Symbioses are restructured by repeated mass coral bleaching.

Survival of symbiotic reef-building corals under global warming requires rapid acclimation or adaptation. The impact of accumulated heat stress was compared across 1643 symbiont communities before and after the 2016 mass bleaching in three coral species and free-living in the environment across ~900 kilometers of the Great Barrier Reef. Resilient reefs (less aerial bleaching than predicted from high satellite sea temperatures) showed low variation in symbioses. Before 2016, heat-tolerant environmental symbionts were common in ~98% of samples and moderately abundant (9 to 40% in samples). In corals, heat-tolerant symbionts were at low abundances (0 to 7.3%) but only in a minority (13 to 27%) of colonies. Following bleaching, environmental diversity doubled (including heat-tolerant symbionts) and increased in one coral species. Communities were dynamic (Acropora millepora) and conserved (Acropora hyacinthus and Acropora tenuis), including symbiont community turnover and redistribution. Symbiotic restructuring after bleaching occurs but is a taxon-specific ecological opportunity.

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 (<3 °C above MMM) under laboratory and natural conditions, this species would not survive ocean temperatures projected for 2100 without acclimatisation or adaptation (≥3 °C above MMM). Hence, as ocean temperatures increase above local thermal thresholds, C. orientalis will have a negligible impact on reef erosion.

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 operational taxonomic unit (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 destabilization 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.

Sibling species of mutualistic Symbiodinium clade G from bioeroding sponges in the western Pacific and western Atlantic oceans.

Dinoflagellates in the genus Symbiodinium associate with a broad array of metazoan and protistian hosts. Symbiodinium-based symbioses involving bioeroding sponge hosts have received less attention than those involving popular scleractinian hosts. Certain species of common Cliona harbor high densities of an ecologically restricted group of Symbiodinium, referred to as Clade G. Clade G Symbiodinium are also known to form stable and functionally important associations with Foraminifera and black corals (Antipatharia) Analyses of genetic evidence indicate that Clade G likely comprises several distinct species. Here, we use nucleotide sequence data in combination with ecological and geographic attributes to formally describe Symbiodinium endoclionum sp. nov. obtained from the Pacific boring sponge Cliona orientalis and Symbiodinium spongiolum sp. nov. from the congeneric western Atlantic sponge Cliona varians. These species appear to be part of an adaptive radiation comprising lineages of Clade G specialized to the metazoan phyla Porifera and Cnidaria, which began prior to the separation of the Pacific and Atlantic Oceans.

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 effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, Symbiodinium spp.

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 Symbiodinium 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, Symbiodinium 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 Eunicea tourneforti, E. flexuosa and Pseudoplexaura porosa. These gorgonian corals reacted and coped with 32°C seawater temperatures. Neither Symbiodinium genotypes nor densities differed between the ambient 29.5°C and 32°C. Chlorophyll a and c2 per Symbiodinium 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 a 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, Qm, 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.

MycoDB, a global database of plant response to mycorrhizal fungi.

Plants form belowground associations with mycorrhizal fungi in one of the most common symbioses on Earth. However, few large-scale generalizations exist for the structure and function of mycorrhizal symbioses, as the nature of this relationship varies from mutualistic to parasitic and is largely context-dependent. We announce the public release of MycoDB, a database of 4,010 studies (from 438 unique publications) to aid in multi-factor meta-analyses elucidating the ecological and evolutionary context in which mycorrhizal fungi alter plant productivity. Over 10 years with nearly 80 collaborators, we compiled data on the response of plant biomass to mycorrhizal fungal inoculation, including meta-analysis metrics and 24 additional explanatory variables that describe the biotic and abiotic context of each study. We also include phylogenetic trees for all plants and fungi in the database. To our knowledge, MycoDB is the largest ecological meta-analysis database. We aim to share these data to highlight significant gaps in mycorrhizal research and encourage synthesis to explore the ecological and evolutionary generalities that govern mycorrhizal functioning in ecosystems.

Symbiodinium photosynthesis in Caribbean octocorals.

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. Symbiodinium 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 Symbiodinium photosynthetic performance could not be attributed to Symbiodinium type. All P. anceps (n = 9) and P. wagenaari (n = 6) colonies, in addition to one E. tourneforti and three P. porosa colonies, associated with Symbiodinium type B1. The B1 Symbiodinium from these four gorgonian species did not cluster with lineages of B1 Symbiodinium from scleractinian corals. The remaining eight E. tourneforti colonies harbored Symbiodinium type B1L, while six P. porosa colonies harbored type B1i. Understanding the symbioses between gorgonian corals and Symbiodinium will aid in deciphering why gorgonian corals dominate many Caribbean reefs.

Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: Evidence of heteroplasmy and putative host-specific symbiont lineages.

Among the Porifera, symbiosis with Symbiodinium spp. (i.e., zooxanthellae) is largely restricted to members of the family Clionaidae. We surveyed the diversity of zooxanthellae associated with sponges from the Caribbean and greater Indo-Pacific regions using chloroplast large subunit (cp23S) domain V sequences. We provide the first report of Clade C Symbiodinium harbored by a sponge (Cliona caesia), and the first report of Clade A Symbiodinium from an Indo-Pacific sponge (C. jullieni). Clade A zooxanthellae were also identified in sponges from the Caribbean, which has been reported previously. Sponges that we examined from the Florida Keys all harbored Clade G Symbiodinium as did C. orientalis from the Indo-Pacific, which also supports earlier work with sponges. Two distinct Clade G lineages were identified in our phylogenetic analysis; Symbiodinium extracted from clionaid sponges formed a monophyletic group sister to Symbiodinium found in foraminiferans. Truncated and 'normal' length variants of 23S rDNA sequences were detected simultaneously in all three morphotypes of C. varians providing the first evidence of chloroplast-based heteroplasmy in a sponge. None of the other sponge species examined showed evidence of heteroplasmy. As in previous work, length variation in cp23S domain V sequences was found to correspond in a highly precise manner to finer resolution of phylogenetic topology among Symbiodinium clades. On a global scale, existing data indicate that members of the family Clionaidae that host zooxanthellae can form symbiotic associations with at least four Symbiodinium clades. The majority of sponge hosts appear to harbor only one cladal type of symbiont, but some species can harbor more than one clade of zooxanthellae concurrently. The observed differences in the number of partners harbored by sponges raise important questions about the degree of coevolutionary integration and specificity of these symbioses. Although our sample sizes are small, we propose that one of the Clade G lineages identified in this study is comprised of sponge-specialist zooxanthellae. These zooxanthellae are common in Caribbean sponges, but additional work in other geographic regions is necessary to test this idea. Sponges from the Indo-Pacific region harbor zooxanthellae from Clades A, C, and G, but more sponges from this region should be examined.

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.