Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians
2006; Elsevier BV; Volume: 16; Issue: 23 Linguagem: Inglês
10.1016/j.cub.2006.10.049
ISSN1879-0445
AutoresMary Alice Coffroth, Cynthia F. Lewis, Scott R. Santos, Jessica Weaver,
Tópico(s)Marine and coastal plant biology
ResumoInvertebrate–dinoflagellate symbioses are responsible for the high productivity and structural complexity of the coral reef ecosystem. Coral reefs around the world are in decline with much of the mortality attributed to coral bleaching — the loss of photosynthetic algal symbionts — resulting from global warming [1Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs.Mar. Freshwater Res. 1999; 50: 839-866Crossref Scopus (2453) Google Scholar, 2Hughes T.P. Baird A.H. Bellwood D.R. Card M. Connolly S.R. Folke C. Grosberg R. Hoegh-Guldberg O. Jackson J.B.C. Kleypas J. et al.Climate change, human impacts, and the resilience of coral reefs.Science. 2003; 301: 929-933Crossref PubMed Scopus (2555) Google Scholar, 3Graham N.A.J. Wilson S.K. Jennings S. Polunin N.V.C. Bijoux J.P. Robinson J. Dynamic fragility of oceanic coral reef ecosystems.Proc. Natl. Acad. Sci. USA. 2006; 101: 8251-8253Google Scholar]. These algae are essential to a host's survival, but many cnidarians must acquire their symbionts, members of the genus Symbiodinium referred to as zooxanthellae, anew at each generation. The presence of zooxanthellate corals on reefs, and the rapid acquisition of Symbiodinium by newly settled polyps ('recruits') in the field [4Coffroth M.A. Santos S.R. Goulet T.L. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis.Mar. Ecol. Prog. Ser. 2001; 222: 85-96Crossref Scopus (126) Google Scholar], imply the existence of an external supply of Symbiodinium. 'Symbiodinium-like' dinoflagellates have been isolated from both sand and the water column [5Loeblich III, A.R. Sherley J.L. Observations on the theca of the mobile phase of free-living and symbiotic isolates of Zooxanthella microadriaticum (Freudenthal) Comb. nov.J. Mar. Biol. Ass. UK. 1979; 59: 195-205Crossref Scopus (83) Google Scholar, 6Chang F.H. Winter phytoplankton and microzooplankton populations off the coast of Westland, New Zealand.N.Z.J. Mar. Freshw. Res. 1983; 17: 279-304Crossref Scopus (45) Google Scholar, 7Gou W. Sun J. Li X. Zhen Y. Xin Z. Yu Z. Li R. Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaohou Bay, P.R. China.J. Exp. Mar. Biol. Ecol. 2003; 296: 135-144Crossref Scopus (41) Google Scholar, 8Carlos A.A. Baillie B.K. Kawachi M. Maruyama T. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain.J. Phycol. 1999; 35: 1054-1062Crossref Scopus (183) Google Scholar], but neither the location(s) nor the dynamics of this symbiont reservoir are known. To understand how corals may respond to current threats on local and global scales, such as overfishing and global warming, respectively, and to successfully manage and protect potential symbiont sources that may repopulate reef corals, we need to identify the location of Symbiodinium in the environment and, more importantly, demonstrate that these populations are capable of establishing symbioses. Here, we confirm the presence of Symbiodinium within the water column and the benthos, and show that these environmentally derived isolates are able to infect cnidarian (octocoral) recruits. Symbiont change has been proposed to occur in stressful environments [9Buddemeier R.W. Fautin D.C. Coral bleaching as an adaptive mechanism.Bioscience. 1993; 43: 322-326Crossref Google Scholar, 10Baker A.C. Reef corals bleach to survive.Nature. 2001; 411: 765-766Crossref PubMed Scopus (341) Google Scholar], but it is unclear whether these repopulating symbionts are from a residual population within the host or from an exogenous source. 'Symbiodinium-like' dinoflagellates have been isolated from the water column [5Loeblich III, A.R. Sherley J.L. Observations on the theca of the mobile phase of free-living and symbiotic isolates of Zooxanthella microadriaticum (Freudenthal) Comb. nov.J. Mar. Biol. Ass. UK. 1979; 59: 195-205Crossref Scopus (83) Google Scholar, 6Chang F.H. Winter phytoplankton and microzooplankton populations off the coast of Westland, New Zealand.N.Z.J. Mar. Freshw. Res. 1983; 17: 279-304Crossref Scopus (45) Google Scholar, 7Gou W. Sun J. Li X. Zhen Y. Xin Z. Yu Z. Li R. Phylogenetic analysis of a free-living strain of Symbiodinium isolated from Jiaohou Bay, P.R. China.J. Exp. Mar. Biol. Ecol. 2003; 296: 135-144Crossref Scopus (41) Google Scholar] and benthic environments [8Carlos A.A. Baillie B.K. Kawachi M. Maruyama T. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain.J. Phycol. 1999; 35: 1054-1062Crossref Scopus (183) Google Scholar], and phylogenetic analyses of a dinoflagellate isolated from sand on Oahu, Hawaii [8Carlos A.A. Baillie B.K. Kawachi M. Maruyama T. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain.J. Phycol. 1999; 35: 1054-1062Crossref Scopus (183) Google Scholar] show that this isolate (Symbiodinium HA3-5) is allied with Clade A, but lays outside the members of the clade known to establish symbioses with cnidarians (Figure 1). Although these 'free-living' forms fall within the genus Symbiodinium, or are closely allied, it remains to be established whether they are capable of a symbiotic lifestyle, an essential criterion for identifying the source of potentially repopulating symbionts. To this end, we sampled Symbiodinium from the water column 20 metres above the reef using asymbiotic octocoral recruits (Briareum sp.) as 'symbiont sampler arrays'. Symbiodinium were detected within all polyps, establishing their presence in the water column. Symbiodinium Clades A, B and C were identified in 7%, 63% and 2% of the polyps, respectively; an additional 28% of the polyps hosted multiple clades simultaneously (for example, A+B, 23%; B+C, 5%). We also established that Symbiodinium resides in benthic habitats by culturing 'Symbiodinium-like' dinoflagellates from reef rubble and from substrates placed at several sites in the Middle Florida Keys (see Table S1 in the Supplemental data available online). Over 380 cultures were established and molecular analyses of those containing dinoflagellate-like microorganisms confirmed their relationship to Symbiodinium (Table S2). Phylogenetic analyses of internal transcribed spacer (ITS) rDNA sequences from a subset of these cultures placed many within Symbiodinium (Figure 1); three of the isolates grouped within established Symbiodinium taxa (Figure 1): isolate 5196 had an identical sequence to AY074983 (Bermuda Cassiopeia[11Savage A.M. Goodson M.S. Visram S. Trapido R.H. Wiedenmann J. Douglas A.E. Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and anemones.Mar. Ecol. Prog. Ser. 2002; 244: 17-26Crossref Scopus (84) Google Scholar], Symbiodinium type A1), while isolate 4562 grouped closely with Symbiodinium type A1 and Symbiodinium of Bermuda Cassiopeia (0.2% difference from 5196, Table S5). Additionally, isolate 4404 belonged to Symbiodinium Clade B, being most similar to type B1 (0.8% difference, Table S6). Our study only identified members of Symbiodinium Clades A and B, and probably does not represent the true diversity of environmental populations. The inability to bring many Symbiodinium into culture is most likely due to these dinoflagellates being notoriously difficult to culture [12Santos S.R. Taylor D.J. Coffroth M.A. Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis.J. Phycol. 2001; 37: 900-912Crossref Scopus (133) Google Scholar]. However, other clades have been detected in the environment, although their ability to establish symbioses has not been tested (I. Porto and J. Sánchez, personal communication). Our sampling and culturing methods also recovered potentially non-symbiotic, 'Symbiodinium-like' isolates (5176, 5177, 5182, 5184, 5186 and 5870); phylogenetic analysis placed these within Symbiodinium Clade A along with types that have previously been characterized as 'free-living' (Figure 1A). Specifically, isolates 5177, 5186 and 5870 possessed identical ITS sequences to Symbiodinium HA3-5 (AF184948), the 'free-living' isolate from Hawaii [8Carlos A.A. Baillie B.K. Kawachi M. Maruyama T. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain.J. Phycol. 1999; 35: 1054-1062Crossref Scopus (183) Google Scholar]. We verified that these environmental populations of 'Symbiodinium-like' dinoflagellates are capable of establishing a symbiosis with cnidarians by exposing asymbiotic recruits to the environmental isolates and recovering the specific isolate used to inoculate the polyp in six of eight treatments (Table S3). Phylogenetic analysis of ITS sequences from a subset of these polyps verified that the Symbiodinium recovered from the polyps were identical to that of the cultures (eight cases) while in a single case, the isolate differed by a single nucleotide (Figure 2). Based on this, three isolates (4404, 4562 and 5196) successfully infected recruits, establishing that these environmental isolates, phylogenetically similar to Symbiodinium, are indeed capable of initiating a symbiosis (Figure 2). In two treatments, the dominant clade recovered did not correspond to the environmental isolate used as an inoculum (isolates 5177 and 5184, Table S3), although isolate 5184 was detected in one polyp following analysis of ITS sequences (Figure 2). These observations suggest that isolates allied with the 'free-living' Symbiodinium (Figure 1A) may not readily form symbioses. Our results show that a reservoir of Symbiodinium exists in the water column and the benthos. Recovering Symbiodinium from benthic substrates clarifies the mystery as to where these important symbionts reside outside of the host. Given the tendency of laboratory cultures of Symbiodinium to populate the bottom and sides of culture containers and undergo periodic motility into the 'water column' of the flask [13Fitt W.K. Chang S.S. Trench R.K. Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (= Gymnodinium) microadriaticum (Freudenthal) in culture.Bull. Mar. Sci. 1981; 31: 436-443Google Scholar], we propose that the intrinsic diurnal motility of the cells results in the movement of Symbiodinium from the benthos into the water column and ensures encounters with competent hosts. The environmental source of Symbiodinium that we have shown can infect cnidarian recruits is likely to be available to all reef-dwelling cnidarians and may prove important in the recovery of reef-building corals following bleaching events. Our results also show that not all Symbiodinium spp. isolated from the environment are capable of establishing symbioses with cnidarians. Future research should examine if these 'free-living' Symbiodinium can form symbioses with other, non-cnidarian hosts, determine whether environmental isolates that infect cnidarians are able to maintain the symbiosis in the field and test their competitive ability with other Symbiodinium types. Additional work is also needed to determine the physiological tolerances of these potential symbionts and if they represent a symbiont pool that might repopulate reef corals following temperature-induced (or other stress related) bleaching. We thank the FKNMS, Keys Marine Lab, Niagara Aquarium, Sherwood, L. Bright, M. Dorner, A. Hannes, L. Holland, N. Kirk, H. Lasker, G. May, M. Medina, A. Monteiro, T. Naeher, D. Poland, T. Shearer, A. Siegel, B. Spataro, J. Stamos and D. Taylor. This research was supported by the National Science Foundation (M.A.C.) Download .pdf (.08 MB) Help with pdf files Document S1. Supplemental Experimental Procedures and Six Tables
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