Bio-optical properties and radiative energy budgets in fed and unfed scleractinian corals (Pocillopora sp.) during thermal bleaching

Corals live in symbiosis with algal dinoflagellates, which can achieve outstanding photosynthetic energy efficiencies in hospite approaching theoretical limits. However, how such photosynthetic efficiency varies with environmental stress remains poorly known. Using fiber-optic and electrochemical microsensors in combination with variable chlorophyll fluorescence imaging, we investigated the combined effects of thermal stress and active feeding on the radiative energy budget and photosynthetic efficiency of the symbiotic coral Pocillopora sp. At ambient temperature (25°C), the percentage of absorbed light energy used for photosynthesis under low irradiance was higher for fed (~5-6%) compared to unfed corals (4%). Corals from both feeding treatments responded equally to stress from high light exposure (2400 µmol photons m-2 s-1), exhibiting a decrease in photosynthetic efficiency, down to 0.5-0.6%. Fed corals showed increased resilience to thermal-induced bleaching (loss of symbionts) compared to unfed corals. In addition, while unfed corals decreased their photosynthetic efficiency almost immediately when exposed to thermal stress, fed corals maintained a constant and high photosynthetic efficiency for 5 more days after onset of thermal stress. We conclude that active feeding is beneficial to corals by prolonging coral health and resilience during thermal stress as a result of an overall healthier symbiont population.

Autotrophic and heterotrophic nutrient fluxes in the dinoflagellate-coral symbiosis – A NanoSIMS perspective

Julia Marie Jeanne Yvonne Bodin, Isabelle Domart-Coulon, Maoz Fine, Thomas Krüger, Anders Meibom

The exchange of metabolites between photosynthetic symbionts and their coral host in shallow-water scleractinians provides the nutritional basis for their successful evolution and the existence of massive coral reefs in oligotrophic tropical waters. Autotrophic nutrition, based on carbon- and nitrogen-rich photosynthetic metabolites, is complemented by heterotrophic uptake and assimilation of organic matter to obtain additional carbon, nitrogen and phosphorus. By combining TEM ultrastructural observations with quantitative NanoSIMS isotopic imaging of tissue sections at sub-cellular resolution, we have compared the exchange of nutrients from the autotrophic assimilation of 15N-nitrate and 13C-bicarbonate with the heterotrophic uptake from 15N- and 13C-labelled brine shrimps in Stylophora pistillata from the Red Sea. Our results confirm that heterotrophy serves as the dominant source of nitrogen for the coral holobiont. On a time scale of 6 hours, heterotrophy provided approximately nine times more nitrogen to the host gastrodermal anabolism than symbiont nitrate fixation and translocation. Heterotrophic nitrogen was also used in anabolic processes in the symbionts, but at a level about 40% lower compared with nitrogen incorporation from nitrate fixation. The role of photosynthesizing symbionts the major contributors of carbon to the coral host was evident from the observation that autotrophic carbon enrichment in the gastrodermal layer was seven times higher in comparison to the heterotrophic carbon acquisition. Our observations directly demonstrate the complementing roles of heterotrophic and autotrophic food acquisition and support the notion that recycling of nutrients in symbiotic coral holobionts is critical to their vitality. The effects of stress from environmental change, including increasing water temperature and ocean acidification, are under investigation.

2015

Coral photosymbiosis: Linking phylogenetic identity to single cell metabolic activity in mixed symbiont populations

Isabelle Domart-Coulon, Maoz Fine, Béatrice Gaume, Anders Meibom

Tropical reef-building corals live in symbiosis with a wide range of micro-organisms, including unicellular Symbiodinium dinoflagellates also called zooxanthellae. These photosynthetic endosymbionts live inside the coral gastroderm cells. Although corals can feed on planktonic preys, the dinoflagellates significantly contribute to the nutrition of their host by transferring a large fraction (up to 90%) of photosynthates that are produced through the fixation of dissolved inorganic carbon (DIC) and nitrogen (nitrate or ammonium). Nine major clades (A-I) of Symbiodinium have been identified by molecular genetic analyses. Each clade presents distinct physiological features and the specific association between coral species and Symbiodinium clade determines the phenotype of the holobiont. Differences in the photosynthetic response to irradiance, rates of carbon fixation, and thermal tolerance can be attributed to symbiont clade. Several Symbiodinium clades can simultaneously exist within a single coral and the host can dynamically modify the proportion between dominant and background clades to adapt to changing environmental conditions. Investigating at the cellular level the metabolic exchanges between coral and Symbiodinium is of great interest to understand e.g. the bleaching process (loss of zooxanthellae) which often leads to coral death. We are aiming at quantitatively image the differential metabolic activity between symbiont clades in the same host, in the intact symbiosis. Previous studies have used mass bulk techniques to investigate the metabolism of symbionts at the colony scale. However, such studies cannot determine the specific contribution of the individual cells, as a function of their distribution in the coral host tissue. We have developed a SIMS-ISH method combining nanoscale secondary ion mass spectrometry (NanoSIMS) and in situ hybridization (ISH) for the simultaneous in situ identification of Symbiodinium genotype, and visualization of symbiont-host metabolic exchange at the level of individual cell. We focus on two reef-building coral species Pocillopora damicornis and Stylophora pistillata for which a large amount of complementary metabolic data exists. We designed specific fluorescent DNA probes to identify clade C Symbiodinium in P. damicornis and clade A in S. pistillata, and in mixed cultures. We combined the probes with pulse-chase experiments using isotopically labeled seawater (13C-bicarbonate and 15N-nitrate) to attribute a particular metabolism to a specific clade. This combined method enables us to phylogenetically identify metabolically active cells from a NanoSIMS isotopic/elemental image. The precise correlation between TEM and the NanoSIMS isotopic maps allows us to follow the turnover and translocation of metabolites with sub-cellular precision in both the symbionts and the host. Due to the complex nature of the coral symbiosis, the ability to discriminate the phylogenetic identity and metabolic role of specific Symbiodinium populations in situ is crucial to understand the effects of environmental stress on the coral holobiont plasticity. Moreover, analyzing symbiotic associations in situ provides a unique insight into the spatio-temporal patterns of metabolic interactions in holobionts. This analytical breakthrough promises to open entirely new areas of research focused on understanding the dynamics of interactions between animals and the microbial world.

2017

Effect of temperature and feeding on carbon budgets and O2 dynamics in Pocillopora damicornis

Niclas Heidelberg Lyndby

Studying carbon dynamics in the coral holobiont provides essential knowledge of nutritional strategies and is thus central to understanding coral ecophysiology. In this study, we assessed the carbon budget in Pocillopora damicornis (usingH13CO3) as a function of feeding status and temperature stress. We also compared dissolved oxygen (O2) fluxes measured at the colony scale and at the polyp scale. At both scales, O2 production rates were enhanced for fed vs. unfed corals, and unfed corals exhibited higher bleaching and reduced photosynthetic activity at high temperature. Unfed corals exclusively respired autotrophically acquired carbon, while fed corals mostly respired heterotrophically acquired carbon. As a consequence, fed corals excreted on average >5 times more organic carbon than unfed corals. Photosynthate translocation was higher under thermal stress, but most of the carbon was lost via respiration and/or mucus release (42−46% and 57−75% of the fixed carbon for unfed and fed corals, respectively). Such high loss of translocated carbon, coupled to low assimilation rates in the coral tissue and symbionts, suggests that P. dami - cornis was nitrogen and/or phosphorus limited. Heterotrophy might thus cover a larger portion of the nutritional demand for P. damicornis than previously assumed. Our results suggest that active feeding plays a fundamental role in metabolic dynamics and bleaching susceptibility of corals.