The specificity of temperate anthozoan-dinoflagellate symbioses.

The aim of this study was to investigate the specificity of temperate dinoflagellate - anthozoan symbioses and the influence of any specificity on the percentage contribution of photosynthetically fixed carbon to the host's daily respiratory carbon budget (CZAR). The British symbiotic Anthozoa Cereus pedunculatus (Pennant) I Anthopleura ballii (Cocks), Anemonia viridis (Forskal) and Isozoanthus sulcatus (Gos3e) and the sub-tropical anthozoan Aiptasia pallida (Verrill) and their algal symbionts were investigated. The characteristics of freshly isolated and cultured symbionts were studied to determine whether the algal cells residing in each host species appeared different and how symbiont characteristics may be determined by the host environment. Horphology, division behaviour and photosynthetic pigment composition were examined using SEMO TEMO LMO TLC and HPLC respectively. The symbionts of each host species were identified as dinoflagellates of the genus Symbiodinium, even though there was an absence of a motile phase in the cell cycle of the British hosts. Differences between symbionts of different host species and conspecific hosts were evident with respect to thylakoid arrangement, cell size and cell division rate, and possibly pigment concentrations. Host determined phenotypic plasticity was observed with respect to the absence of a "pellicle". Host-symbiont recognition and specificity were investigated - by reinfecting aposymbiotic C. _pedunculatus with symbionts from different host species and measuring the density and biomass of symbionts at different time intervals. The presence of different strains or species of Symbiodinium was evident, with recognition of these different symbionts being predominantly post-endocytotic. 'Homologous' symbionts were the most 'successful' at repopulating C. pedunculatus. After 9 months, the population densities and biomasses, and division rates of the different 'strains' Of 3ymbionts were the same, suggesting a greater symbiotic integration with 'heterologous, 'strains' with time. The reflection of specificity by the photosynthetic fixation of carbon in vivo was measured using an 02 electrode. 1110mologous, symbiontW photosynthesized at a greater rate than 'heterologous' symbionts in vivo, despite the higher photosynthetic rates of some of these 'heterologous' symbionts in their original hosts. Photosynthate translocation by symbionts in response to different host environments was investigated using in vivo and in vitro 14C labelling and the 'growth rate method'. The percentage translocation was host-symbiont specific and appeared to be controlled by different mechanisms in different host species and conspecific hosts from different locations. The CZAR in 'natural' and reestablished symbioses was calculated. Values ranged from 25.7 to 112.2 % in the 'natural' symbi T9 es and 58.1 to 76.7 % in the reestablished symbioses when measured using C. When measured using the 'growth rate method' values were 73.2 to 188.4 % and 88.3 to 146.5 % respectively. The CZAR in the reestablished symbioses and consequently their ability to survive autotrophically reflected the specific host-symbiont relationship. Symbiosis specificity and the reduced availability of carbon to host growth and reproduction in 'heterologous' symbioses may limit 'novel' symbioses in the field.

Mucus Sugar Content Shapes the Bacterial Community Structure in Thermally Stressed Acropora muricata

It has been proposed that the chemical composition of a coral’s mucus can influence the associated bacterial community. However, information on this topic is rare, and non-existent for corals that are under thermal stress. This study therefore compared the carbohydrate composition of mucus in the coral Acropora muricata when subjected to increasing thermal stress from 26°C to 31°C, and determined whether this composition correlated with any changes in the bacterial community. Results showed that, at lower temperatures, the main components of mucus were N-acetyl glucosamine and C6 sugars, but these constituted a significantly lower proportion of the mucus in thermally-stressed corals. The change in the mucus composition coincided with a shift from a γ-Proteobacteria- to a Verrucomicrobiae- and α-Proteobacteria-dominated community in the coral mucus. Bacteria in the class Cyanobacteria also started to become prominent in the mucus when the coral was thermally stressed. The increase in the relative abundance of the Verrucomicrobiae at higher temperature was strongly associated with a change in the proportion of fucose, glucose and mannose in the mucus. Increase in the relative abundance of α-Proteobacteria were associated with GalNAc and glucose, while the drop in relative abundance of γ-Proteobacteria at high temperature coincided with changes in fucose and mannose. Cyanobacteria were highly associated with arabinose and xylose. Changes in mucus composition and the bacterial community in the mucus layer occurred at 29°C, which were prior to visual signs of coral bleaching at 31°C. A compositional change in the coral mucus, induced by thermal stress could therefore be a key factor leading to a shift in the associated bacterial community. This, in turn, has the potential to impact the physiological function of the coral holobiont

Cell Biology of Cnidarian-Dinoflagellate Symbiosis

The symbiosis between cnidarians (e.g., corals or sea anemones) and intracellular dinoflagellate algae of the genus Symbiodinium is of immense ecological importance. In particular, this symbiosis promotes the growth and survival of reef corals in nutrient-poor tropical waters; indeed, coral reefs could not exist without this symbiosis. However, our fundamental understanding of the cnidarian-dinoflagellate symbiosis and of its links to coral calcification remains poor. Here we review what we currently know about the cell biology of cnidarian-dinoflagellate symbiosis. In doing so, we aim to refocus attention on fundamental cellular aspects that have been somewhat neglected since the early to mid-1980s, when a more ecological approach began to dominate. We review the four major processes that we believe underlie the various phases of establishment and persistence in the cnidarian/coral-dinoflagellate symbiosis: (i) recognition and phagocytosis, (ii) regulation of host-symbiont biomass, (iii) metabolic exchange and nutrient trafficking, and (iv) calcification. Where appropriate, we draw upon examples from a range of cnidarian-alga symbioses, including the symbiosis between green Hydra and its intracellular chlorophyte symbiont, which has considerable potential to inform our understanding of the cnidarian-dinoflagellate symbiosis. Ultimately, we provide a comprehensive overview of the history of the field, its current status, and where it should be going in the future.Keywords: inorganic carbon uptake, Anemone aiptasia pallida, Coral stylophora pistillata, Pocillopora damicornis linnaeus, Host release factor, Free amino acids, Reef building corals, Alga invertebrate symbiosis, Symbiodinium microadriaticum freudenthal, Green hydra symbiosi

Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals

Coral bleaching poses a threat to coral reefs worldwide. As a consequence of the temperature-induced breakdown in coral–dinoflagellate symbiosis, bleaching can have extensive effects on reef communities. However, our understanding of bleaching at a cellular level is limited, and this is particularly true regarding differential susceptibility among coral species. Recent work suggests that bleaching may represent a host innate immune-like response to symbiont dysfunction that involves synthesis of the signalling compound nitric oxide (NO) and the induction of host apoptotic-like cell death. In this study, we examined the activity of apoptosis-regulating enzymes alongside oxidised NO accumulation (a proxy for NO synthesis) in the reef corals Acropora millepora, Montipora digitata, and Pocillopora damicornis during experimental thermal stress. P. damicornis was the most sensitive species, suffering mortality (tissue sloughing) after 5 days at 33 °C but non-lethal bleaching after 9 days at 31.5 °C. A. millepora bleached at 33 °C but remained structurally intact, while M. digitata showed little evidence of bleaching. P. damicornis and A. millepora both exhibited evidence of temperature-induced NO synthesis and, after 5 days of heating, levels of oxidised NO in both species were fivefold higher than in controls maintained at 28.5 °C. These responses preceded bleaching by a number of days and may have occurred before symbiont dysfunction (measured as chlorophyll a degradation and oxidised NO accumulation). In A. millepora, apparent NO synthesis correlated with the induction of host apoptotic-like pathways, while in P. damicornis, the upregulation of apoptotic pathways occurred later. No evidence of elevated NO production or apoptosis was observed in M. digitata at 33 °C and baseline activity of apoptosis-regulating enzymes was negligible in this species. These findings provide important physiological data in the context of the responses of corals to global change and suggest that early events in the host may be important in the collapse of the coral–dinoflagellate symbiosis

Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species

Reef-building corals and some other cnidarians form symbiotic relationships with members of the dinoflagellate family Symbiodinaceae. As Symbiodinaceae is a highly diverse taxon, the physiological interactions between its members and their hosts are assumed to differ between associations. The presence of different symbiont types is known to affect expression levels of specific host genes, but knowledge of the effects on the transcriptome more broadly remains limited. In the present study, transcriptome profiling was conducted on the tropical corallimorpharian, Ricordea yuma, following the establishment of symbiosis with either the \u27homologous\u27 symbiont Symbiodinium goreaui (also known as Cladocopium goreaui; ITS2 type C1) or \u27heterologous\u27 symbionts (predominantly S. trenchii, which is also known as Durusdinium trenchii; ITS2 type D1a) isolated from a different corallimorpharian host (Rhodactis indosinensis). Transcriptomic analyses showed that genes encoding host glycogen biosynthesis pathway components are more highly induced during colonization by the homologous symbiont than by the heterologous symbiont. Similar patterns were also observed for several other genes thought to facilitate symbiotic nutrient exchange, including those involved in lipid translocation/storage and metabolite transport. The gene expression results presented here imply that colonization by homologous or heterologous Symbiodinium types may have very different metabolic consequences for the Ricordea host, supporting the notion that even though some cnidarians may be able to form novel symbioses after bleaching, the metabolic performance of these may be compromised.This article has an associated First Person interview with the first author of the paper

Antioxidant responses to heat and light stress differ with habitat in a common reef coral

Coral bleaching—the stress-induced collapse of the coral–Symbiodinium symbiosis—is a significant driver of worldwide coral reef degradation. Yet, not all corals are equally susceptible to bleaching, and we lack a clear understanding of the mechanisms underpinning their differential susceptibilities. Here, we focus on cellular redox regulation as a potential determinant of bleaching susceptibility in the reef coral Stylophora pistillata. Using slow heating (1 °C d−1) and altered irradiance, we induced bleaching in S. pistillata colonies sampled from two depths [5–8 m (shallow) and 15–18 m (deep)]. There was significant depth-dependent variability in the timing and extent of bleaching (loss of symbiont cells), as well as in host enzymatic antioxidant activity [specifically, superoxide dismutase and catalase (CAT)]. However, among the coral fragments that bleached, most did so without displaying any evidence of a host enzymatic antioxidant response. For example, both deep and shallow corals suffered significant symbiont loss at elevated temperature, but only deep colonies exposed to high temperature and high light displayed any up-regulation of host antioxidant enzyme activity (CAT). Surprisingly, this preceded the equivalent antioxidant responses of the symbiont, which raises questions about the source(s) of hydrogen peroxide in the symbiosis. Overall, changes in enzymatic antioxidant activity in the symbionts were driven primarily by irradiance rather than temperature, and responses were similar across depth groups. Taken together, our results suggest that in the absence of light stress, heating of 1 °C d−1 to 4 °C above ambient is not sufficient to induce a substantial oxidative challenge in S. pistillata. We provide some of the first evidence that regulation of coral enzymatic antioxidants can vary significantly depending on habitat, and, in terms of determining bleaching susceptibility, our results suggest a significant role for the host’s differential regulation of cellular redox status

Climate change alterations to ecosystem dominance: how might sponge-dominated reefs function?

Anthropogenic stressors are impacting ecological systems across the world. Of particular concern are the recent rapid changes occurring in coral reef systems. With ongoing degradation from both local and global stressors, future reefs are likely to function differently to current coral-dominated ecosystems. Determining key attributes of future reef states is critical to reliably predict outcomes for ecosystem service provision. Here we explore the impacts of changing sponge dominance on coral reefs. Qualitative modelling of reef futures suggests that changing sponge dominance due to increased sponge abundance will have different outcomes for other trophic levels compared with increased sponge dominance as a result of declining coral abundance. By exploring uncertainty in the model outcomes we identify the need to: i) quantify changes in carbon flow through sponges, ii) determine the importance of food limitation for sponges, iii) assess the ubiquity of the recently described 'sponge loop', iv) determine the competitive relationships between sponges and other benthic taxa, particularly algae, and v) understand how changing dominance of other organisms alters trophic pathways and energy flows through ecosystems. Addressing these knowledge gaps will facilitate development of more complex models that assess functional attributes of sponge-dominated reef ecosystems. This article is protected by copyright. All rights reserved

Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific

Growth anomalies (GAs) are common, tumor-like diseases that can cause significant morbidity and decreased fecundity in the major Indo-Pacific reef-building coral genera, Acropora and Porites. GAs are unusually tractable for testing hypotheses about drivers of coral disease because of their pan-Pacific distributions, relatively high occurrence, and unambiguous ease of identification. We modeled multiple disease-environment associations that may underlie the prevalence of Acropora growth anomalies (AGA) (n = 304 surveys) and Porites growth anomalies (PGA) (n = 602 surveys) from across the Indo-Pacific. Nine predictor variables were modeled, including coral host abundance, human population size, and sea surface temperature and ultra-violet radiation anomalies. Prevalence of both AGAs and PGAs were strongly host density-dependent. PGAs additionally showed strong positive associations with human population size. Although this association has been widely posited, this is one of the first broad-scale studies unambiguously linking a coral disease with human population size. These results emphasize that individual coral diseases can show relatively distinct patterns of association with environmental predictors, even in similar diseases (growth anomalies) found on different host genera (Acropora vs. Porites). As human densities and environmental degradation increase globally, the prevalence of coral diseases like PGAs could increase accordingly, halted only perhaps by declines in host density below thresholds required for disease establishment

Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations

Experimental manipulation of the symbiosis between cnidarians and photosynthetic dinoflagellates (Symbiodinium spp.) is crucial to advancing the understanding of the cellular mechanisms involved in host-symbiont interactions, and overall coral reef ecology. The anemone Aiptasia sp. is a model for cnidarian-dinoflagellate symbiosis, and notably it can be rendered aposymbiotic (i.e. dinoflagellate-free) and re-infected with a range of Symbiodinium types. Various methods exist for generating aposymbiotic hosts; however, they can be hugely time consuming and not wholly effective. Here, we optimise a method using menthol for production of aposymbiotic Aiptasia. The menthol treatment produced aposymbiotic hosts within just 4 weeks (97-100% symbiont loss), and the condition was maintained long after treatment when anemones were held under a standard light: dark cycle. The ability of Aiptasia to form a stable symbiosis appeared to be unaffected by menthol exposure, as demonstrated by successful re-establishment of the symbiosis when anemones were experimentally re-infected. Furthermore, there was no significant impact on photosynthetic or respiratory performance of re-infected anemones.Keywords: Coral reefs, Symbiodinium, Cnidarian-dinoflagellate symbiosisKeywords: Coral reefs, Symbiodinium, Cnidarian-dinoflagellate symbiosi

Molecular techniques and their limitations shape our view of the holobiont

It is now recognised that the biology of almost any organism cannot be fully understood without recognising the existence and potential functional importance of associated microbes. Arguably, the emergence of this holistic viewpoint may never have occurred without the development of a crucial molecular technique, 16S rDNA amplicon sequencing, which allowed microbial communities to be easily profiled across a broad range of contexts. A diverse array of molecular techniques are now used to profile microbial communities, infer their evolutionary histories, visualise them in host tissues, and measure their molecular activity. In this review, we examine each of these categories of measurement and inference with a focus on the questions they make tractable, and the degree to which their capabilities and limitations shape our view of the holobiont