Divergent Proteomic Responses Offer Insights into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios

Reef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive to climate change. To gain insight into their responses to near-future conditions, Amphistegina lobifera from the Gulf of Aqaba were cultured under three pCO conditions (492, 963, 3182 ppm) crossed with two temperature conditions (28 °C, 31 °C) for two months. Differential protein abundances in host and photosymbionts were investigated alongside physiological responses and microenvironmental pH gradients assessed via proton microsensors. Over 1000 proteins were identified, of which > 15% varied significantly between treatments. Thermal stress predominantly reduced protein abundances, and holobiont growth. Elevated pCO caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing pCO under all light/dark and temperature combinations. However, the difference between [H] at the test surface and [H] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and pCO. Combined stressors resulted in reduced pore sizes and increased microenvironmental pH gradients, indicating acclimative mechanisms that support calcite test production and/or preservation under climate change. Substantial proteomic variations at moderate-pCO and 31 °C and putative decreases in test stability at high-pCO and 31 °C indicate cellular modifications and impacts on calcification, in contrast to the LBFs’ apparently stable overall physiological performance. Our experiment shows that the effects of climate change can be missed when stressors are assessed in isolation, and that physiological responses should be assessed across organismal levels to make more meaningful inferences about the fate of reef calcifiers.