Symbiosis and host morphological variation: Symbiodiniaceae photosynthesis in the octocoral Briareum asbestinum at ambient and elevated temperatures

Intra-species morphological variation may occur in sessile organisms, such as corals, living in different habitats. Conversely, the octocoral Briareum asbestinum exhibits both encrusting and upright branching morphologies at the same shallow water habitat, enabling studying physiological differences uncoupled from habitat variation due to depth or reef location. We investigated the mutualism between endosymbiotic dinoflagellate algae, Breviolum spp. (previously clade B Symbiodinium), and these B. asbestinum morphologies at ambient and elevated temperatures. Based on msh1 gene sequences, the host morphologies were genetically similar although they differed in protein content, polyp expansion behavior, and associated Breviolum (B19 for encrusting and B21 for branching B. asbestinum). Due to colony orientation, polyps in encrusting B. asbestinum experienced irradiance levels nearly three times higher than polyps in the branching morph, which probably contributed to the lower photochemical and light absorption efficiencies of the Breviolum in encrusting fragments. The light-limited portion of photosynthesis-irradiance curves and the intracellular chlorophyll concentrations, however, indicated that Breviolum in both morphologies were acclimated to similar internal irradiances. Encrusting B. asbestinum exhibited higher Breviolum density, areal chlorophyll a, and greater photosynthetic rates cm(-2) compared to branching B. asbestinum. Notably, elevated temperature did not cause bleaching in either morphology, as Breviolum and chlorophyll densities did not differ significantly from ambient temperature, although the two morphologies adjusted some of the measured parameters, indicating coping with the stressor. In the face of continued ocean warming, the high thermal tolerance of octocorals may reinforce the shift of Caribbean reefs from scleractinian coral to octocoral dominance

Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge

Bioeroding sponges break down calcium carbonate substratum, including coral skeleton, and their capacity for reef erosion is expected to increase in warmer and more acidic oceans. However, elevated temperature can disrupt the functionally important microbial symbionts of some sponge species, often with adverse consequences for host health. Here, we provide the first detailed description of the microbial community of the bioeroding sponge Cliona orientalis and assess how the community responds to seawater temperatures incrementally increasing from 23°C to 32°C. The microbiome, identified using 16S rRNA gene sequencing, was dominated by Alphaproteobacteria, including a single OTU (Rhodothalassium sp.) that represented 21% of all sequences. The 'core' microbial community (taxa present in >80% of samples) included putative nitrogen fixers and ammonia oxidizers, suggesting that symbiotic nitrogen metabolism may be a key function of the C. orientalis holobiont. The C. orientalis microbiome was generally stable at temperatures up to 27°C, however a community shift occurred at 29°C, including changes in the relative abundance and turnover of microbial OTUs. Notably, this microbial shift occurred at a lower temperature than the 32°C threshold that induced sponge bleaching, indicating that changes in the microbiome may play a role in the destabilisation of the C. orientalis holobiont. C. orientalis failed to regain Symbiodinium or restore its baseline microbial community following bleaching, suggesting that the sponge has limited ability to recover from extreme thermal exposure, at least under aquarium conditions. This article is protected by copyright. All rights reserved

Dissolved inorganic nutrient enrichment does not affect sponge growth or condition

Changing land use and an increasing human population have led to increased terrestrial runoff, which delivers nutrients, pesticides, and heavy metals into aquatic ecosystems. Elevated nutrient levels can adversely affect nearshore corals by reducing the amount of light reaching the benthos, exacerbating coral disease and bleaching, as well as stimulating algal growth, but the effects on other reef taxa are poorly understood. We investigated the effects of dissolved inorganic nutrient enrichment and changes in irradiance on the growth and condition of 5 common Great Barrier Reef sponges: 4 sponges with photosynthetic symbionts and 1 lacking photosynthetic symbionts. Concentrations of up to 7 µM total dissolved inorganic nitrogen (DIN) did not significantly affect the growth, condition, or chl a content of any sponge species after 10 wk exposure. However, 2 species lost >20% volume across all nutrient treatments, suggesting that aquarium conditions may have been suboptimal for these species. Irradiance (80 vs. 160 µmol quanta m s) did not affect 4 of the 5 sponge species; however, higher irradiance resulted in higher organic content and chl a levels in the bioeroding sponge Cliona orientalis, the only studied species that associates with the photosynthetic dinoflagellate Symbiodinium, suggesting that sponge-Symbiodinium associations may be more sensitive to irradiance levels than sponge- Cyanobacteria associations. While elevated nutrient levels are exacerbating the decline of reef-building corals, exposure to the average DIN levels within flood plumes that reach inshore reefs appears to have negligible effects on reef sponges

Zooxanthellar Symbionts Shape Host Sponge Trophic Status through Translocation of Carbon

Sponges belonging to the genus Cliona are common inhabitants of many coral reefs, and as bioeroders, they play an important role in the carbonate cycle of the reef. Several Cliona species maintain intracellular populations of dinoflagellate zooxanthellae (i.e., Symbiodinium spp.), which also form symbioses with a variety of other invertebrates and protists (e.g., corals, molluscs, foraminifera). Unlike the case of coral symbioses, however, almost nothing is known of the metabolic interaction between sponges and their zooxanthella symbionts. To assess this interaction, we performed a tracer experiment to follow C and N in the system, performed a reciprocal transplant experiment, and measured the stable carbon isotope ratio of Cliona spp. with and without zooxanthellae to study the influence of environment on the interaction. We found strong evidence of a transfer of C from zooxanthellae to their sponge hosts but no evidence of a transfer of N from sponge to zooxanthellae. We also saw significant influences of the environment on the metabolism of the sponges. Finally, we observed significant differences in carbon metabolism of sponge species with and without symbionts. These data strongly support hypotheses of metabolic integration between zooxanthellae and their sponge host and extend our understanding of basic aspects of benthic-pelagic coupling in shallow-water marine environments

A decadal analysis of bioeroding sponge cover on the inshore Great Barrier Reef

Decreasing coral cover on the Great Barrier Reef (GBR) may provide opportunities for rapid growth and expansion of other taxa. The bioeroding sponges Cliona spp. are strong competitors for space and may take advantage of coral bleaching, damage, and mortality. Benthic surveys of the inshore GBR (2005–2014) revealed that the percent cover of the most abundant bioeroding sponge species, Cliona orientalis, has not increased. However, considerable variation in C. orientalis cover, and change in cover over time, was evident between survey locations. We assessed whether biotic or environmental characteristics were associated with variation in C. orientalis distribution and abundance. The proportion of fine particles in the sediments was negatively associated with the presence-absence and the percent cover of C. orientalis, indicating that the sponge requires exposed habitat. The cover of corals and other sponges explained little variation in C. orientalis cover or distribution. The fastest increases in C. orientalis cover coincided with the lowest macroalgal cover and chlorophyll a concentration, highlighting the importance of macroalgal competition and local environmental conditions for this bioeroding sponge. Given the observed distribution and habitat preferences of C. orientalis, bioeroding sponges likely represent site-specific – rather than regional – threats to corals and reef accretion

The bioeroding sponge Cliona orientalis will not tolerate future projected ocean warming

Coral reefs face many stressors associated with global climate change, including increasing sea surface temperature and ocean acidification. Excavating sponges, such as Cliona spp., are expected to break down reef substrata more quickly as seawater becomes more acidic. However, increased bioerosion requires that Cliona spp. maintain physiological performance and health under continuing ocean warming. In this study, we exposed C. orientalis to temperature increments increasing from 23 to 32 °C. At 32 °C, or 3 °C above the maximum monthly mean (MMM) temperature, sponges bleached and the photosynthetic capacity of Symbiodinium was compromised, consistent with sympatric corals. Cliona orientalis demonstrated little capacity to recover from thermal stress, remaining bleached with reduced Symbiodinium density and energy reserves after one month at reduced temperature. In comparison, C. orientalis was not observed to bleach during the 2017 coral bleaching event on the Great Barrier Reef, when temperatures did not reach the 32 °C threshold. While C. orientalis can withstand current temperature extremes

<i>Symbiodinium</i> Photosynthesis in Caribbean Octocorals

<div><p>Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. <i>Symbiodinium</i> associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm² but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in <i>Symbiodinium</i> photosynthetic performance could not be attributed to <i>Symbiodinium</i> type. All <i>P. anceps</i> (n = 9) and <i>P. wagenaari</i> (n = 6) colonies, in addition to one <i>E. tourneforti</i> and three <i>P. porosa</i> colonies, associated with <i>Symbiodinium</i> type B1. The B1 <i>Symbiodinium</i> from these four gorgonian species did not cluster with lineages of B1 <i>Symbiodinium</i> from scleractinian corals. The remaining eight <i>E. tourneforti</i> colonies harbored <i>Symbiodinium</i> type B1L, while six <i>P. porosa</i> colonies harbored type B1i. Understanding the symbioses between gorgonian corals and <i>Symbiodinium</i> will aid in deciphering why gorgonian corals dominate many Caribbean reefs.</p></div

The effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, <i>Symbiodinium</i> spp.

<div><p>Global climate change not only leads to elevated seawater temperatures but also to episodic anomalously high or low temperatures lasting for several hours to days. Scleractinian corals are detrimentally affected by thermal fluctuations, which often lead to an uncoupling of their mutualism with <i>Symbiodinium</i> spp. (coral bleaching) and potentially coral death. Consequently, on many Caribbean reefs scleractinian coral cover has plummeted. Conversely, gorgonian corals persist, with their abundance even increasing. How gorgonians react to thermal anomalies has been investigated utilizing limited parameters of either the gorgonian, <i>Symbiodinium</i> or the combined symbiosis (holobiont). We employed a holistic approach to examine the effect of an experimental five-day elevated temperature episode on parameters of the host, symbiont, and the holobiont in <i>Eunicea tourneforti</i>, <i>E</i>. <i>flexuosa</i> and <i>Pseudoplexaura porosa</i>. These gorgonian corals reacted and coped with 32°C seawater temperatures. Neither <i>Symbiodinium</i> genotypes nor densities differed between the ambient 29.5°C and 32°C. Chlorophyll <i>a</i> and <i>c</i>_<i>2</i> per <i>Symbiodinium</i> cell, however, were lower at 32°C leading to a reduction in chlorophyll content in the branches and an associated reduction in estimated absorbance and increase in the chlorophyll <i>a</i> specific absorption coefficient. The adjustments in the photochemical parameters led to changes in photochemical efficiencies, although these too showed that the gorgonians were coping. For example, the maximum excitation pressure, <i>Q</i>_m, was significantly lower at 32°C than at 29.5°C. In addition, although per dry weight the amount of protein and lipids were lower at 32°C, the overall energy content in the tissues did not differ between the temperatures. Antioxidant activity either remained the same or increased following exposure to 32°C further reiterating a response that dealt with the stressor. Taken together, the capability of Caribbean gorgonian corals to modify symbiont, host and consequently holobiont parameters may partially explain their persistence on reefs faced with climate change.</p></div

Summary of the results of a linear mixed effects model analyses testing the effect of elevated temperature on <i>Symbiodinium</i> parameters in the Caribbean gorgonian corals <i>Eunicea tourneforti</i> (<i>ET)</i>, <i>E</i>. <i>flexuosa</i> (<i>EF</i>) and <i>Pseudoplexaura porosa</i> (<i>PP</i>).

<p>Summary of the results of a linear mixed effects model analyses testing the effect of elevated temperature on <i>Symbiodinium</i> parameters in the Caribbean gorgonian corals <i>Eunicea tourneforti</i> (<i>ET)</i>, <i>E</i>. <i>flexuosa</i> (<i>EF</i>) and <i>Pseudoplexaura porosa</i> (<i>PP</i>).</p

A maximum likelihood phylogenetic tree based on microsatellite flanking regions of B1 <i>Symbiodinium</i>.

<p>The phylogeny includes B1 <i>Symbiodinium</i> from the four gorgonian species in this study (highlighted in gray), from other gorgonian corals <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a>, from scleractinian and hydrozoan corals <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Finney1" target="_blank">[36]</a>, as well as <i>Symbiodinium minutum</i> from <i>Aiptasia</i>, a sea anemone <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a>. Branch tips are labeled with host species and sample sizes when n>1. Gorgonian and scleractinian coral species are shown in black and red, respectively, and the other cnidarians are shown in blue. B1 lineages described by Finney et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Finney1" target="_blank">[36]</a> are listed besides the host taxa. Numbers above the branches are the posterior probability above the maximum likelihood consensus support for each group. B1 <i>Symbiodinium</i> from 16 of 19 gorgonian colonies sampled clustered in a phylogenetic group with high posterior probability (top gray box). Three gorgonian colonies were placed outside of this clade (bottom gray box) and were most closely related to <i>Symbiodinium</i> isolated from <i>Pseudoplexaura porosa</i> from Florida (indicated with (+1)) and cultured <i>Symbiodinium</i> from <i>Gorgonia ventalina</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106419#pone.0106419-Thornhill1" target="_blank">[47]</a> indicated with *. (#) indicates a group recovered in the maximum likelihood tree, but not the Bayesian phylogenetic tree.</p