The North Atlantic spring bloom is one of the largest annual biological events in the ocean, and is characterized by dominance transitions from siliceous (diatoms) to calcareous (coccolithophores) algal groups. To study the effects of future global change on these phytoplankton and the biogeochemical cycles they mediate, a shipboard continuous culture experiment (Ecostat) was conducted in June 2005 during this transition period. Four treatments were examined: (1) 12°C and 390 ppm CO 2 (ambient control), (2) 12°C and 690 ppm CO 2 (high pCO 2 ), (3) 16°C and 390 ppm CO 2 (high temperature), and (4) 16°C and 690 ppm CO 2 ('greenhouse'). Nutrient availability in all treatments was designed to reproduce the low silicate conditions typical of this late stage of the bloom. Both elevated pCO 2 and temperature resulted in changes in phytoplankton community structure. Increased temperature promoted whole community photosynthesis and particulate organic carbon (POC) production rates per unit chlorophyll a. Despite much higher coccolithophore abundance in the greenhouse treatment, particulate inorganic carbon production (calcification) was significantly decreased by the combination of increased pCO 2 and temperature. Our experiments suggest that future trends during the bloom could include greatly reduced export of calcium carbonate relative to POC, thus providing a potential negative feedback to atmospheric CO 2 concentration. Other trends with potential climate feedback effects include decreased community biogenic silica to POC ratios at higher temperature. These shipboard experiments suggest the need to examine whether future pCO 2 and temperature increases on longer decadal timescales will similarly alter the biological and biogeochemical dynamics of the North Atlantic spring bloom.
The elemental stoichiometry of microalgae reflects their underlying macromolecular composition and influences competitive interactions among species and their role in the food web and biogeochemistry. Here we provide a new estimate of the macromolecular composition of microalgae using a hierarchical Bayesian analysis of data compiled from the literature. The median macromolecular composition of nutrient-sufficient exponentially growing microalgae is 32.2% protein, 17.3% lipid, 15.0% carbohydrate, 17.3% ash, 5.7% RNA, 1.1% chlorophyll-a and 1.0% DNA as percent dry weight. Our analysis identifies significant phylogenetic differences in macromolecular composition undetected by previous studies due to small sample sizes and the large inherent variability in macromolecular pools. The phylogenetic differences in macromolecular composition lead to variations in carbon-to-nitrogen ratios that are consistent with independent observations. These phylogenetic differences in macromolecular and elemental composition reflect adaptations in cellular architecture and biochemistry; specifically in the cell wall, the light harvesting apparatus, and storage pools.
Biogeochemical cycles in the ocean are strongly affected by the elemental stoichiometry (C:N:P) of phytoplankton, which largely reflects their macromolecular content. A greater understanding of how this macromolecular content varies among phytoplankton taxa and with resource limitation may strengthen physiological and biogeochemical modeling efforts. We determined the macromolecular basis (protein, carbohydrate, lipid, nucleic acids, pigments) of C:N:P in diatoms and prasinophytes, two globally important phytoplankton taxa, in response to N starvation. Despite their differing cell sizes and evolutionary histories, the relative decline in protein during N starvation was similar in all four species studied and largely determined variations in N content. The accumulation of carbohydrate and lipid dominated the increase in C content and C:N in all species during N starvation, but these processes differed greatly between diatoms and prasinophytes. Diatoms displayed far greater accumulation of carbohydrate with N starvation, possibly due to their greater cell size and storage capacity, resulting in larger increases in C content and C:N. In contrast, the prasinophytes had smaller increases in C and C:N that were largely driven by lipid accumulation. Variation in C:P and N:P was species-specific and mainly determined by residual P pools, which likely represent intracellular storage of inorganic P and accounted for the majority of cellular P in all species throughout N starvation. Our findings indicate that carbohydrate and lipid accumulation may play a key role in determining the environmental and taxonomic variability in phytoplankton C:N. This quantitative assessment of macromolecular and elemental content spanning several marine phytoplankton species can be used to develop physiological models for ecological and biogeochemical applications.
Increased atmospheric p CO 2 is expected to render future oceans warmer and more acidic than they are at present. Calcifying organisms such as coccolithophores that fix and export carbon into the deep sea provide feedbacks to increasing atmospheric p CO 2 . Acclimation experiments suggest negative effects of warming and acidification on coccolithophore calcification, but the ability of these organisms to adapt to future environmental conditions is not well understood. Here, we tested the combined effect of p CO 2 and temperature on the coccolithophore Emiliania huxleyi over more than 700 generations. Cells increased inorganic carbon content and calcification rate under warm and acidified conditions compared with ambient conditions, whereas organic carbon content and primary production did not show any change. In contrast to findings from short-term experiments, our results suggest that long-term acclimation or adaptation could change, or even reverse, negative calcification responses in E. huxleyi and its feedback to the global carbon cycle. Genome-wide profiles of gene expression using RNA-seq revealed that genes thought to be essential for calcification are not those that are most strongly differentially expressed under long-term exposure to future ocean conditions. Rather, differentially expressed genes observed here represent new targets to study responses to ocean acidification and warming.
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.
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