Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

Symbiosis with unicellular algae in the family Symbiodiniaceae is common across tropical marine invertebrates. Reef-building corals offer a clear example of cellular dysfunction leading to a dysbiosis that disrupts entire ecosystems in a process termed coral bleaching. Due to their obligate symbiotic relationship, understanding the molecular underpinnings that sustain this symbiosis in tropical reef-building corals is challenging, as any aposymbiotic state is inherently coupled with severe physiological stress. Here, we leverage the subtropical, facultatively symbiotic and calcifying coral Oculina arbuscula to investigate gene expression differences between aposymbiotic and symbiotic branches within the same colonies under baseline conditions. We further compare gene ontology (GO) and KOG enrichment in gene expression patterns from O. arbuscula with prior work in the sea anemone Exaiptasia pallida (Aiptasia) and the salamander Ambystoma maculatum—both of which exhibit endophotosymbiosis with unicellular algae. We identify nitrogen cycling, cell cycle control, and immune responses as key pathways involved in the maintenance of symbiosis under baseline conditions. Understanding the mechanisms that sustain a healthy symbiosis between corals and Symbiodiniaceae algae is of urgent importance given the vulnerability of these partnerships to changing environmental conditions and their role in the continued functioning of critical and highly diverse marine ecosystems.

Recruits of the temperate coral Oculina arbuscula mimic adults in their resilience to ocean acidification

Ocean acidification has been investigated extensively in scleractinian corals, but studies on different life stages of the same species are lacking. We investigated the response of recruits of the temperate coral Oculina arbuscula to increased CO2 concentrations, a species whose adults show significant tolerance to elevated concentrations of CO2. Specifically, we exposed small colonies (5-12 mm diameter) to 475, 710, and 1261 ppm CO2 for 75 d in the laboratory to address the hypothesis that, like adults, the health of O. arbuscula recruits is not affected by increased CO2 concentrations. Calcification rates were monitored regularly during the experiment, while mortality, respiration rates, photosynthetic rates, algal symbiont densities, and soluble protein were quantified at the end. As predicted, CO2 concentration did not impact survival, algal densities, or soluble protein concentrations in O. arbuscula recruits. In contrast, both calcification rates and photosynthesis:respiration ratios tended to be lower at higher CO2. Comparing the results of this study on recruits with published studies on adults suggested that both life stages exhibit a similar non-linear response to CO2 concentration, whereby recruits may be unable to counter the increased energetic cost of calcification that occurs at the highest CO2. Based on these results and environmental monitoring showing that mean pCO2 is increasing by ~2.4% yr-1 in the waters off Georgia, USA, we conclude that O. arbuscula recruits may begin to exhibit depressed calcification rates within the current century if CO2 emissions are not reduced.

<i>δ</i>¹¹B as monitor of calcification site pH in divergent marine calcifying organisms

The boron isotope composition (δ11B) of marine biogenic carbonates has been predominantly studied as a proxy for monitoring past changes in seawater pH and carbonate chemistry. However, a number of assumptions regarding chemical kinetics and thermodynamic isotope exchange reactions are required to derive seawater pH from δ11B biogenic carbonates. It is also probable that δ11B of biogenic carbonate reflects seawater pH at the organism's site of calcification, which may or may not reflect seawater pH. Here, we report the development of methodology for measuring the δ11B of biogenic carbonate samples at the multi-collector inductively coupled mass spectrometry facility at Ifremer (Plouzané, France) and the evaluation of δ11BCaCO3 in a diverse range of marine calcifying organisms reared for 60 days in isothermal seawater (25 °C) equilibrated with an atmospheric pCO2 of ca. 409 µatm. Average δ11BCaCO3 composition for all species evaluated in this study range from 16.27 to 35.09 ‰, including, in decreasing order, coralline red alga Neogoniolithion sp. (35.89 ± 3.71 ‰), temperate coral Oculina arbuscula (24.12 ± 0.19 ‰), serpulid worm Hydroides crucigera (19.26 ± 0.16 ‰), tropical urchin Eucidaris tribuloides (18.71 ± 0.26 ‰), temperate urchin Arbacia punctulata (16.28 ± 0.86 ‰), and temperate oyster Crassostrea virginica (16.03 ‰). These results are discussed in the context of each species' proposed mechanism of biocalcification and other factors that could influence skeletal and shell δ11B, including calcifying site pH, the proposed direct incorporation of isotopically enriched boric acid (instead of borate) into biogenic calcium carbonate, and differences in shell/skeleton polymorph mineralogy. We conclude that the large inter-species variability in δ11BCaCO3 (ca. 20 ‰) and significant discrepancies between measured δ11BCaCO3 and δ11BCaCO3 expected from established relationships between abiogenic δ11BCaCO3 and seawater pH arise primarily from fundamental differences in calcifying site pH amongst the different species. These results highlight the potential utility of δ11B as a proxy of calcifying site pH for a wide range of calcifying taxa and underscore the importance of using species-specific seawater-pH–δ11BCaCO3 calibrations when reconstructing seawater pH from δ11B of biogenic carbonates.

δ¹¹B as monitor of calcification site pH in marine calcifying organisms

The isotope composition of boron (B) in marine biogenic carbonates has been predominantly studied as a proxy for monitoring past changes in seawater pH and carbonate chemistry. In order to derive seawater pH from boron isotope ratio data, a number of assumptions related to chemical kinetics and themodynamic isotope exchange reactions are necessary. Furthermore, the boron isotope composition (δ11B) of biogenic carbonates (δ11BCaCO3) is assumed to reflect the δ11B of dissolved borate (B(OH)4−) in seawater. Here we report the development of methodology for measuring the δ11B in biogenic carbonate samples at the multi-collector inductively coupled mass spectrometry facility at Ifremer (Plouzané, France) and the evaluation of δ11BCaCO3 in a diverse range of marine calcifying organisms. We evaluated the δ11BCaCO3 of 6 species of marine calcifiers (a temperate coral, Oculina arbuscula; a coralline red alga, Neogoniolithion sp.; a tropical urchin, Eucidaris tribuloides; a temperate urchin, Arbacia punctulata; a serpulid worm, Hydroides crucigera; and an American oyster, Crassostrea virginica) that were reared for 60 days in isothermal seawater (25 °C) equilibrated with an atmospheric pCO2 of ca. 409 μatm. We observe large inter-species variability in δ11BCaCO3 (ca. 20 ‰) and significant discrepancies between measured δ11BCaCO3 and δ11BCaCO3 expected from established relationships between δ11BCaCO3 and seawater pH. We discuss these results in the context of various proposed mechanisms of biocalcification, including the potential dominant role that internal calcifying site pH plays in regulating CaCO3 saturation state and borate δ11B at the site of calcification and, thus, the δ11B composition of calcifers’ shells and skeletons.