Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata

Abstract

Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ15N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a, lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.

Amino acid δ13C and δ15N analyses reveal distinct species‐specific patterns of trophic plasticity in a marine symbiosis

“…While intriguing, due to the low statistical power (small effect size and low replication) and no difference in either TP Glx-Phe or the difference in the δ 15 N-weighted mean values for trophic and source amino acids of hosts and symbionts, caution is required in interpreting these percent heterotrophy calculations from TP Glx-Phe . However, these results suggest corals feed less often on prey of TP Glx-Phe of 2.0 and microalgae-derived detritus, and not zooplanktivory, is the dominant source of heterotrophy identified in previous studies using these calculations (Fujii et al 2020;Martinez et al 2020). As more AA-CSIA data sets become available for coral and invertebrates (Shih et al 2020), it will be important for fundamental assumptions in these methods to be evaluated (i.e., canonical constants, enrichment factors, prey sources) as these may vary in response to diet quality or due to underlying differences in the potential for corals and their Symbiodiniaceae or microbiomes to synthesize amino acids and demonstrate nutritional flexibility or fidelity.…”

“…CSIA also have greater resolution and can simultaneously provide information on dietary food sources, nutrition, and physiology of an organism (Ohkouchi et al 2017; Whiteman et al 2019). Recently, carbon AA‐CSIA (Fox et al 2019), nitrogen AA‐CSIA (Fujii et al 2020; Martinez et al 2020), and FA‐CSIA (Teece et al 2011) have been applied in corals to examine nutritional modes at biological (i.e., within and among species) and environmental levels (i.e., shallow and mesophotic habitats). However, to date, few CSIA of reef corals exist and AA‐CSIA have been limited to ecological studies without experimental manipulation of feeding in controlled laboratory conditions.…”

A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity

“…A critical coral cellular specialization is the establishment of a stable photosymbiosis with Symbiodiniaceae dinoflagellate algae. To gain insights into this symbiosis at single-cell resolution, we devised a FACS-sorting strategy that allowed us to sample coral cells bearing Symbiodinium microadriaticum dinoflagellates ( Martinez et al, 2020 ) and to simultaneously analyze the single-cell transcriptomes of the coral cell and the dinoflagel-late cell inside it ( Figures 4A, 4B , S5A, and S5B ). These symbionts reside inside cells found around the gastrovascular cavity and along the vascular canals in the coenenchyma, as revealed by ISH against a predicted host cell marker (XP_022783975_1) ( Figure 4C ).…”

“…To quantify single-cell gene expression in symbiont cells, we applied the same strategy to MARS-seq reads but this time mapped reads to the Symbiodinium microadriaticum genome, the dominant dinoflagellate symbiont species in S . pistillata in shallow waters ( Aranda et al, 2016 ; Martinez et al, 2020 ). For the comparison of Symbiodinium inside coral against free-living Symbiodinium ,we used published transcriptomics data from cultures grown under standard conditions (“control” samples) ( Liew et al, 2017 ).…”

Physiological and transcriptomic variability indicative of differences in key functions within a single coral colony

“…The reef-building corals are also host to intracellular symbiotic dinoflagellates, whose photosynthetic activity restricts the scleractinian coral holobiont to the top ∼100 m of the ocean and fulfills much of the host’s carbon nutritional requirements [e.g., 6]. Nevertheless, uptake of dissolved nutrients and active feeding on particles from the water column both play significant roles as well [e.g., 7, 8] [reviewed in 9], with active predation utilizing toxins produced and delivered by cnidocytes [recently reviewed by 10]. These fixed carbon sources ultimately power the production of the external calcium carbonate skeleton that forms the reef and persists after the animal has died.…”