Thermal Performance Curves of Functional Traits Aid Understanding of Thermally Induced Changes in Diatom-Mediated Biogeochemical Fluxes

Abstract

How the functional traits (FTs) of phytoplankton change with temperature is important for understanding the impacts of ocean warming on phytoplankton mediated biogeochemical fluxes. This study quantifies the thermal performance curves (TPCs) of FTs in the cosmopolitan model diatom, Thalassiosira pseudonana, to advance understanding of trade-offs between physiological (photoacclimation, carbon fixation, nitrate, phosphate, and silicate uptake) and morphological traits (cell volume and frustule silicification). We show that each FT has substantial phenotypic plasticity and exhibits a unique TPC, varying in both shape and thermal optimum, and diverging from the growth response. The TPC for growth was symmetric with a thermal optimum (T opt ) of 18 • C. In comparison, the TPC for primary productivity was warm-skewed with a T opt around 21 • C, whereas frustule silicification decreased linearly with increasing temperature. Together, this suggests that the optimal temperature for overall fitness is a balance of trade-offs in the underlying functional traits. Moreover, these results demonstrate that growth is not necessarily an accurate estimate of overall biogeochemical performance and that temperature change will likely influence elemental fluxes such as carbon and silicon. Finally, we show that temperature-driven changes in individual traits e.g., photoacclimation, can mimic responses experienced under other environmental stressors (high light) and so a multi-trait assessment is essential for accurate interpretation of the cellular impact of warming. This study also reveals that multi-trait analysis, in the context of TPCs, provides insight into the cellular physiology regulating the whole cell response and has the potential to provide better estimates of how diatom-mediated biogeochemical fluxes are likely to be impacted in the context of ocean warming. Analyzing the response of multiple traits more comprehensively over other environmental gradients may therefore provide a useful framework to advance understanding of how taxon-specific functional traits will respond to multifaceted ocean change.

Temperature–nutrient interactions exacerbate sensitivity to warming in phytoplankton

“…A previous study (Baker et al, 2016) has found that nutrient uptake rates are highest at intermediate temperatures. A previous study (Baker et al, 2016) has found that nutrient uptake rates are highest at intermediate temperatures.…”

Thermal niche evolution of functional traits in a tropical marine phototroph

“…(), respectively, as described in Baker et al. (). Net flux was calculated as the difference between nutrient concentrations normalized to cell abundance at the start and end of the exponential phase.…”

“…The supernatant was discarded and cell pellets stored frozen at −80°C until extraction and later analysis as previously described in Baker et al. (). Samples were extracted in 3 mL volume of 3:2 90% acetone: 100% dimethyl sulfoxide extraction reagent in the dark at 4°C for 15 min (Shoaf and Lium ).…”

Rapid thermal adaptation in a marine diatom reveals constraints and trade‐offs

“…The thermal reaction norm for population growth depends on the temperature dependences of enzyme activities (Corkrey et al, 2014;Ratkowsky, Olley, & Ross, 2005), and few processes or pathways within the cell should be immune to the effects of directional temperature selection (Baker et al, 2016;Nedwell, 1999;Padfield et al, 2015;Schaum et al, 2017). Depending on the genes affected, changes in growth rate may be accompanied by changes in traits not directly associated with the thermal reaction norm.…”

“…Depending on the genes affected, changes in growth rate may be accompanied by changes in traits not directly associated with the thermal reaction norm. For example, stoichiometry may respond to thermal adaptation due to changes in relative resource requirements of phytoplankton cells, which in turn may affect species' competitive abilities (e.g., for N and P) and ultimately global biogeochemical cycles (Baker et al, 2016;Litchman, Klausmeier, Schofield, & Falkowski, 2007;Redfield, 1958). An increase in maximum growth rate at the selection temperature may lead to a decrease in affinity for a given nutrient due to a trade-off between allocation of cellular resources to reproduction versus nutrient uptake (Grover, 1991;Klausmeier, Litchman, Daufresne, & Levin, 2004).…”