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

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Representative Diatom and Coccolithophore Species Exhibit Divergent Responses Throughout Simulated Upwelling Cycles bioRxiv preprint doi: https://doi.org/10.1101/2020.04.30.071480; this version posted May 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. Representative diatom and coccolithophore species exhibit divergent responses throughout simulated upwelling cycles Robert H. Lampe1,2, Gustavo Hernandez2, Yuan Yu Lin3, and Adrian Marchetti2, 1Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, USA 2Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA Phytoplankton communities in upwelling regions experience a ton blooms following upwelling (2, 5, 6). When upwelling wide range of light and nutrient conditions as a result of up- delivers cells and nutrients into well-lit surface waters, di- welling cycles. These cycles can begin with a bloom at the sur- atoms quickly respond to available nitrate and increase their face followed by cells sinking to depth when nutrients are de- nitrate uptake rates compared to other phytoplankton groups pleted. Cells can then be transported back to the surface with allowing them to bloom (7). This phenomenon may partially upwelled waters to seed another bloom. In spite of the physico- be explained by frontloading nitrate assimilation genes, i.e. chemical extremes associated with these cycles, diatoms consis- high expression before the upwelling event occurs, in addi- tently outcompete other phytoplankton when upwelling events occur. Here we simulated the conditions of a complete upwelling tion to diatom’s unique metabolic integration of nitrogen and cycle with a common diatom, Chaetoceros decipiens, and coccol- carbon metabolic pathways (6, 8). ithophore, Emiliania huxleyi. We show that while both organ- Coupled to rapid nitrate uptake rates, phytoplankton in isms exhibited physiological and transcriptomic plasticity, the natural communities have been observed to dramatically al- diatom displayed a distinct response enabling it to rapidly shift- ter their carbon-to-nitrogen (C:N) ratios (6, 7, 9). C:N ratios up growth and nitrate assimilation when returned to light and well above the predicted Redfield value (6.6:1) imply that the nutrients. As observed in natural diatom communities, C. de- cells faced nitrogen limitation as the upwelled waters aged, cipiens frontloads key transcriptional and nitrate assimilation and then the cells sank to depth, but this alteration has yet to genes coordinating its rapid response. Low iron simulations be shown in the context of a complete UCBC cycle and with- showed that C. decipiens is capable of maintaining this response out the influence of other non-phytoplankton detrital material when iron is limiting whereas E. huxleyi could not. Differential expression between iron treatments further revealed molecular which would affect these measurements (6, 7, 9). Ultimately, mechanisms used by each organism under low iron availability. such shifts in cellular elemental quotas associated with sink- Overall, these results highlight the responses of two dominant ing cells can decouple the biogeochemical cycling of these phytoplankton groups to upwelling cycles, providing insight into elements. the mechanisms fueling diatom success during upwelling events The responses of phytoplankton within the UCBC are in current and future oceans. also influenced by the availability of the micronutrient iron. In the California and Peru/Humboldt Upwelling Zones for Correspondence: [email protected] example, iron delivery is primarily dependent on riverine in- put and upwelling-driven resuspension of continental shelf Introduction sediments (10–14). In areas with steep continental shelves, Phytoplankton communities in coastal upwelling regions dis- reduced interaction between upwelled waters and sediment proportionately contribute to global primary production and can result in decreased iron relative to macronutrients result- serve as the base of highly productive food chains (1). Within ing in iron limitation as the phytoplankton bloom develops. these environments, phytoplankton undergo a cycle in which As upwelling is anticipated to intensify from climate change subsurface populations are vertically transported with up- (15), increased upwelled nitrate has the potential to be fur- welled water masses to seed surface blooms and return to ther unmatched by upwelled iron causing an expansion of depth as upwelling subsides and nutrients are depleted (2). iron limitation regions (1). Furthermore, ocean acidification Surviving cells at depth may act as seed stocks when up- may result in reduced iron bioavailability to phytoplankton welling returns, and the cells are once again transported up- (16, 17). wards with nutrient-rich waters. Herein this loop is referred An understanding of phytoplankton responses to the to as the upwelling conveyer belt cycle (UCBC; Fig.1). UCBC remains limited and is primarily based on a relatively The physiological response of phytoplankton to the up- small collection of field studies focused on the shift-up re- welling portion of the UCBC is referred to as the shift-up sponse resulting in no complete view of the cycle (2, 7). response and includes an acceleration of processes such as Importantly, differences in responses among phytoplankton nitrate uptake, assimilation, and growth (3, 4). Based on groups influences both the community structure and biogeo- field observations, diatoms are believed to be particularly chemical cycling in upwelling areas which may be altered suited for shift-up leading to their dominance of phytoplank- by iron limitation (1). Using a combined physiological and Lampe et al. | bioRχiv | May 1, 2020 | 1–11 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.30.071480; this version posted May 1, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. tures were grown in artificial Aquil* medium following trace metal clean (TMC) techniques at 12°C and approximately High Light, Low Nutrients Balanced Growth High Light, High Nutrients -2 -1 (Shift-Down; T6) (T1, T5) (Shift-up; T4) 115 µmol photons m s (23–25). Starting macronutrient concentrations were modified from standard Aquil* such that nitrate rather than silicate would be drawn down and depleted Sinking -1 -1 first by diatoms (50 µmol L NO3, 10 µmol L PO4, 200 -1 µmol L H4SiO4). Aquil was chelexed in a TMC room, mi- Low Light, High Nutrients Upwelling (T2, T3) crowave sterilized, allowed to cool, and then supplemented with filter-sterilized (0.2 µm Acrodisc®) EDTA-trace metals (minus iron) and vitamins (B12, thiamine, and biotin). Trace metals were buffered using 100 µmol L-1 EDTA and added at the concentrations listed in Sunda et al. (25) except Cd which was added at a total concentration of 121 nmol L-1. Premixed Fe-EDTA (1:1) was added separately at a total concentration -1 -1 Fig. 1. Conceptual overview of the upwelling conveyer belt cycle (UCBC) repro- of 1370 nmol L for the high iron treatments or 3.1 nmol L duced from Wilkerson and Dugdale (4) and annotated with experimental time points. for the low iron treatments. The resulting concentrations of iron not complexed to EDTA (Fe’) were estimated as 2730 Table 1. Description of experimental time points. pmol L-1 (high iron) and 6 pmol L-1 (low iron)(25) result- Name Latitude ing in Fe-replete and Fe-limited growth, respectively. Vita- 1 Mid-exponential growth #1 mins were added at f/2 concentrations. Media were allowed 2 Stationary Phase #1 to equilibrate overnight before use. (4 d in stationary phase, 1 d in dark) Cultures were acclimated to medium using the semi- 3 Stationary Phase #2 continuous batch culture technique at the two iron concentra- (13 d in stationary phase, 10 d in dark) tions in acid-cleaned 28 mL polycarbonate centrifuge tubes 4 12 hours after returning to light and nutrients with stable growth rates (26). Cultures were then grown in a 5 Mid-exponential growth #2 1 L polycarbonate bottle, and when in exponential phase, 5 6 Stationary Phase #3 mL (high iron) or 20 mL (low iron) of each culture were then (2 days in stationary phase, light) transferred to triplicate clean 2 L polycarbonate bottles fitted with Teflon tubing for subsampling and bubbling. Seawater was gently stirred and continuously bubbled with air passed transcriptomic approach, we examine the responses of phy- through 1.2 mol L-1 HCl then TMC Milli-Q before the culture toplankton throughout the various light and nutrient condi- bottle. Cultures were not axenic although sterile techniques tions associated with the UCBC via culture-based simula- were used for all culture work to minimize contamination. tions. Samples were collected with higher resolution sur- rounding the upwelling portion of the UCBC to evaluate the The upwelling conveyer belt cycle (UCBC) was simu- ability to exhibit a shift-up respone. In order to compare lated by growing or transitioning the cultures to varying light two phytoplankton lineages commonly present in upwelled and nutrient conditions (Fig. 1, Table 1). First, to simu- waters, a representative diatom, Chaetoceros decipiens, and late bloom and termination phases, cultures were grown in coccolithophore, Emiliania huxleyi, were used; both
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