Intracellular competition for nitrogen controls dinoflagellate population density in corals

Abstract

The density of dinoflagellate microalgae in the tissue of symbiotic corals is an important determinant for health and productivity of the coral animal. Yet, the specific mechanism for their regulation and the consequence for coral nutrition are insufficiently understood due to past methodological limitations to resolve the fine-scale metabolic consequences of fluctuating densities. Here, we characterized the physiological and nutritional consequences of symbiont density variations on the colony and tissue level in Stylophora pistillata from the Red Sea. Alterations in symbiont photophysiology maintained coral productivity and host nutrition across a broad range of symbiont densities. However, we demonstrate that density-dependent nutrient competition between individual symbiont cells, manifested as reduced nitrogen assimilation and cell biomass, probably creates the negative feedback mechanism for symbiont population growth that ultimately defines the steady-state density. Despite fundamental changes in symbiont nitrogen assimilation, we found no density-related metabolic optimum beyond which host nutrient assimilation or tissue biomass declined, indicating that host nutrient demand is sufficiently met across the typically observed range of symbiont densities under ambient conditions.

Coral Productivity Is Co-Limited by Bicarbonate and Ammonium Availability

“…Although this remains to be tested, similar changes might have occurred in our coral symbiosis following iC enrichment, which have requested higher nitrogen acquisition by the symbionts, only possible, in oligotrophic waters, with an additional input of iN. In turn, the increased nitrogen input has promoted Symbiodinium proliferation within host tissues, resulting very likely in a greater competition for CO 2 /HCO 3 − between individual endosymbiotic cells [66]. Therefore, when CO 2 is provided concomitantly with nitrogen, photosynthetic rates at the symbiont and the holobiont levels are further improved.…”

Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming

“…As cell division is directly linked to respiratory metabolism (which converts carbohydrates produced during photosynthesis into cellular metabolites used in the construction of cells; Falkowski et al ., 1985; Geider & Osborne, 1989), respiration rates must also be kept low when in hospite (Rädecker et al ., 2018; M. Pierangelini, unpublished). However, at the same time, photosynthesis must be maintained in order to guarantee the translocation of the fixed carbon to the host (Matthews et al ., 2017, 2018; Krueger et al ., 2020). Thus, we put forward the idea that having photosynthetic activity which can function independently from respiration could represent an advantage for Symbiodiniaceae in establishing successful endosymbiosis.…”

Competitive traits of coral symbionts may alter the structure and function of the microbiome

“…For example, in N-limited coral reef habitats, symbionts with low nitrogen demand will have a relatively lower sensitivity to nutrient limitation and therefore higher competitive potential in oligotrophic environments [42]. Nitrogen limitation within coral cells has recently been confirmed by NanoSIMS with density dependent effects on symbiont populations [8]. The lower baseline requirement for nutrients observed in C. goreaui relative to D. trenchii at 26°C correlates with their tendency to dominate coral hosts under ambient temperature conditions [19].…”

“…Evidence of symbiont competition for host habitat [44] and resources [8] has been accumulating with potential negative effects on the coral host. The competitively driven changes in symbiont metabolism revealed herein would have downstream effects on the coral symbiosis potentially through both resource diversion, allelopathy, and/or competitive outcomes.…”

“…Endosymbiotic dinoflagellates from the genetically diverse lineage Symbiodiniaceae [4] supply the majority of a coral's energy (carbon; [5]) and growth (nitrogen; [6,7]) resources through photosynthesis and tight recycling of the host's metabolic waste. Indeed, emerging evidence suggests that host modulation of nitrogen to the symbionts keeps them in a nitrogen-limited state [8]-a condition which is well-known to slow cell division and induce the accumulation of carbohydrates and lipid compounds with relatively high C:N ratios in marine phytoplankton [9,10]. While coral species/individuals tend to associate with one or a few predictable, dominant symbiodinians, these associations can vary with depth (light availability) and temperature.…”