Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles

Abstract

Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens, and coccolithophore, Emiliania huxleyi. We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth, whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions.

Complementary environmental analysis and functional characterization of a plastid diatom lower glycolytic-gluconeogenesis pathway

“…It remains to be determined what roles plastidial glycolysis plays in other habitats where diatoms dominate phytoplankton biomass, e.g. in upwelling cycles where diatoms may preciously upregulate components of their core metabolism to rapidly avail of optimal light and nutrient conditions (119, 122)…”

Variability in the phytoplankton response to upwelling across an iron limitation mosaic within the California Current System

“…Upwelling-simulation studies conducted in the laboratory have recently showed an increase in the relative expression of nitrogen assimilation genes in the dark (simulated sinking out of the euphotic zone) in the diatom Chaetoceros decipiens , while the coccolithophore, Emiliania huxleyi showed a relatively lower expression of the same genes in the dark, further supporting the diatom “frontloading” hypothesis for N assimilation [Lampe et al 2021]. Ultimately, diatoms can ensure a more rapid physiological response to upwelling compared to other phytoplankton taxa.…”

“…In essence, upwelled diatoms employ a proactive approach and maintain elevated pools of these nitrogen-related genes throughout the upwelling conveyor belt cycle, whereas other phytoplankton employ a more reactive approach and upregulate primary nitrate assimilation genes post-upwelling. This distinctive molecular strategy to constitutively express nitrogen assimilation genes is believed to provide these diatom taxa with a physiological edge in their "shift-up" response to upwelling [Lampe et al 2021].…”

“…During this stage, the aging waters may be increasingly nitrate limited, and cells increase their C:N ratios above that of the Redfield ratio (6.6:1) as they sink below the euphotic zone. Once at depth (low light, high nutrients), diatoms are set apart by the differential expression of nitrogen transporters and other nitrogen assimilation genes compared to other phytoplankton taxa [Lampe et al 2021].…”

“…A conceptual model of the upwelling conveyor belt cycle (UCBC) in upwelling systems and the idealized zones within the upwelling cycle. Image modified from Lampe et al (2021).…”