Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient

Christopher B Wall,Ruth D Gates,Brian N Popp,Mario Kaluhiokalani,Megan J Donahue

doi:10.1038/s41396-019-0570-1

Abstract

Reef corals are mixotrophic organisms relying on symbiont-derived photoautotrophy and water column heterotrophy. Coral endosymbionts (Family: Symbiodiniaceae), while typically considered mutualists, display a range of species-specific and environmentally mediated opportunism in their interactions with coral hosts, potentially requiring corals to rely more on heterotrophy to avoid declines in performance. To test the influence of symbiont communities on coral physiology (tissue biomass, symbiont density, photopigmentation) and nutrition (δ13C, δ15N), we sampled Montipora capitata colonies dominated by a specialist symbiont Cladocopium spp. or a putative opportunist Durusdinium glynnii (hereafter, C- or D-colonies) from Kāne‘ohe Bay, Hawai‘i, across gradients in photosynthetically active radiation (PAR) during summer and winter. We report for the first time that isotope values of reef corals are influenced by Symbiodiniaceae communities, indicative of different autotrophic capacities among symbiont species. D-colonies had on average 56% higher symbiont densities, but lower photopigments per symbiont cell and consistently lower δ13C values in host and symbiont tissues; this pattern in isotope values is consistent with lower symbiont carbon assimilation and translocation to the host. Neither C- nor D-colonies showed signs of greater heterotrophy or nutritional plasticity; instead changes in δ13C values were driven by PAR availability and photoacclimation attributes that differed between symbiont communities. Together, these results reveal Symbiodiniaceae functional diversity produces distinct holobionts with different capacities for autotrophic nutrition, and energy tradeoffs from associating with opportunist symbionts are not met with increased heterotrophy.

Highlights

Nutrient exchanges between scleractinian corals and dinoflagellate symbionts (Symbiodiniaceae, formerly Symbiodinium spp.) [1] underpin the success of reef-building corals as habitat engineers in coral reef ecosystems [2]
Ammonium, and nitrate + nitrite (N + N) concentrations were higher in winter compared to summer (p ≤ 0.046) (Table S1), and the two northern sites had higher N + N and phosphate concentrations compared to southern sites (p < 0.001)
Light attenuation in Kāne‘ohe Bay was rapid across a narrow depth gradient with maximum photosynthetically active radiation (PAR) at 1 m-depth across all sites attenuated to 50–350 μmol photons m−2 s−1 at 8 m-depth— equivalent to PAR attenuation observed at 40–70 m in coral reefs of the Red Sea [73] and 20–40 m in the Caribbean

Summary

Introduction

Nutrient exchanges between scleractinian corals and dinoflagellate symbionts (Symbiodiniaceae, formerly Symbiodinium spp.) [1] underpin the success of reef-building corals as habitat engineers in coral reef ecosystems [2]. Associations with stress-tolerant symbionts can provide increased stress tolerance for corals albeit at the expense of coral performance [11], potentially requiring greater heterotrophic feeding to meet energy demands. The genetic and functional diversity of Symbiodiniaceae shapes the energy balance and stress tolerance of reef corals. Taxonomic resolution of Symbiodiniaceae has been achieved using genetic markers, primarily the internal transcribed spacer 2 (ITS2) region of nrDNA [12, 13], and has revealed distinct symbiont genera and species (formerly clades and subclades) [1] with different capacities to support coral nutrition [14, 15] and tolerate environmental stress [16].

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Results

Discussion

Conclusion