Genetic diversity of free-living Symbiodinium in the Caribbean: the importance of habitats and seasons

Abstract

Although reef corals are dependent of the dinoflagellate Symbiodinium, the large majority of corals spawn gametes that do not contain their vital symbiont. This suggests the existence of a pool of Symbiodinium in the environment, of which surprisingly little is known. Reefs around Curaçao (Caribbean) were sampled for freeliving Symbiodinium at three time periods (summer 2009, summer 2010, and winter 2010) to characterize different habitats (water column, coral rubble, sediment, the macroalgae Halimeda spp., Dictyota spp., and Lobophora variegata, and the seagrass Thalassia testudinum) that could serve as environmental sources of symbionts for corals. We detected the common clades of Symbiodinium that engage in symbiosis with Caribbean coral hosts A, B, and C using Symbiodinium-specific primers of the hypervariable region of the chloroplast 23S ribosomal DNA gene. We also discovered clade G and, for the first time in the Caribbean, the presence of free-living Symbiodinium clades F and H. Additionally, this study expands the habitat range of free-living Symbiodinium as environmental Symbiodinium was detected in T. testudinum seagrass beds. The patterns of association between free-living Symbiodinium types and habitats were shown to be complex. An interesting, strong association was seen between some clade A sequence types and sediment, suggesting that sediment could be a niche where clade A radiated from a free-living ancestor. Other interesting relationships were seen between sequence types of Symbiodinium clade C with Halimeda spp. and clades B and F with T. testudinium. These relationships highlight the importance of some macroalgae and seagrasses in hosting free-living Symbiodinium. Finally, studies spanning beyond a 1-yr cycle are needed to further expand on our results in order to better understand the variation of Symbiodinium in the environment through time. All together, results presented here showed that the great diversity of free-living Symbiodinium has a dynamic distribution across habitats and time.

Worldwide Occurrence and Activity of the Reef-Building Coral Symbiont Symbiodinium in the Open Ocean

“…Clade C was the dominant Symbiodinium lineage (73%), with a lower contribution of clade A (18%), compared to pelagic waters, followed by clade D (2.6%). In the smallest size fraction, the presence of clades C and A (60% and 31%, respectively) corroborates previous tropical reef studies showing the presence of free-living clade C (the most speciose and common clade of symbionts of reef-building corals [22,29]) and clade A in reefs' water columns and sediment [10,11,[30][31][32]. The other clades (B, D, F, and G) were relatively more prevalent in reef waters (4.5% of Symbiodinium reads) than open oceans (1.7%), particularly in larger size fractions ( Figure 2A).…”

Chronic disturbance modulates symbiont (Symbiodiniaceae) beta diversity on a coral reef

“…Symbiodiniaceae in the environment may also provide a source for adult corals to take up new symbionts after disturbance and bleaching 37,38 , but the frequency and ecological relevance of this uptake is contested 39,40 . Symbiodiniaceae found in the environment ("free-living Symbiodiniaceae") occur in several different reef habitat "compartments", including sediment, the water column, and as epiphytes on macroalgae and seagrass [41][42][43][44] . These free-living Symbiodiniaceae can be divided into two categories: (1) "exclusively free-living Symbiodiniaceae" are those that do not participate in symbioses with eukaryotic hosts 45 ; (2) "transiently free-living Symbiodiniaceae" are typically associated with invertebrate hosts but can be transient in the environment 46,47 .…”

What will it take to understand the ecology of symbiotic microorganisms?

“…As mentioned earlier, experiments that include manipulation of hosts, especially host exclusion, will be very informative to our understanding of the ecology of symbiotic microorganisms. For many systems, the free-living populations of symbiotic microorganisms are apparently restricted to the immediate environs of their hosts (Lee and Ruby, 1994;Granados-Cifuentes et al, 2015;van Elsas et al, 2011). These observations are commonly interpreted as evidence that the symbiotic microorganisms are short-lived in the external environment, raising the possibility that their free-living populations are sink populations maintained by microbial cells shed from hosts, that is, the persistence of the free-living populations is dependent on cycling between hosts and the external environment with population amplification in hosts (Adair and Douglas, 2017).…”