Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades

Abstract

Many reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. There is increasing evidence of functional significance to Symbiodinium diversity, which affects the coral holobiont's response to changing environmental conditions. For example, corals hosting Symbiodinium from the clade D taxon exhibit greater resistance to heat-induced coral bleaching than conspecifics hosting the more common clade C. Yet, the relatively low prevalence of clade D suggests that this trait is not advantageous in non-stressful environments. Thus, clade D may only be able to out-compete other Symbiodinium types within the host habitat when conditions are chronically stressful. Previous studies have observed enhanced photosynthesis and fitness by clade C holobionts at non-stressful temperatures, relative to clade D. Yet, carbon-centered metrics cannot account for enhanced growth rates and patterns of symbiont succession to other genetic types when nitrogen often limits reef productivity. To investigate the metabolic costs of hosting thermally tolerant symbionts, we examined the assimilation and translocation of inorganic (15)N and (13)C in the coral Acropora tenuis experimentally infected with either clade C (sub-type C1) or D Symbiodinium at 28 and 30 °C. We show that at 28 °C, C1 holobionts acquired 22% more (15)N than clade D. However, at 30 °C, C1 symbionts acquired equivalent nitrogen and 16% less carbon than D. We hypothesize that C1 competitively excludes clade D in hospite via enhanced nitrogen acquisition and thus dominates coral populations despite warming oceans.

Figure 1

Mean AP¹³C (a, c) and AP¹⁵N (b, d) in clade C1 and D Symbiodinium (symbiont fractions) sampled during a 12-h incubation with ¹⁵NO₃⁻ and H¹³CO₃⁻. Left panels represent the ambient (28 °C) temperature treatment and right panels show results from the elevated (30 °C) treatment. Error bars represent 95% credible intervals (Bayesian). (*) Indicates significantly higher isotope assimilation between clades within each temperature treatment and (‡) represents a significant difference between temperature treatments within a clade as determined by no overlap of the 95% credible intervals.

Figure 2

Mean AP¹³C (a, c) and AP¹⁵N (b, d) of A. tenuis host fractions hosting either clade C1 or D Symbiodinium, sampled during a 12-hour incubation with H¹³CO₃⁻ and ¹⁵NO₃⁻. Left panels represent the ambient (28 °C) temperature treatment and right panels show results of the elevated (30 °C) treatment. Error bars represent 95% credible intervals (Bayesian). (*) Indicates significantly higher isotope assimilation within each temperature treatment and sampling time as determined by no overlap of the 95% credible intervals between clades.