Symbiodinium photosynthesis in Caribbean octocorals

Abstract

Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. Symbiodinium associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm2 but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in Symbiodinium photosynthetic performance could not be attributed to Symbiodinium type. All P. anceps (n = 9) and P. wagenaari (n = 6) colonies, in addition to one E. tourneforti and three P. porosa colonies, associated with Symbiodinium type B1. The B1 Symbiodinium from these four gorgonian species did not cluster with lineages of B1 Symbiodinium from scleractinian corals. The remaining eight E. tourneforti colonies harbored Symbiodinium type B1L, while six P. porosa colonies harbored type B1i. Understanding the symbioses between gorgonian corals and Symbiodinium will aid in deciphering why gorgonian corals dominate many Caribbean reefs.

Figure 1. In hospite net photosynthesis-irradiance (P-E) curves from four Caribbean gorgonian species.

(A) P-E curves per cm² of gorgonian branches and, (B) P-E curves per Symbiodinium cell. Solid lines represent the average fitted values for Pterogorgia anceps (n = 9), Eunicea tourneforti (n = 8), Pseudoplexaura porosa (n = 6), and Pseudoplexaura wagenaari (n = 6). Dotted lines represent ± standard error. The photosynthetic rate at 1800 µmol quanta was used as a proxy for the maximum photosynthetic rate.

Figure 2. Symbiodinium parameters in four Caribbean gorgonian species.

(A) Cell densities and, (B) Concentration of chlorophylls a (circles) and c ₂ (squares) per Symbiodinium cell. Points represent sample means ± standard error. Gorgonian species that do not share a letter are significantly different from each other in either density or chlorophyll a per cell (α = 0.05, see Figure 1 for full species names and sample sizes). See Table 3 for significant differences in chlorophyll c ₂ per cell.

Figure 3. Estimated absorbance spectra, D_e (A), and Chlorophyll a specific absorption, a*_{chl a} (B) in four Caribbean gorgonian species.

Pterogorgia anceps (red line; n = 9), Eunicea tourneforti (green line; n = 8), Pseudoplexaura porosa (blue line; n = 6), and Pseudoplexaura wagenaari (purple line; n = 6). Lines in (A) represent average D_e spectra for each species. The equation for the line in (B) is y = 0.7586*(x^−0.8976).

Figure 4. A maximum likelihood phylogenetic tree based on microsatellite flanking regions of B1 Symbiodinium.

The phylogeny includes B1 Symbiodinium from the four gorgonian species in this study (highlighted in gray), from other gorgonian corals , from scleractinian and hydrozoan corals , as well as Symbiodinium minutum from Aiptasia, a sea anemone . Branch tips are labeled with host species and sample sizes when n>1. Gorgonian and scleractinian coral species are shown in black and red, respectively, and the other cnidarians are shown in blue. B1 lineages described by Finney et al. are listed besides the host taxa. Numbers above the branches are the posterior probability above the maximum likelihood consensus support for each group. B1 Symbiodinium from 16 of 19 gorgonian colonies sampled clustered in a phylogenetic group with high posterior probability (top gray box). Three gorgonian colonies were placed outside of this clade (bottom gray box) and were most closely related to Symbiodinium isolated from Pseudoplexaura porosa from Florida (indicated with (+1)) and cultured Symbiodinium from Gorgonia ventalina indicated with *. (#) indicates a group recovered in the maximum likelihood tree, but not the Bayesian phylogenetic tree.