Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Abstract

Summary Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume‐specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2‐concentrating mechanisms (CCMs). Previous studies have focused on among‐species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3‐fold difference in cell volume. We compared CO2 affinity, external carbonic anhydrase (CAext), isotopic signatures (δ13C) and growth among size‐selected lineages. Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13C. Larger cells also achieved faster growth and higher maximum biovolume densities. We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

Temporal declines in Wadden Sea phytoplankton cell volumes observed within and across species

“…Many monitoring series use standard (literature or once measured) values per species, which not only precludes observing the intraspecific shifts in cell size we found here: Cell volumes are used to transfer abundances into carbon estimates (Montagnes et al 1994; Menden‐Deuer and Lessard 2000), which then are fed into carbon budgets. Moreover, carbon fixation per cell allometrically scales to cell size, whereas C‐specific carbon fixation shows a nonlinear pattern (Taguchi 1976; Marañón et al 2007; Malerba et al 2021). Not accounting for temporal shifts in cell size might thus lead to highly biased estimates for phytoplankton biomass and performance.…”

“…Larger cells have higher cell‐specific but lower volume‐specific affinity to both nitrogen and phosphorus and exhibit lower maximum growth rates (Edwards et al 2012). Also, light affinity and carbon assimilation depend on cell size (Edwards et al 2015; Malerba et al 2021). At the same time, size is decisive in constraining vulnerability to grazing (Kiørboe 1993; Irigoien et al 2005; Branco et al 2020), nutrient storage capacity (Grover 1991; Litchman et al 2009; Kerimoglu et al 2012), or mobility (Sommer 1988).…”

Cell size as driver and sentinel of phytoplankton community structure and functioning

“…The same relationship is potentially true within species, as Malerba et al. (2021) experimentally evolved a nearly 10‐fold size difference in the marine green algae Dunaiella tertiolecta , finding size scaling for CO 2 affinity, external carbonic anhydrase, and maximum carbon fixation (all positive) and half‐saturation constants (negative).…”

“…Whereas the amount of cell‐size‐related information on different species is massive, intraspecific plasticity in cell size and variance in size‐scaling has rarely been addressed except for some specific size‐selection experiments (Malerba et al., 2021). However, intraspecific changes in mean size were major in a long‐term phytoplankton monitoring programme (Hillebrand et al., 2022).…”

Disentangling top-down drivers of mortality underlying diel population dynamics ofProchlorococcusin the North Pacific Subtropical Gyre

“…Highly resolved surface ocean observations suggest that diel light rhythms drive repeatable changes in the abundance of ubiquitous cyanobacteria at the base of the microbial food web, including both Prochlorococcus and Synechococcus [1, 2]. Cyanobacterial population dynamics are influenced by both nutrients and light availability [2, 3, 4, 5, 6, 7, 8] as well as by density- and size-dependent feedback processes with other components of the community [9, 10, 11, 12, 13, 14, 15]. These interactions lead to diel oscillations, including in grazing rates, viral abundances, viral infection rates, and viral activity [16, 17, 18, 19, 20, 21].…”