Nitrogen source and pCO₂ synergistically affect carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle

Abstract

Coccolithophores are unicellular phytoplankton that produce calcium carbonate coccoliths as an exoskeleton. Emiliania huxleyi, the most abundant coccolithophore in the world's ocean, plays a major role in the global carbon cycle by regulating the exchange of CO 2 across the ocean-atmosphere interface through photosynthesis and calcium carbonate precipitation. As CO 2 concentration is rising in the atmosphere, the ocean is acidifying and ammonium (NH 4 + ) concentration of future ocean water is expected to rise. The latter is attributed to increasing anthropogenic nitrogen (N) deposition, increasing rates of cyanobacterial N 2 fixation due to warmer and more stratified oceans, and decreased rates of nitrification due to ocean acidification. Thus, future global climate change will cause oceanic phytoplankton to experience changes in multiple environmental parameters including CO 2 , pH, temperature and nitrogen source. This study reports on the combined effect of elevated pCO 2 and increased NH 4 + to nitrate (NO 3 À ) ratio (NH 4on E. huxleyi, maintained in continuous cultures for more than 200 generations under two pCO 2 levels and two different N sources. Herein, we show that NH 4 + assimilation under N-replete conditions depresses calcification at both low and high pCO 2 , alters coccolith morphology, and increases primary production. We observed that N source and pCO 2 synergistically drive growth rates, cell size, and the ratio of inorganic to organic carbon. These responses to N source suggest that, compared to increasing CO 2 alone, a greater disruption of the organic carbon pump could be expected in response to the combined effect of increased NH 4 + /NO 3 À ratio and CO 2 level in the future acidified ocean. Additional experiments conducted under lower nutrient conditions are needed prior to extrapolating our findings to the global oceans. Nonetheless, our results emphasize the need to assess combined effects of multiple environmental parameters on phytoplankton biology to develop accurate predictions of phytoplankton responses to ocean acidification.

Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and p CO 2

“…Unfortunately, these studies are difficult and time consuming to conduct, but they yield critical information to correctly predict additive or synergistic effects of elevated pCO 2 and other changing parameters that will characterize the future oceans. Elevating pCO 2 concentration and shifting nitrogen source have a synergistic effect on calcification [24], and here we indicate that the responses of E. huxleyi to elevated pCO 2 might be offset by simultaneously increasing temperature. Responses of E. huxleyi to simultaneous shifts in multiple environmental parameters add to the complexity of understanding how coccolithophores will respond to the future ocean and the subsequent feedback to the global carbon cycle.…”

“…Allowing for multiple days to pass between sampling for physiological parameters ensured that the population of cells had been replaced completely between collection points, given the high growth rate in our chemostats of 1.1 d 21 (more than one division per day). This sampling strategy is routinely used for continuous culture experiments, as cells several generations apart represent independent samples of the same population [13,24,31,36].…”

“…While there have been tests of E. huxleyi responses to multiple variables [14,[21][22][23], only one study has tested the effect of multiple environmental factors in long-term experiments [24] and found a synergistic effect of pCO 2 and nitrogen source on carbon partitioning in E. huxleyi.…”

Effects of CO2 and their modulation by light in the life‐cycle stages of the coccolithophore Emiliania huxleyi

“…Increased [CO 2 ] might directly benefit biomass production either by enhancing the carboxylation reaction at RubisCO (Raven et al 2005), by reducing CO 2 leakage (Rost et al 2006), or by allowing a down-regulation of activity of the energyintensive carbon concentrating mechanism (CCM; Kranz et al 2010). It has also been indicated that responses to OA are often modulated by light intensities (Kranz et al 2010; Lefebvre et al 2010). Investigating the underlying processes as well as the modulating effects of energy availability will therefore improve the understanding of the origins of measured responses.…”

“…An increased proton (H + ) concentration may impair transport processes, such as the uptake of inorganic carbon (C i ) or calcium ions (Ca 2+ ), being dependent on electrochemical membrane potentials (Mackinder et al 2010;Taylor et al 2011). Increased [CO 2 ] might directly benefit biomass production either by enhancing the carboxylation reaction at RubisCO (Raven et al 2005), by reducing CO 2 leakage (Rost et al 2006), or by allowing a down-regulation of activity of the energyintensive carbon concentrating mechanism (CCM; Kranz et al 2010).…”