Symbiont shuffling during thermal bleaching and recovery in the sea anemone Entacmaea quadricolor (original) (raw)
Related papers
Anemone bleaching increases the metabolic demands of symbiont anemonefish
Proceedings. Biological sciences, 2018
Increased ocean temperatures are causing mass bleaching of anemones and corals in the tropics worldwide. While such heat-induced loss of algal symbionts (zooxanthellae) directly affects anemones and corals physiologically, this damage may also cascade on to other animal symbionts. Metabolic rate is an integrative physiological trait shown to relate to various aspects of organismal performance, behaviour and locomotor capacity, and also shows plasticity during exposure to acute and chronic stressors. As climate warming is expected to affect the physiology, behaviour and life history of animals, including ectotherms such as fish, we measured if residing in bleached versus unbleached sea anemones () affected the standard (i.e. baseline) metabolic rate and behaviour (activity) of juvenile orange-fin anemonefish () Metabolic rate was estimated from rates of oxygen uptake [Formula: see text], and the standard metabolic rate [Formula: see text] of anemonefish from bleached anemones was sig...
Anemonefish facilitate bleaching recovery in a host sea anemone
Scientific Reports
Ocean warming is causing the symbioses between cnidarians and their algal symbionts to breakdown more frequently, resulting in bleaching. For sea anemones, nutritional benefits derived from hosting anemonefishes increase their algal symbiont density. The sea anemone-anemonefish relationship could, therefore, facilitate bleaching recovery. To test this, bleached and unbleached sea anemones, both with and without anemonefish, were monitored in the laboratory. At the start of our experiment, algal symbiont density and colour score were lower in the bleached than unbleached sea anemones, whereas total chlorophyll remained similar. After 106 days, bleached sea anemones with anemonefish had an algal symbiont density and colour score equal to the controls (unbleached sea anemones and without anemonefish), indicating recovery had occurred. Furthermore, total chlorophyll was 66% higher in the bleached sea anemones with anemonefish than the controls. In contrast, recovery did not occur for th...
Frontiers in Microbiology, 2020
The ability of some symbiotic cnidarians to resist and better withstand stress factors that cause bleaching is a trait that is receiving increased attention. The adaptive bleaching hypothesis postulates that cnidarians that can form a stable symbiosis with thermotolerant Symbiodiniaceae strains may cope better with increasing seawater temperatures. We used polyps of the scyphozoan, Cassiopea xamachana, as a model system to test symbiosis success under heat stress. We sought to determine: (1) if aposymbiotic C. xamachana polyps could establish and maintain a symbiosis with both native and non-native strains of Symbiodiniaceae that all exhibit different tolerances to heat, (2) whether polyps with these newly acquired Symbiodiniaceae strains would strobilate (produce ephyra), and (3) if thermally tolerant Symbiodiniaceae strains that established and maintained a symbiosis exhibited greater success in response to heat stress (even if they are not naturally occurring in Cassiopea). Following recolonization of aposymbiotic C. xamachana polyps with different strains, we found that: (1) strains Smic, Stri, Slin, and Spil all established a stable symbiosis that promoted strobilation and (2) strains Bmin1 and Bmin2 did not establish a stable symbiosis and strobilation did not occur. Strains Smic, Stri, Slin, and Spil were used in a subsequent bleaching experiment; each of the strains was introduced to a subset of aposymbiotic polyps and once polyp tissues were saturated with symbionts they were subjected to elevated temperatures-32 • C and 34 • C-for 2 weeks. Our findings indicate that, in general, pairings of polyps with Symbiodiniaceae strains that are native to Cassiopea (Stri and Smic) performed better than a non-native strain (Slin) even though this strain has a high thermotolerance. This suggests a degree of partner specificity that may limit the adaptive potential of certain cnidarians to increased ocean warming. We also observed that the free-living, non-native thermotolerant strain Spil was relatively successful in resisting bleaching during experimental trials. This suggests that free-living Symbiodiniaceae may provide a supply of potentially "new" thermotolerant strains to cnidarians following a bleaching event.
2001
Coral bleaching involves the loss of symbiotic dinoflagellates (zooxanthellae) from reef corals and other cnidarians and may be a stress response of the host, algae or both. To determine the role of zooxanthellae in the bleaching process, aposymbiotic sea anemones from Bermuda (Aiptasia pallida) were infected with symbionts from other sea anemones (Aiptasia pallida from Florida, Bartholomea annulata and Condylactis gigantea). The expulsion of algae was measured during 24-h incubations at 25, 32 and 348C. Photosynthetic rates of freshly isolated zooxanthellae were also measured at these temperatures. The C. gigantea (Cg) symbionts were expelled in higher numbers than the other algae at 328C. Photosynthesis by the Cg algae was completely inhibited at this temperature, in contrast to the other symbionts. At 348 all of the symbionts had increased expulsion rates, and at this temperature only the symbionts from Florida A. pallida exhibited any photosynthesis. These results provide the first evidence that the differential release of symbionts from the same host species is related to decreased photosynthesis at elevated temperatures, and support other findings suggesting that zooxanthellae are directly affected by elevated temperatures during bleaching events.
Physiological correlates of symbiont migration during bleaching of two octocoral species
The Journal of Experimental Biology, 2014
Perturbed colonies of Phenganax parrini and Sarcothelia sp. exhibit migration of symbionts of Symbiodinium spp. into the stolons. Densitometry and visual inspection indicated that polyps bleached while stolons did not. When migration was triggered by temperature, light and confinement, colonies of Sarcothelia sp. decreased rates of oxygen formation in the light (due to the effects of perturbation on photosynthesis and respiration) and increased rates of oxygen uptake in the dark (due to the effects of perturbation on respiration alone). Colonies of P. parrini, by contrast, showed no significant changes in either aspect of oxygen metabolism. When migration was triggered by light and confinement, colonies of Sarcothelia sp. showed decreased rates of oxygen formation in the light and increased rates of oxygen uptake in the dark, while colonies of P. parrini maintained the former and increased the latter. During symbiont migration into their stolons, colonies of both species showed dramatic increases in reactive oxygen species (ROS), as visualized with a fluorescent probe, with stolons of Sarcothelia sp. exhibiting a nearly immediate increase of ROS. Differences in symbiont type may explain the greater sensitivity of colonies of Sarcothelia sp. Using fluorescent probes, direct measurements of migrating symbionts in the stolons of Sarcothelia sp. showed higher levels of reactive nitrogen species and lower levels of ROS than the surrounding host tissue. As measured by native fluorescence, levels of NAD(P)H in the stolons were unaffected by perturbation. Symbiont migration thus correlates with dramatic physiological changes and may serve as a marker for coral condition.
Symbiodinium migration mitigates bleaching in three octocoral species
Coral reefs are increasingly threatened by bleaching, a breakdown of the mutualism between coral hosts and symbionts (Symbiodinium spp.). Symbiont movement within a host may mitigate the effect of environmental stressors that trigger bleaching. Octocorals represent an important component of reef ecosystems, and the alcyonacean taxa Phenganax parrini, Sarcothelia sp., and Sympodium sp. were experimentally perturbed. In colonies subject to elevated temperature (incubated at 30-32 C to a maximum temperature of 31.5-33.5 C) and illumination, the number of Symbiodinium decreased in the tissue but increased in the gastrovascular system, with only a small proportion of symbionts expelled. Following within-colony symbiont migration, the three octocoral species retained high densities of symbionts in the coenenchyme. Nevertheless, variable mortality and retention occurred (85, 0, and 53% of the initial number of Symbiodinium were calculated to have died and 15, 100, and 45% were calculated to have been retained by P. parrini [maximum 33.5 C, 24 h],
University of Mauritius Research Journal, 2009
Coral species, one susceptible (Stylophora pistillata) and the other resistant (Platygyra ryukyuensis) to bleaching, were exposed to a sudden elevated temperature (33.5 o C) under dim light (5 µmol quanta m-2 s-1) for 10 to 720 min in time course experiments and to temperatures varying from 30 o C to 40 o C at 65 µmol quanta m-2 s-1 for 10 min at each temperature. Chlorophyll a fluorescence measurements in Symbiodinium of both coral species indicated that the maximum electron transport rate (ETR max) and the maximum quantum yield of photosystem II (PSII) fluorescence (F v /F m) were sensitive to thermal stress. The non-stressed Symbiodinium ETR max value in S. pistillata was halved earlier and at a lower temperature stress than in those of P. ryukyuensis. Denaturing gradient gel electrophoresis (DGGE) analysis of the internal transcribed spacer 2 (ITS2) region of the ribosomal DNA revealed inter-colony diversity of Symbiodinium in both species, though each species contained genetically distinct Symbiodinium types. Heat dissipation in PSII, through non-photochemical quenching (NPQ), increased in Symbiodinium of P. ryukyuensis irrespective of Symbiodinium genotype (C60 and C55), while in S. pistillata it either increased (C59) or decreased (C1) depending on genotype. Thus distinct Symbiodinium ITS2 types exhibit diverse photo-physiological responses to thermal stress, and may partially explain the variable bleaching susceptibilities of some hermatypic coral species.
Journal of Experimental Marine Biology and Ecology, 2001
Coral bleaching involves the loss of symbiotic dinoflagellates (zooxanthellae) from reef corals and other cnidarians and may be a stress response of the host, algae or both. To determine the role of zooxanthellae in the bleaching process, aposymbiotic sea anemones from Bermuda (Aiptasia pallida) were infected with symbionts from other sea anemones (Aiptasia pallida from Florida, Bartholomea annulata and Condylactis gigantea). The expulsion of algae was measured during 24-h incubations at 25, 32 and 348C. Photosynthetic rates of freshly isolated zooxanthellae were also measured at these temperatures. The C. gigantea (Cg) symbionts were expelled in higher numbers than the other algae at 328C. Photosynthesis by the Cg algae was completely inhibited at this temperature, in contrast to the other symbionts. At 348 all of the symbionts had increased expulsion rates, and at this temperature only the symbionts from Florida A. pallida exhibited any photosynthesis. These results provide the first evidence that the differential release of symbionts from the same host species is related to decreased photosynthesis at elevated temperatures, and support other findings suggesting that zooxanthellae are directly affected by elevated temperatures during bleaching events.
Proceedings of The National Academy of Sciences, 2004
Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylakoid membranes reveal that the critical threshold temperature separating thermally tolerant from sensitive species of zooxanthellae is determined by the saturation of the lipids. The lipid composition is potentially diagnostic of the differential nature of thermally induced bleaching found in scleractinian corals. Measurements of variable chlorophyll fluorescence kinetic transients indicate that thermally damaged membranes are energetically uncoupled but remain capable of splitting water. Consequently, a fraction of the photosynthetically produced oxygen is reduced by photosystem I through the Mehler reaction to form reactive oxygen species, which rapidly accumulate at high irradiance levels and trigger death and expulsion of the endosymbiotic algae. Differential sensitivity to thermal stress among the various species of Symbiodinium seems to be distributed across all clades. A clocked molecular phylogenetic analysis suggests that the evolutionary history of symbiotic algae in cnidarians selected for a reduced tolerance to elevated temperatures in the latter portion of the Cenozoic.