Adaptive physiology of reef-associated foraminifera to the combined effects of ocean acidification and warming

ABSTRACT: The association with photosymbiotic algae is crucial for the proliferation of many coral reef organisms, but increases their sensitivity to environmental changes. Large benthic foraminifera (LBF) are a diverse group of carbonate producers harboring algal photosymbionts. They act as key ecological engineers and are widely used as bioindicators. As in corals, elevated temperatures and light intensities are known to induce bleaching in LBF, but the combined effects of ocean acidification and warming remain unclear. To shed light into the adaptive physiology of LBF, we linked the assessment of the holobiont and photosymbiont physiological condition (mortality, growth, coloration, and chlorophyll a) to a bottom-up proteomics approach that allows the examination of cellular responses of host and symbionts simultaneously. In a two-months experiment, we exposed Amphistegina lobifera to the combined effects of ocean acidification (400, 1000 and 2800 ppm pCO2) and warming (28-control and 31°C). More than 1,000 proteins were identified by label-free mass spectrometry-based whole proteome analysis and assigned to the host or photosymbionts. Photopigment concentrations declined in response to elevated pCO2, visible by discoloration. These indicate the reduction of photosymbiont densities under ocean acidification, despite the fertilizing effects suggested for high inorganic carbon availability, and imply metabolic adjustments. Increases of proteolytic proteins suggest active host regulation of photosymbiont density in order to maintain homeostasis with its algal photosymbionts. Growth rates, however, were unaffected by elevated pCO2 levels at control temperatures, but high pCO2 levels (2800 ppm, pH 7.52) combined with thermal stress (31°C) impaired growth, though mortality and shell dissolution was negligible. While growth was unaffected by intermediate pCO2 levels (1000 ppm, pH 7.98) combined with ocean warming, this treatment induced the most distinct proteome responses. These include the regulation of ion transporters and host cytoplasmic proteins that likely abet calcification under ocean acidification. This study reveals a highly complex cellular response in both the host and the photosymbiont, which appears to facilitate a high resilience potential of A. lobifera to end of the century ocean conditions. Nevertheless, our results imply that when pCO2 levels rise above 1000 ppm during persistent ocean warming or extreme heating events these adaptive mechanisms become disrupted.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Bacillariophyta Amphistegina Lobifera

SUBMITTER: Bernhard Blank-Landeshammer  

LAB HEAD: Albert Sickmann

PROVIDER: PXD009890 | Pride | 2022-02-23

REPOSITORIES: Pride