Abstract

With rising atmospheric CO2, phytoplankton face shifts in ocean chemistry including increased dissolved CO2 and acidification that will likely influence the relative competitive fitness of different phytoplankton taxa. Here we compared the physiological and gene expression responses of six species of phytoplankton including a diatom, a raphidophyte, two haptophytes, and two dinoflagellates to ambient (~400 ppm) and elevated (~800 ppm) CO2. Dinoflagellates had significantly slower growth rates and higher, yet variable, chlorophyll a per cell under elevated CO2. The other phytoplankton tended to have increased growth rates and/or decreased chlorophyll a per cell. Carbon and nitrogen partitioning of cells shifted under elevated CO2 in some species, indicating potential changes in energy fluxes due to changes in carbon concentrating mechanisms (CCM) or photorespiration. Consistent with these phenotypic changes, gene set enrichment analyses revealed shifts in energy, carbon and nitrogen metabolic pathways, though with limited overlap between species in the genes and pathways involved. Similarly, gene expression responses across species revealed few conserved CO2-responsive genes within CCM and photorespiration categories, and a survey of available transcriptomes found high diversity in biophysical CCM and photorespiration expressed gene complements between and within the four phyla represented by these species. The few genes that displayed similar responses to CO2 across phyla were from understudied gene families, making them targets for further research to uncover the mechanisms of phytoplankton acclimation to elevated CO2. These results underscore that eukaryotic phytoplankton have diverse gene complements and gene expression responses to CO2 perturbations and highlight the value of cross-phyla comparisons for identifying gene families that respond to environmental change.

Highlights

  • Anthropogenic CO2 emissions have increased the concentration of CO2 in the atmosphere from ∼280 ppm at the start of the Industrial Revolution to ∼400 ppm at present (Le Quéré et al, 2012), with levels predicted to rise to ∼800 ppm by 2100 (Ciais et al, 2013)

  • To examine how concentrating mechanisms (CCM) and photorespiration genes are modulated in response to CO2 and what impact this has on core metabolic processes and growth rate responses, six eukaryotic phytoplankton species from four phyla were cultured under elevated (∼800 ppm) and ambient (∼400 ppm) CO2

  • The chlorophyll a content trended higher under elevated CO2 in both dinoflagellates, it was highly variable within biological replicates and not statistically significantly different between CO2 treatments (Figure 1, Table 1)

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Summary

INTRODUCTION

Anthropogenic CO2 emissions have increased the concentration of CO2 in the atmosphere from ∼280 ppm at the start of the Industrial Revolution to ∼400 ppm at present (Le Quéré et al, 2012), with levels predicted to rise to ∼800 ppm by 2100 (Ciais et al, 2013). To examine how CCM and photorespiration genes are modulated in response to CO2 and what impact this has on core metabolic processes and growth rate responses, six eukaryotic phytoplankton species from four phyla were cultured under elevated (∼800 ppm) and ambient (∼400 ppm) CO2. These phytoplankton included: a cosmopolitan diatom (Chaetoceros affinis), a raphidophyte (Heterosigma akashiwo), a calcifying haptophyte (Gephyrocapsa oceanica), a non-calcifying haptophyte (Chrysochromulina polylepis), and two dinoflagellates (Alexandrium monilatum and Prorocentrum minimum). A comprehensive analysis of all consensus sequences from the same four phyla within the marine microbial eukaryote transcriptome project (MMETSP) database was conducted to assess the potential for these phytoplankton lineages to acclimate to rising CO2 based on the expressed gene complement of CCM and photorespiration pathways

METHODS
Section 1: CO2 Physiology of Six Eukaryotic Phytoplankton Species
Section 2: CO2-Induced Changes in Gene Expression
Section 3: Survey of CCM and Photorespiration Gene Complement of
CONCLUSIONS
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