Biogeography of the endosymbiotic dinoflagellates (Symbiodiniaceae) community associated with the brooding coral Favia gravida in the Atlantic Ocean

Abstract

Zooxanthellate corals live in symbiosis with phototrophic dinoflagellates of the family Symbiodiniaceae, enabling the host coral to dwell in shallow, nutrient-poor marine waters. The South Atlantic Ocean is characterized by low coral diversity with high levels of endemism. However, little is known about coral-dinoflagellate associations in the region. This study examined the diversity of Symbiodiniaceae associated with the scleractinian coral Favia gravida across its distributional range using the ITS-2 marker. This brooding coral endemic to the South Atlantic can be found across a wide range of latitudes and longitudes, including the Mid-Atlantic islands. Even though it occurs primarily in shallower environments, F. gravida is among the few coral species that live in habitats with extreme environmental conditions (high irradiance, temperature, and turbidity) such as very shallow tide pools. In the present study, we show that F. gravida exhibits some degree of flexibility in its symbiotic association with zooxanthellae across its range. F. gravida associates predominantly with Cladocopium C3 (ITS2 type Symbiodinium C3) but also with Symbiodinium A3, Symbiodinium linucheae (ITS2 type A4), Cladocopium C1, Cladocopium C130, and Fugacium F3. Symbiont diversity varied across biogeographic regions (Symbiodinium A3 and S. linucheae were found in the Tropical Eastern Atlantic, Cladocopium C1 in the Mid-Atlantic, and other subtypes in the Southwestern Atlantic) and was affected by local environmental conditions. In addition, Symbiodiniaceae diversity was highest in a southwestern Atlantic oceanic island (Rocas Atoll). Understanding the relationship between corals and their algal symbionts is critical in determining the factors that control the ecological niches of zooxanthellate corals and their symbionts, and identifying host-symbiont pairs that may be more resistant to environmental changes.

Fig 1. Sampling sites and geographic distribution of dominant endosymbiotic dinoflagellates associated with Favia gravida in the Southern Atlantic Ocean.

Numerals inside the circles indicate the number of colonies found associated with the respective endosymbiont lineages. Tropical Eastern Atlantic: ST = São Tomé; Mid-Atlantic: ASC = Ascension Island; Southwestern Atlantic: CE = Ceará, RA = Rocas Atoll, FN = Fernando de Noronha, RN = Rio Grande do Norte, PB = Paraíba, PE = Pernambuco, AL = Alagoas, PS = Porto Seguro (Bahia), AB = Abrolhos (Bahia), and TR = Trindade Island.

Fig 2. Proportion of each Symbiodiniaceae lineages per depth at sampling sites with more than one subtype.

Fig 3. Bayesian phylogenetic tree based on Symbiodiniaceae ITS2 sequences of Cladocopium spp.

(a), Symbiodinium spp. (b), and Fugacium spp. (c). Posterior probability distributions and bootstrap values of 1,000 replicates from maximum-likelihood analysis are shown for branch support. GenBank accession numbers are indicated on the tree. Sampling site abbreviations from this study are explained in Fig 1. Colors represent biogeographic regions: dark green = Northwestern Atlantic, light green = Caribbean, black = Southwestern Atlantic, pink = Mid-Atlantic, yellow = Tropical Eastern Atlantic, blue = Red Sea, red = Pacific Ocean, and orange = Indian Ocean.

Fig 4. Median-joining haplotype network of endosymbiotic dinoflagellates Symbiodinium spp.

(a), Cladocopium spp. (b) and Fugacium spp. (c) with sequences from this study and from the GenBank. Black dashes correspond to mutational events.