Formal recognition of host-generalist species of dinoflagellate (Cladocopium, Symbiodiniaceae) mutualistic with Indo-Pacific reef corals.

The existence of widespread species with the capacity to endure diverse, or variable, environments are of importance to ecological and genetic research, and conservation. Such "ecological generalists" are more likely to have key adaptations that allow them to better tolerate the physiological challenges of rapid climate change. Reef-building corals are dependent on endosymbiotic dinoflagellates (Family: Symbiodiniaceae) for their survival and growth. While these symbionts are biologically diverse, certain genetic types appear to have broad geographic distributions and are mutualistic with various host species from multiple genera and families in the order Scleractinia that must acquire their symbionts through horizontal transmission. Despite the considerable ecological importance of putative host-generalist symbionts, they lack formal species descriptions. In this study, we used molecular, ecological, and morphological evidence to verify the existence of five new host-generalist species in the symbiodiniacean genus Cladocopium. Their geographic distribution and prevalence among host communities corresponds to prevailing environmental conditions at both regional and local scales. The influence that each species has on host physiology may partially explain regional differences in thermal sensitivities among coral communities. The potential increased prevalence of a generalist species that endures environmental instability is a consequential ecological response to warming oceans. Large-scale shifts in symbiont dominance could ensure reef coral persistence and productivity in the near term. Ultimately, these formal designations should advance scientific communication and generate informed research questions on the physiology and ecology of coral-dinoflagellate mutualisms.

Comparative Genomic Insights into Bacterial Induction of Larval Settlement and Metamorphosis in the Upside-Down Jellyfish Cassiopea.

Bacteria are important mediators of the larval transition from pelagic to benthic environments for marine organisms. Bacteria can therefore dictate species distribution and success of an individual. Despite the importance of marine bacteria to animal ecology, the identity of inductive microbes for many invertebrates are unknown. Here, we report the first successful isolation of bacteria from natural substrates capable of inducing settlement and metamorphosis of the planula larvae stage of a true jellyfish, the upside-down jellyfish Cassiopea xamachana. Inductive bacteria belonged to multiple phyla, with various capacity to induce settlement and metamorphosis. The most inductive isolates belonged to the genus Pseudoalteromonas, a marine bacterium known to induce the pelago-benthic transition in other marine invertebrates. In sequencing the genome of the isolated Pseudoalteromonas and a semiinductive Vibrio, we found biosynthetic pathways previously implicated in larval settlement were absent in Cassiopea inducing taxa. We instead identified other candidate biosynthetic gene clusters involved in larval metamorphosis. These findings could provide hints to the ecological success of C. xamachana compared to sympatric congeneric species within mangrove environments and provide avenues to investigate the evolution of animal-microbe interactions. IMPORTANCE The pelagic to benthic transition for the larvae of many marine invertebrate species are thought to be triggered by microbial cues. The microbial species and exact cue that initiates this transition remains unknown for many animals. Here, we identify two bacterial species, a Pseudoalteromonas and a Vibrio, isolated from natural substrate that induce settlement and metamorphosis of the upside-down jellyfish Cassiopea xamachana. Genomic sequencing revealed both isolates lacked genes known to induce the life history transition in other marine invertebrates. Instead, we identified other gene clusters that may be important for jellyfish settlement and metamorphosis. This study is the first step to identifying the bacterial cue for C. xamachana, an ecologically important species to coastal ecosystems and an emerging model system. Understanding the bacterial cues provides insight into marine invertebrate ecology and evolution of animal-microbe interactions.

Molecular composition and biodegradation of loggerhead sponge Spheciospongia vesparium exhalent dissolved organic matter.

Sponges are critical components of marine reefs due to their high filtering capacity, wide abundance, and alteration of biogeochemical cycling. Here, we characterized dissolved organic matter (DOM) composition in the sponge holobiont exhalent seawater of a loggerhead sponge (Spheciospongia vesparium) and in ambient seawater in Florida Bay (USA), as well as the microbial responses to each DOM pool through dark incubations. The sponge holobiont removed 6% of the seawater dissolved organic carbon (DOC), utilizing compounds that were low in carbon and oxygen, yet high in nitrogen content relative to the ambient seawater. The microbial community accessed 7% of DOC from the ambient seawater during a 5-day incubation but only 1% of DOC from the sponge exhalent seawater, suggesting a decrease in lability possibly due to holobiont removal of nitrogen-rich compounds. If this holds true for other sponges, it may have important implications for DOM lability and cycling in coastal environments.

Internal carbonic anhydrase activity in the tissue of scleractinian corals is sufficient to support proposed roles in photosynthesis and calcification.

Reef-building corals import inorganic carbon (Ci) to build their calcium carbonate skeletons and to support photosynthesis by the symbiotic algae that reside in their tissue. The internal pathways that deliver Ci for both photosynthesis and calcification are known to involve the enzyme carbonic anhydrase (CA), which interconverts CO2 and HCO3 (-). We have developed a method for absolute quantification of internal CA (iCA) activity in coral tissue based on the rate of (18)O-removal from labeled Ci. The method was applied to three Caribbean corals (Orbicella faveolata, Porites astreoides and Siderastrea radians) and showed that these species have similar iCA activities per unit surface area, but that S. radians has ∼10-fold higher iCA activity per unit tissue volume. A model of coral Ci processing shows that the measured iCA activity is sufficient to support the proposed roles for iCA in Ci transport for photosynthesis and calcification. This is the case even when iCA activity is homogeneously distributed throughout the coral, but the model indicates that it would be advantageous to concentrate iCA in the spaces where calcification (the calcifying fluid) and photosynthesis (the oral endoderm) take place. We argue that because the rates of photosynthesis and calcification per unit surface area are similar among the corals studied here, the areal iCA activity used to deliver Ci for these reactions should also be similar. The elevated iCA activity per unit volume of S. radians compared with that of the other species is probably due to the thinner effective tissue thickness in this species.

A connection between colony biomass and death in Caribbean reef-building corals.

Increased sea-surface temperatures linked to warming climate threaten coral reef ecosystems globally. To better understand how corals and their endosymbiotic dinoflagellates (Symbiodinium spp.) respond to environmental change, tissue biomass and Symbiodinium density of seven coral species were measured on various reefs approximately every four months for up to thirteen years in the Upper Florida Keys, United States (1994-2007), eleven years in the Exuma Cays, Bahamas (1995-2006), and four years in Puerto Morelos, Mexico (2003-2007). For six out of seven coral species, tissue biomass correlated with Symbiodinium density. Within a particular coral species, tissue biomasses and Symbiodinium densities varied regionally according to the following trends: Mexico≥Florida Keys≥Bahamas. Average tissue biomasses and symbiont cell densities were generally higher in shallow habitats (1-4 m) compared to deeper-dwelling conspecifics (12-15 m). Most colonies that were sampled displayed seasonal fluctuations in biomass and endosymbiont density related to annual temperature variations. During the bleaching episodes of 1998 and 2005, five out of seven species that were exposed to unusually high temperatures exhibited significant decreases in symbiotic algae that, in certain cases, preceded further decreases in tissue biomass. Following bleaching, Montastraea spp. colonies with low relative biomass levels died, whereas colonies with higher biomass levels survived. Bleaching- or disease-associated mortality was also observed in Acropora cervicornis colonies; compared to A. palmata, all A. cervicornis colonies experienced low biomass values. Such patterns suggest that Montastraea spp. and possibly other coral species with relatively low biomass experience increased susceptibility to death following bleaching or other stressors than do conspecifics with higher tissue biomass levels.

Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals.

BACKGROUND: The dinoflagellate genus Symbiodinium forms symbioses with numerous protistan and invertebrate metazoan hosts. However, few data on symbiont genetic structure are available, hindering predictions of how these populations and their host associations will fair in the face of global climate change. METHODOLOGY/PRINCIPAL FINDINGS: Here, Symbiodinium population structure from two of the Caribbean's ecologically dominant scleractinian corals, Montastraea faveolata and M. annularis, was examined. Tagged colonies on Florida Keys and Bahamian (i.e., Exuma Cays) reefs were sampled from 2003-2005 and their Symbiodinium diversity assessed via internal transcribed spacer 2 (ITS2) rDNA and three Symbiodinium Clade B-specific microsatellite loci. Generally, the majority of host individuals at a site harbored an identical Symbiodinium ITS2 "type" B1 microsatellite genotype. Notably, symbiont genotypes were largely reef endemic, suggesting a near absence of dispersal between populations. Relative to the Bahamas, sympatric M. faveolata and M. annularis in the Florida Keys harbored unique Symbiodinium populations, implying regional host specificity in these relationships. Furthermore, within-colony Symbiodinium population structure remained stable through time and environmental perturbation, including a prolonged bleaching event in 2005. CONCLUSIONS/SIGNIFICANCE: Taken together, the population-level endemism, specificity and stability exhibited by Symbiodinium raises concerns about the long-term adaptive capacity and persistence of these symbioses in an uncertain future of climate change.

Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians.

Photoinhibition, exacerbated by elevated temperatures, underlies coral bleaching, but sensitivity to photosynthetic loss differs among various phylotypes of Symbiodinium, their dinoflagellate symbionts. Symbiodinium is a common symbiont in many cnidarian species including corals, jellyfish, anemones, and giant clams. Here, we provide evidence that most members of clade A Symbiodinium, but not clades B-D or F, exhibit enhanced capabilities for alternative photosynthetic electron-transport pathways including cyclic electron transport (CET). Unlike other clades, clade A Symbiodinium also undergo pronounced light-induced dissociation of antenna complexes from photosystem II (PSII) reaction centers. We propose these attributes promote survival of most cnidarians with clade A symbionts at high light intensities and confer resistance to bleaching conditions that conspicuously impact deeper dwelling corals that harbor non-clade A Symbiodinium.

CORRESPONDENCE BETWEEN COLD TOLERANCE AND TEMPERATE BIOGEOGRAPHY IN A WESTERN ATLANTIC SYMBIODINIUM (DINOPHYTA) LINEAGE(1).

Many corals form obligate symbioses with photosynthetic dinoflagellates of the genus Symbiodinium Freudenthal (1962). These symbionts vary genotypically, with their geographical distribution and abundance dependent upon host specificity and tolerance to temperature and light variation. Despite the importance of these mutualistic relationships, the physiology and ecology of Symbiodinium spp. remain poorly characterized. Here, we report that rDNA internal transcribed spacer region 2 (ITS2) defined Symbiodinium type B2 associates with the cnidarian hosts Astrangia poculata and Oculina arbuscula from northerly habitats of the western Atlantic. Using pulse-amplitude-modulated (PAM) fluorometry, we compared maximum photochemical efficiency of PSII of type B2 to that of common tropical Symbiodinium lineages (types A3, B1, and C2) under cold-stress conditions. Symbiont cultures were gradually cooled from 26°C to 10°C to simulate seasonal temperature declines. Cold stress decreased the maximum photochemical efficiency of PSII and likely the photosynthetic potential for all Symbiodinium clades tested. Cultures were then maintained at 10°C for a 2-week period and gradually returned to initial conditions. Subsequent to low temperature stress, only type B2 displayed rapid and full recovery of PSII photochemical efficiency, whereas other symbiont phylotypes remained nonfunctional. These findings indicate that the distribution and abundance of Symbiodinium spp., and by extension their cnidarian hosts, in temperate climates correspond significantly with the photosynthetic cold tolerance of these symbiotic algae.

Patterns of inorganic phosphate uptake in Cassiopea xamachana: a bioindicator species.

Nutrient levels in the nearshore waters of the Florida Keys have increased over the past few decades concomitant with a decline in the health of Florida's reef system. Phosphorus is a particular concern in the Florida Keys as it may be the limiting nutrient in nearshore waters. We demonstrate that the upside-down jellyfish, Cassiopea xamachana, decreases its rate of phosphate uptake following exposure to elevated levels of dissolved inorganic phosphate. We also show that this subsequent suppression of uptake rates persists for some time following exposure to elevated phosphates. Using these attributes, we experimentally investigated the use of C. xamachana as a bioindicator for dissolved inorganic phosphates in seawater. Our results show that these animals reveal comparative differences in environmental phosphates despite traditional testing methods yielding no detectable phosphates. We propose that C. xamachana is a bioindicator useful for integrating relevant information about phosphate availability in low nutrient environments.