Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters (original) (raw)

Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals

Marine Biology, 2009

The establishment of symbiosis in early developmental stages is important for reef-building corals because of the need for photosynthetically derived nutrition. Corals spawn eggs and sperm, or brood planula larvae and shed them into the water. Some coral eggs or planulae directly inherit symbiotic dinoflagellates (Symbiodinium spp.) from their parents, while others acquire them at each generation. In most species examined to date, the larvae without dinoflagellates (aposymbiotic larvae) can acquire symbionts during the larval stage, but little is known regarding the timing and detailed process of the onset of symbiosis. We examined larval uptake of symbiotic dinoflagellates in nine species of scleractinian corals, the onset of symbiosis through the early larval stages, and the distribution pattern of symbionts within the larval host, while living and with histology, of two acroporid corals under laboratory conditions. The larvae acquired symbiotic dinoflagellates during the planktonic phase in all corals examined which included Acropora digitifera, A. florida, A. intermedia, A. tenuis, Isopora palifera, Favia pallida, F. lizardensis, Pseudosiderastrea tayamai, and Ctenactis echinata. The larvae of A. digitifera and A. tenuis first acquired symbionts 6 and 5 days after fertilization, respectively. In A. digitifera larvae, this coincided with the formation of an oral pore and coelenteron. The number of symbiotic dinoflagellates increased over the experimental periods in both species. To test the hypothesis that nutrients promotes symbiotic uptake, the number of incorporated dinoflagellates was compared in the presence and absence of homogenized Artemia sp. A likelihood ratio test assuming a log-linear model indicated that Artemia sp. had a significantly positive effect on symbiont acquisition. These results suggest that the acquisition of symbiotic dinoflagellates during larval stages is in common with many coral species, and that the development of both a mouth and coelenteron play important roles in symbiont acquisition.

Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus

Coral Reefs, 2008

Scleractinian corals may acquire Symbiodinium from their parents (vertically) or from the environment (horizontally). In the present study, adult colonies of the coral Acropora longicyathus from One Tree Island (OTI) on the southern Great Barrier Reef (Australia) acquired two distinct varieties of symbiotic dinoXagellates (Symbiodinium) from the environment. Adult colonies had either Symbiodinium from clade C (86.7%) or clade A (5.3%), or a mixture of both clades A and C (8.0% of all colonies). In contrast, all 10-day-old juveniles were associated with Symbiodinium from clade A, while 83-day-old colonies contained clades A, C and D even though they were growing at the same location. Symbiodinium from clade A were dominant in both 10-and 83-day-old juveniles (99 and 97% of all recruits, respectively), while clade D was also found in 31% of 83-day-old juveniles. Experimental manipulation also revealed that parental association (with clade A or C), or the location within the OTI reef, did not inXuence which clade of symbiont was acquired by juvenile corals. The diVerences between the genetic identity of populations of Symbiodinium resident in juveniles and adult A. longicyathus suggest that ontogenetic changes in the symbiosis may occur during the development of scleractinian corals. Whether or not these changes are due to host selective processes or diVerences in the physical environment associated with juvenile versus adult colonies remains to be determined.

Specificity of a Model Cnidarian-Dinoflagellate Symbiosis

To understand the flexibility of symbiotic associations in coral reefs, we investigated the specificity of the Aiptasia (cf. insignis)-Symbiodinium association in the laboratory by rendering the anemones aposymbiotic and inoculating them with different isolates of Symbiodinium. Infective algal symbionts were monitored over 3 months by re-isolation and identification using denaturing-gradient gel electrophoresis and sequence comparison of their amplified 18S rRNA hypervariable V1 ϩ V2 gene region. Despite similarity in their external morphology, the algal isolates differed in their infectivity towards the host. Within days of single-isolate inoculation, aposymbiotic anemones formed associations with fresh or cultured isolates (clade B) from the anemones Aiptasia sp. or A. tagetes, respectively. They associated to a limited extent with cultured isolates (clade A) from the tridacnids Tridacna crocea or Hippopus hippopus, and not at all with a cultured isolate (clade C) from the stony coral Montipora verrucosa, nor with a free-living isolate (clade A) from subtidal sands. Aposymbiotic anemones inoculated with a mixture of all isolates had only the anemone taxon as their detectable symbionts. Re-inoculation of induced symbioses with a mixture of all isolates and incubation with wild anemones showed that the initial induced symbioses with the anemone taxon were stable. Anemones originally infected with tridacnid isolates either additionally acquired the anemone taxon or had the former outgrown by the latter. These results demonstrate the pres-ence of a host-symbiont recognition mechanism, and possibly competition among potential algal symbionts in the Aiptasia-Symbiodinium association. Here we present a method that may be useful in monitoring the algal population dynamics in symbiotic corals in the field, along with an efficient method of rendering Aiptasia aposymbiotic for further laboratory investigation of Aiptasia-Symbiodinium symbioses.

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

Molecular Ecology, 2018

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef‐building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit...

Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium

Comparative Biochemistry and Physiology D-genomics & Proteomics, 2009

Dinoflagellates are ubiquitous marine and freshwater protists. The endosymbiotic relationship between dinoflagellates of the genus Symbiodinium (also known as zooxanthellae) and corals forms the basis of coral reefs. We constructed and analyzed a cDNA library from a cultured Symbiodinium species clade A (CassKB8). The majority of annotated ESTs from the Symbiodinium sp. CassKB8 library cover metabolic genes. Most of those belong to either carbohydrate or energy metabolism. In addition, components of extracellular signal transduction pathways and genes that play a role in cell-cell communication were identified. In a subsequent analysis, we determined all orthologous cDNA sequences between this library (1,484 unique sequences) and a library from a Symbiodinium species clade C (C3) (3,336 unique sequences) that was isolated directly from its symbiotic host. A set of 115 orthologs were identified between Symbiodinium sp. CassKB8 and Symbiodinium sp. C3. These orthologs were subdivided into three groups that show different characteristics and functions: conserved across eukaryotes (CE), dinoflagellate-specific (DS) and Symbiodinium-specific (SS). Orthologs conserved across eukaryotes are mainly comprised of housekeeping genes, photosynthesis-related transcripts and metabolic proteins, whereas the function for most of the dinoflagellate-specific orthologs remains unknown. A dN/dS analysis identified the highest ratio in a Symbiodinium-specific ortholog and evidence for positive selection in a dinoflagellate-specific gene. Evolution of genes and pathways in different dinoflagellates seems to be affected by different lifestyles, and a symbiotic lifestyle may affect population structure and strength of selection. This study is the first evolutionary comparative analysis of orthologs from two coral dinoflagellate symbionts.

Do clades of symbiotic dinoflagellates in scleractinian corals of the Gulf of Eilat (Red Sea) differ from those of other coral reefs?

Journal of Experimental Marine Biology and Ecology, 2004

The symbiotic association between corals and zooxanthellae has been a major contributing factor in the success of reef-building corals. Most of these endocellular microalgal symbionts belong to the dinoflagellate genus Symbiodinium. However, considerable genetic diversity was revealed within this taxon, as is evident in the several clades of Symbiodinium found in association with hermatypic corals all over the world. The coral reefs of Eilat (Aqaba), where winter temperature minima of 21 jC are close to threshold values that prevent reef development, are among the northernmost reefs in the world. Furthermore, due to the circulation patterns of the Gulf, the extremely high evaporation, and lack of any riverine inputs, the Gulf's waters are highly saline (40.5x). In spite of the extreme location, a high diversity of coral species has been reported in this area. In this study, using PCR, we specifically amplified zooxanthellae 18S ribosomal DNA from symbionts of 11 coral species, and analyzed it with respect to RFLP and DNA sequence.

Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis

Marine Ecology Progress Series, 2004

This study aimed at determining whether fine-scale molecular diversity of Symbiodinium corresponds to functional differences in host/symbiont specificity during the onset of symbiosis in cnidarian/alga mutualisms. Infection experiments were conducted in aposymbiotic larvae of the scleractinian Fungia scutaria using known algal Internal Transcribed Spacer (ITS)-2 types within Clade C. Our results show that algal type is directly related to specificity during the onset of symbiosis in F. scutaria larvae. The 3 ITS symbiont types (C 1f, C 15 and C 31) within the major Symbiodinium Clade C engaged differentially in symbiosis with coral larvae. The homologous symbiont (C 1f), found in adult F. scutaria from the field, showed a significantly better association with the host larvae than the other 2 heterologous symbionts (C 15 extracted from Porites compressa, and C 31 from Montipora capitata). This is the first evidence that fine-scale ITS diversity of Symbiodinium confers functionality in the symbiosis.