Evidence for changes in carbon isotopic fractionation by phytoplankton between 1960 and 2010

Rising CO₂ is expected to drive a myriad of environmental changes in the surface ocean. Deciphering the phytoplankton response to this complex change is difficult. Here we determine whether a trend in the biological fractionation of stable carbon isotopes (ε_p) has occurred over the past 50 years. ε_p is primarily controlled by the acquistion and intracellular transport of inorganic carbon and the rate of carbon fixation. In turn, these processes are sensitive to phytoplankton physiology, community composition, and, notably, inorganic carbon availability. ε_p may therefore carry a signal of biological response to climate change. Temporal and spatial records of ε_p can be deciphered from the difference between the stable carbon isotopic composition of particulate organic matter (δ¹³C_POC) and that of the ambient inorganic carbon pool (δ¹³C_CO2). Here we establish a global record of ε_p extending from the 1960s to today, extracted from a newly compiled dataset of global measured δ¹³C_POC and part measured/part climatology δ¹³C_CO2. We find that ε_p has changed significantly since the 1960s in the low- to mid-latitude surface ocean. The increase is most pronounced in the subtropics, where it is is estimated at > 0.015 ‰ per year. Our findings of such rates of change are further supported by a high resolution temporal record from a single sediment trap near Bermuda. Our results are consistent with the idea that ε_p is affected by increased inorganic carbon availability driven by the rise in atmospheric CO₂.

Long-term trends in calcifying plankton and pH in the North Sea

Relationships between six calcifying plankton groups and pH are explored in a highly biologically productive and data-rich area of the central North Sea using time-series datasets. The long-term trends show that abundances of foraminiferans, coccolithophores, and echinoderm larvae have risen over the last few decades while the abundances of bivalves and pteropods have declined. Despite good coverage of pH data for the study area there is uncertainty over the quality of this historical dataset; pH appears to have been declining since the mid 1990s but there was no statistical connection between the abundance of the calcifying plankton and the pH trends. If there are any effects of pH on calcifying plankton in the North Sea they appear to be masked by the combined effects of other climatic (e.g. temperature), chemical (nutrient concentrations) and biotic (predation) drivers. Certain calcified plankton have proliferated in the central North Sea, and are tolerant of changes in pH that have occurred since the 1950s but bivalve larvae and pteropods have declined. An improved monitoring programme is required as ocean acidification may be occurring at a rate that will exceed the environmental niches of numerous planktonic taxa, testing their capacities for acclimation and genetic adaptation.

Sensitivity of Antarctic phytoplankton species to ocean acidification: growth, carbon acquisition, and species interaction

Despite the fact that ocean acidification is considered to be especially pronounced in the Southern Ocean, little is known about CO₂-dependent physiological processes and the interactions of Antarctic phytoplankton key species. We therefore studied the effects of CO₂ partial pressure (P_CO2) (16.2, 39.5, and 101.3 Pa) on growth and photosynthetic carbon acquisition in the bloom-forming species Chaetoceros debilis, Pseudo-nitzschia subcurvata, Fragilariopsis kerguelensis, and Phaeocystis antarctica. Using membrane-inlet mass spectrometry, photosynthetic O₂ evolution and inorganic carbon (C_i) fluxes were determined as a function of CO₂ concentration. Only the growth of C. debilis was enhanced under high P_CO2. Analysis of the carbon concentrating mechanism (CCM) revealed the operation of very efficient CCMs (i.e., high C_i affinities) in all species, but there were species-specific differences in CO₂-dependent regulation of individual CCM components (i.e., CO₂ and uptake kinetics, carbonic anhydrase activities). Gross CO₂ uptake rates appear to increase with the cell surface area to volume ratios. Species competition experiments with C. debilis and P. subcurvata under different P_CO2 levels confirmed the CO₂-stimulated growth of C. debilis observed in monospecific incubations, also in the presence of P. subcurvata. Independent of P_CO2, high initial cell abundances of P. subcurvata led to reduced growth rates of C. debilis. For a better understanding of future changes in phytoplankton communities, CO₂-sensitive physiological processes need to be identified, but also species interactions must be taken into account because their interplay determines the success of a species.

pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: implications for bloom formation in an acidified ocean

We investigated the effects of pH on movement behaviors of the harmful algal bloom causing raphidophyte Heterosigma akashiwo. Motility parameters from >8000 swimming tracks of individual cells were quantified using 3D digital video analysis over a 6-h period in 3 pH treatments reflecting marine carbonate chemistry during the pre-industrial era, currently, and the year 2100. Movement behaviors were investigated in two different acclimation-to-target-pH conditions: instantaneous exposure and acclimation of cells for at least 11 generations. There was no negative impairment of cell motility when exposed to elevated PCO₂ (i.e., low pH) conditions but there were significant behavioral responses. Irrespective of acclimation condition, lower pH significantly increased downward velocity and frequency of downward swimming cells (p < 0.001). Rapid exposure to lower pH resulted in 9% faster downward vertical velocity and up to 19% more cells swimming downwards (p < 0.001). Compared to pH-shock experiments, pre-acclimation of cells to target pH resulted in ~30% faster swimming speed and up to 46% faster downward velocities (all p < 0.001). The effect of year 2100 PCO₂ levels on population diffusivity in pre-acclimated cultures was >2-fold greater than in pH-shock treatments (2.2 × 10⁵ μm² s⁻¹ vs. 8.4 × 10⁴ μm² s⁻¹). Predictions from an advection-diffusion model, suggest that as PCO₂ increased the fraction of the population aggregated at the surface declined, and moved deeper in the water column. Enhanced downward swimming of H. akashiwo at low pH suggests that these behavioral responses to elevated PCO₂ could reduce the likelihood of dense surface slick formation of H. akashiwo through reductions in light exposure or growth independent surface aggregations. We hypothesize that the HAB alga’s response to higher PCO₂ may exploit the signaling function of high PCO₂ as indicative of net heterotrophy in the system, thus indicative of high predation rates or depletion of nutrients.

Calcification response to climate change in the Pliocene?

As a result of anthropogenic pCO₂ increases future oceans are growing warmer and lower in pH and oxygen, conditions that are likely to impact planktic communities. Past intervals of elevated and changing pCO₂ and temperatures can offer a glimpse into the response of marine calcifying plankton to changes in surface oceans under conditions similar to those projected for the future. Here we present new records of planktic foraminiferal and coccolith calcification from Deep Sea Drilling Project Site 607 (mid North Atlantic) and Ocean Drilling Program Site 999 (Caribbean Sea) from the Pliocene, the last time that pCO₂ was similar to today, and extending through a global cooling event into the Intensification of Northern Hemisphere Glaciation (3.3 to 2.6 million years ago). Test weights of both surface-dwelling foraminifera Globigerina bulloides and thermocline-dwelling foraminifera Globorotalia puncticulata vary, with a potential link to regional temperature variation in the North Atlantic, whereas in the tropics Globigerinoides ruber test weight remains stable. In contrast, reticulofenestrid coccoliths show a narrowing size range and a decline in the largest lith diameters over this interval. Our results suggest no major changes in plankton calcification during the high pCO₂ Pliocene or during the transition into an icehouse world.

Responses of the Emiliania huxleyi proteome to ocean acidification

Ocean acidification due to rising atmospheric CO2 is expected to affect the physiology of important calcifying marine organisms, but the nature and magnitude of change is yet to be established. In coccolithophores, different species and strains display varying calcification responses to ocean acidification, but the underlying biochemical properties remain unknown. We employed an approach combining tandem mass-spectrometry with isobaric tagging (iTRAQ) and multiple database searching to identify proteins that were differentially expressed in cells of the marine coccolithophore species Emiliania huxleyi (strain NZEH) between two CO2 conditions: 395 (~current day) and ~1340 p.p.m.v. CO2. Cells exposed to the higher CO2 condition contained more cellular particulate inorganic carbon (CaCO3) and particulate organic nitrogen and carbon than those maintained in present-day conditions. These results are linked with the observation that cells grew slower under elevated CO2, indicating cell cycle disruption. Under high CO2 conditions, coccospheres were larger and cells possessed bigger coccoliths that did not show any signs of malformation compared to those from cells grown under present-day CO2 levels. No differences in calcification rate, particulate organic carbon production or cellular organic carbon: nitrogen ratios were observed. Results were not related to nutrient limitation or acclimation status of cells. At least 46 homologous protein groups from a variety of functional processes were quantified in these experiments, of which four (histones H2A, H3, H4 and a chloroplastic 30S ribosomal protein S7) showed down-regulation in all replicates exposed to high CO2, perhaps reflecting the decrease in growth rate. We present evidence of cellular stress responses but proteins associated with many key metabolic processes remained unaltered. Our results therefore suggest that this E. huxleyi strain possesses some acclimation mechanisms to tolerate future CO2 scenarios, although the observed decline in growth rate may be an overriding factor affecting the success of this ecotype in future oceans.

Growth performance of microalgae exposed to CO2

The increase of CO₂ emission and other gases of greenhouse effect have caused global debates concerning climatic alterations, stimulating the development of mitigative strategies. Researches in this area include CO₂ kidnapping through aquatic microalgae production, as well as their use in the production of biofuels. The aim of this work was to determine the growth kinetics of microalgae (Chlorella sp, Scenedesmus spinosus, Scenedesmus acuminatus and Coelastrum sp.) exposed directly to CO₂. Measurements of microalgae growth and pH from medium were taken weekly. The results showed that carbon dioxide promoted growth inhibition in most microalgae. This condition should be considered for the developing of operational strategies and in projects of photobioreactors for the biological conversion of CO₂.

Synergism between elevated pCO2 and temperature on the Antarctic sea ice diatom Nitzschia lecointei

Polar oceans are particularly susceptible to ocean acidification and warming. Diatoms play a significant role in sea ice biogeochemistry and provide an important food source to grazers in ice-covered oceans, especially during early spring. However, the ecophysiology of ice living organisms has received little attention in terms of ocean acidification. In this study, the synergism between temperature and partial pressure of CO₂ (pCO₂) was investigated in relationship to the optimal growth temperature of the Antarctic sea ice diatom Nitzschia lecointei. Diatoms were kept in cultures at controlled levels of pCO₂ (∼390 and ∼960 μatm}) and temperature (−1.8 and 2.5 °C) for 14 days. Synergism between temperature and pCO₂ was detected in growth rate and acyl lipid fatty acid content. Carbon enrichment only promoted (3%) growth rate closer to the optimal growth, but not at the control temperature (−1.8 °C). Optimal growth rate was observed around 5 °C in a separate experiment. Polyunsaturated fatty acids (PUFA) comprised up to 98% of the total acyl lipid fatty acid pool at −1.8 °C. However, the total content of fatty acids was reduced by 39% at elevated pCO₂, but only at the control temperature. PUFAs were reduced by 30% at high pCO₂. Effects of carbon enrichment may be different depending on ocean warming scenario or season, e.g. reduced food quality for higher trophic levels during spring. Synergy between temperature and pCO₂ may be particularly important in polar areas since a narrow thermal window generally limits cold-water organisms.

Response of halocarbons to ocean acidification in the Arctic (update)

The potential effect of ocean acidification (OA) on seawater halocarbons in the Arctic was investigated during a mesocosm experiment in Spitsbergen in June–July 2010. Over a period of 5 weeks, natural phytoplankton communities in nine ~ 50 m³ mesocosms were studied under a range of pCO₂ treatments from ~ 185 μatm to ~ 1420 μatm. In general, the response of halocarbons to pCO₂ was subtle, or undetectable. A large number of significant correlations with a range of biological parameters (chlorophyll a, microbial plankton community, phytoplankton pigments) were identified, indicating a biological control on the concentrations of halocarbons within the mesocosms. The temporal dynamics of iodomethane (CH₃I) alluded to active turnover of this halocarbon in the mesocosms and strong significant correlations with biological parameters suggested a biological source. However, despite a pCO₂ effect on various components of the plankton community, and a strong association between CH₃I and biological parameters, no effect of pCO₂ was seen in CH₃I. Diiodomethane (CH₂I₂) displayed a number of strong relationships with biological parameters. Furthermore, the concentrations, the rate of net production and the sea-to-air flux of CH₂I₂ showed a significant positive response to pCO₂. There was no clear effect of pCO₂ on bromocarbon concentrations or dynamics. However, periods of significant net loss of bromoform (CHBr₃) were found to be concentration-dependent, and closely correlated with total bacteria, suggesting a degree of biological consumption of this halocarbon in Arctic waters. Although the effects of OA on halocarbon concentrations were marginal, this study provides invaluable information on the production and cycling of halocarbons in a region of the world’s oceans likely to experience rapid environmental change in the coming decades.

Rising CO2 interacts with growth light and growth rate to alter photosystem II photoinactivation of the coastal diatom Thalassiosira pseudonana

We studied the interactive effects of pCO₂ and growth light on the coastal marine diatom Thalassiosira pseudonana CCMP 1335 growing under ambient and expected end-of-the-century pCO₂ (750 ppmv), and a range of growth light from 30 to 380 µmol photons·m⁻²·s⁻¹. Elevated pCO₂ significantly stimulated the growth of T. pseudonana under sub-saturating growth light, but not under saturating to super-saturating growth light. Under ambient pCO₂ susceptibility to photoinactivation of photosystem II (σ_i) increased with increasing growth rate, but cells growing under elevated pCO₂ showed no dependence between growth rate and σ_i, so under high growth light cells under elevated pCO₂ were less susceptible to photoinactivation of photosystem II, and thus incurred a lower running cost to maintain photosystem II function. Growth light altered the contents of RbcL (RUBISCO) and PsaC (PSI) protein subunits, and the ratios among the subunits, but there were only limited effects on these and other protein pools between cells grown under ambient and elevated pCO₂.