suggesting that the feeding process served as the primary mechanism for N. scintillans to accumulate substantial quantities of nutrients. The findings of this study indicated that N. scintillans, when in a fed state, released nitrogen into the water, while no release of phosphorus was observed (Table 1).…”

“…The culture was incubated at 20 • C, following a light-dark cycle of 14:10 h, and it had a photon flux of 100 µmol m −2 s −1 . Additionally, Tetraselmis subcordiformis (Wille) Butcher was used as the prey [28,29]. To minimize the influence of the prey residues in vivo and externally on the experiments, N. scintillans were starved for 48 h and then washed 2~3 times through a 100 µm mesh using sterilized seawater before the formal experiments.…”

In Situ Molecular Ecological Analyses Illuminate Distinct Factors Regulating Formation and Demise of a Harmful Dinoflagellate Bloom

“…Metatranscriptomic studies have successfully tracked cellular processes associated with life history transitions, nutrient acquisition, defense, and energy production during dinoflagellate blooms by community gene expression analyses ( 23 – 30 ). Previous data also suggested that sexual reproduction (meiosis) could contribute to bloom formation for dinoflagellate blooms ( 25 , 31 ). How grazing by zooplankton and attacks by microbes influence the bloom dynamics were not addressed in those studies.…”

Isolation and characterization of a high-efficiency algicidal bacterium Pseudoalteromonas sp. LD-B6 against the harmful dinoflagellate Noctiluca scintillans

“…Briefly, N. scintillans single cell was isolated with a large-diameter pipette based on the morphology and maintained in sterilized seawater (salinity of 30‰), which was prepared by filtration (0.22 μm filter) and autoclaving of in situ seawater. The culture was incubated at 20°C under light (100 μE m –2 s –1 , 14: 10 h light–dark cycle) and with Tetraselmis subcordiformis as the prey ( Wu et al, 1994 ; Luo et al, 2022 ).…”