Temperature and feeding induce tissue level changes in autotrophic and heterotrophic nutrient allocation in the coral symbiosis – A NanoSIMS study

Abstract

Corals access inorganic seawater nutrients through their autotrophic endosymbiotic dinoflagellates, but also capture planktonic prey through heterotrophic feeding. Correlating NanoSIMS and TEM imaging, we visualized and quantified the subcellular fate of autotrophic and heterotrophic C and N in the coral Stylophora pistillata using stable isotopes. Six scenarios were compared after 6 h: autotrophic pulse (13C-bicarbonate, 15N-nitrate) in either unfed or regularly fed corals, and heterotrophic pulse (13C-, 15N-labelled brine shrimps) in regularly fed corals; each at ambient and elevated temperature. Host assimilation of photosynthates was similar under fed and unfed conditions, but symbionts assimilated 10% more C in fed corals. Photoautotrophic C was primarily channelled into host lipid bodies, whereas heterotrophic C and N were generally co-allocated to the tissue. Food-derived label was detected in some subcellular structures associated with the remobilisation of host lipid stores. While heterotrophic input generally exceeded autotrophic input, it was more negatively affected by elevated temperature. The reduced input from both modes of nutrition at elevated temperature was accompanied by a shift in the partitioning of C and N, benefiting epidermis and symbionts. This study provides a unique view into the nutrient partitioning in corals and highlights the tight connection of nutrient fluxes in symbiotic partners.

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata

“…Even though significant physiological changes were observed, the feeding treatment is likely a conservative representation of food availability on the reef, where corals have access to a quasi‐continuous availability of diverse zooplankton. In previous studies, feeding with similar diets to that used here, has been reported to increase (Treignier, Grover, Ferrier‐Pagés, & Tolosa, ), decrease (Al‐Moghrabi, Allemand, Couret, & Jaubert, ), and not change (Krueger et al, ) symbiont densities and/or Chl a concentration and the outcome likely depends on other environmental factors such as light level. Increased Chl a concentration found in this study may be an acclimation to low food conditions and low light in an attempt to increase light capture and photosynthetic efficiency.…”

“…Treignier, Grover, Ferrier-Pagés, & Tolosa, 2008), decrease (Al-Moghrabi,Allemand, Couret, & Jaubert, 1995), and not change(Krueger et al, 2018) symbiont densities and/or Chl a concentration and the outcome likely depends on other environmental factors such as light level. Increased Chl a concentration found in this study may be an acclimation to low food conditions and low light in an attempt F I G U R E 1 Parent (a-d) and planulae (e-h) physiology from fed (black) and unfed (gray) Stylophora pistillata: (a) parent host protein concentration per surface area, (b) parent symbiont cells per surface area, (c) parent chlorophyll a concentration per symbiont cell (parents fed n = 6, unfed n = 6), (d) total number of planulae released, (e) protein concentration per planula, (f) symbiont cells per planula, (g) chlorophyll a concentration per symbiont cell in planulae (n = triplicate of 20 pooled planulae per treatment), and (h) photosynthetic yield of planulae (n = 10 per treatment.…”

The past, present, and future of coral heat stress studies

“…A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). Recent studies have increasingly been combining coral and Symbiodiniaceae responses in their hypothesis testing.…”

“…Recent studies have increasingly been combining coral and Symbiodiniaceae responses in their hypothesis testing. A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). These have shown that the metabolic balance between the two partners is not only sensitive to environmental stressors but specifically fine-tuned (Cui et al, 2019;Matthews et al, 2017;Nielsen, Petrou, & Gates, 2018).…”

A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

“…Corals are meta-organisms (so-called holobionts 6 ) that host a dynamic population of bacteria, archaea, viruses and photosynthetic dinoflagellate algae (family: Symbiodiniaceae) 7 . The flux of metabolites between the host and its symbionts has been the subject of numerous studies using stable isotope labelling combined with either bulk tissue analyses 8,9 or correlative imaging [10][11][12][13][14][15] . However, these previous studies have generally focused on the photosynthetic performance of the algae and the metabolic interactions between host and symbiont population.…”