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Diversity and Abundance of Symbiodiniaceae and Bacteria in Corals Sarcophyton trocheliophorum and Euphyllia ancora Under Thermal Stimulation

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Abstract

Coral Symbiodiniaceae and bacteria maintain a symbiotic relationship that is essential for coral survival. The symbiotic communities component in the polyps host could affect coral resistance and the ability to recover from stress. In this study, we increased the cultured range temperature (26 ± 1 ℃) of Sarcophyton trocheliophorum and Euphyllia ancora at 32 ℃ for 12 hours, and then amplified the ITS2 sequence of Symbiodinium and the bacterial 16S rRNA sequence in the sample, respectively to compare Symbiodiniaceae and bacteria diversity and abundance with normal culture temperature. The results showed that there was no change in the dominant species of Symbiodinium in these two corals in the heat treatment group, but the diversity of Symbiodinium in the two corals was significantly different. On the other hand, after thermal treatment, the endophytic bacteria of S. trocheliophorum represented more aerobic bacteria Delfitia, while the E. ancora was infected with more pathogenic endosymbiotic bacteria. This difference observation can be attributed to the different tolerance of corals.

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... However, a consensus has been achieved that coral bleaching is mainly caused by losing in vivo pigments of symbiotic Symbiodiniaceae. Symbiodiniaceae lives in the vacuole of the entoderm cells of the host and provides more than 95% of the products of photosynthesis (e.g., amino acids, sugar, carbohydrate, and small molecular peptide) for hosts (Loh et al. 2001, Lu et al. 2021a. Photosynthetic products can supply energy and essential compounds for corals; instead, Symbiodiniaceae can get elemental nutrients (e.g., amine and phosphate) from the metabolic products by corals (Saxby 2000). ...
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Scleractinian corals have demonstrated the ability to shuffle their endosymbiotic dinoflagellate communities (genus Symbiodinium) during periods of acute environmental stress. This has been proposed as a mechanism of acclimation, which would be increased by a diverse and flexible association with Symbiodinium. Conventional molecular techniques used to evaluate Symbiodinium diversity are unable to identify genetic lineages present at background levels below 10%. Next generation sequencing (NGS) offers a solution to this problem and can resolve microorganism diversity at much finer scales. Here we apply NGS to evaluate Symbiodinium diversity and host specificity in Acropora corals from contrasting regions of Western Australia. The application of 454 pyrosequencing allowed for detection of Symbiodinium operational taxonomic units (OTUs) occurring at frequencies as low as 0.001%, offering a 10000-fold increase in sensitivity compared to traditional methods. All coral species from both regions were overwhelmingly dominated by a single clade C OTU (accounting for 98% of all recovered sequences). Only 8.5% of colonies associated with multiple clades (clades C and D, or C and G), suggesting a high level of symbiont specificity in Acropora assemblages in Western Australia. While only 40% of the OTUs were shared between regions, the dominance of a single OTU resulted in no significant difference in Symbiodinium community structure, demonstrating that the coral-algal symbiosis can remain stable across more than 15 degrees of latitude and a range of sea surface temperature profiles. This study validates the use of NGS platforms as tools for providing fine-scale estimates of Symbiodinium diversity and can offer critical insight into the flexibility of the coral-algal symbiosis.
Article
The internal transcribed spacer (ITS) regions from 47 Symbiodinium (Freudenthal) isolates cultured from 34 different host species and two populations sampled from nature were sequenced and compared. Of these, 17 distinct ITS types were identified. The described species Symbiodinium goreaui , S. kawagutii , S. pilosum (Trench and Blank), S. microadriaticum (Freudenthal), and S. ( � Gymnodinium ) linucheae (Trench and Thinh) had ITS sequences distinct from each other. Four of these species share identical ITS sequences with un- characterized isolates. Sequence differences among other isolates indicate that at least seven other cul- tured types await formal species descriptions, whereas numerous others most likely exist in nature. The Sym- biodinium phylogeny is positively correlated with cell size, mycosporine-like amino acid production (UV pro- tection), and host infectivity, whereas the production of water-soluble peridinin-chl a- protein homodimer and monomer apoproteins and isoenzyme similarity do not correlate. There is evidence, based on the lack of phylogenetic congruency with allelic variability, that sexual recombination occurs at some frequency among Symbiodinium populations. Symbiodinium isolates from the Caribbean possess identical ITS sequences to iso- lates originating from the Red Sea or the western Pa- cific. These findings indicate that some Symbiodinium species may have global biogeographic distributions.
Article
Sea temperatures in many tropical regions have increased by almost 1°C over the past 100 years, and are currently increasing at ~1-2°C per century. Coral bleaching occurs when the thermal tolerance of corals and their photosynthetic symbionts (zooxanthellae) is exceeded. Mass coral bleaching has occurred in association with episodes of elevated sea temperatures over the past 20 years and involves the loss of the zooxanthellae following chronic photoinhibition. Mass bleaching has resulted in significant losses of live coral in many parts of the world. This paper considers the biochemical, physiological and ecological perspectives of coral bleaching. It also uses the outputs of four runs from three models of global climate change which simulate changes in sea temperature and hence how the frequency and intensity of bleaching events will change over the next 100 years. The results suggest that the thermal tolerances of reef-building corals are likely to be exceeded every year within the next few decades. Events as severe as the 1998 event, the worst on record, are likely to become commonplace within 20 years. Most information suggests that the capacity for acclimation by corals has already been exceeded, and that adaptation will be too slow to avert a decline in the quality of the world's reefs. The rapidity of the changes that are predicted indicates a major problem for tropical marine ecosystems and suggests that unrestrained warming cannot occur without the loss and degradation of coral reefs on a global scale.
Article
▪ Abstract Reef corals (and other marine invertebrates and protists) are hosts to a group of exceptionally diverse dinoflagellate symbionts in the genus Symbiodinium. These symbionts are critical components of coral reef ecosystems whose loss during stress-related “bleaching” events can lead to mass mortality of coral hosts and associated collapse of reef ecosystems. Molecular studies have shown these partnerships to be more flexible than previously thought, with different hosts and symbionts showing varying degrees of specificity in their associations. Further studies are beginning to reveal the systematic, ecological, and biogeographic underpinnings of this flexibility. Unusual symbionts normally found only in larval stages, marginal environments, uncommon host taxa, or at latitudinal extremes may prove critical in understanding the long-term resilience of coral reef ecosystems to environmental perturbation. The persistence of bleaching-resistant symbiont types in affected ecosystems, and the possibilit...
Article
The genus Symbiodinium is the commonly observed symbiotic dinoflagellate (zooxanthellae) that forms mutual associations with various marine invertebrates. Numerous studies have revealed that the genus is comprised of a group of diverse taxa, and information on the phylogenetic relationships among the genus’ members is increasing. In this study, small subunit (SSU) ribosomal RNA (ssrRNA) gene sequences were determined for 15 more Symbiodinium strains from 12 relatively unstudied host taxa (Indo-Pacific tridacnids, cardiids, sponge, and soft coral), 1 hitherto unreported free-living Symbiodinium strain, and 4 other Symbiodinium strains from four other host taxa (Indo-Pacific zoanthid, foraminifer, jellyfish, and mid-Pacific hard coral). Their respective phylogenetic positions were inferred, and strains that are either closely related to or distinct from previously reported Symbiodinium taxa were revealed. The cultured Symbiodinium strains isolated from individuals of six species of tridacnids and three species of cardiids all had identical ssrRNA gene sequences, are closely related to S. microadriaticum Freudenthal, and are indistinguishable from the RFLP Type A strain previously reported. However, the ssrRNA gene sequences of clam symbionts that were obtained via gene cloning were different from those of the cultured isolates and represent strains that are close to the RFLP Type C strains. The Symbiodinium-like dinoflagellate from the Indo-Pacific sponge Haliclona koremella De Laubenfels is distinct from any of the Symbiodinium taxa studied and may be similar to the symbiont previously isolated from the stony coral Montipora patula Quelch. The isolates from the soft coral Sarcophyton glaucum Quoy et Gaimard and from the zoanthid Zoanthus sp. are both very closely related to S. pilosum Trench et Blank. The free-living Symbiodinium isolate is very closely related to the symbiont isolated from the Indo-Pacific foraminifer Amphisorus hemprichii Ehrenberg, which in turn is distinct from the Red Sea strain isolated from a similar host. Theisolate from Cassiopeia sp. is different from S. microadriaticum F., the type species harbored by Cassiopeia xamachana Bigelow, and is instead very closely related to S. pulchrorum Trench isolated from a sea anemone. The symbiont from the stony coral M. verrucosa Lamarck is a sister taxon to the symbionts isolated from the foraminifera Marginopora kudakajimensis Gudmundsson and Sorites orbiculus Forskål. These data suggest that polymorphic symbioses extend from cnidarians to some bivalve, foraminifer, and jellyfish host species.
Article
SYNOPSIS. The life cycle of the zooxanthella of Cassiopeia sp., as determined by in vitro studies, includes a dominant vegetative autotrophic stage, a reproductive cyst producing autospores, aplanospores, or motile gymnodinioid zoospores, or possible gametes. The predominance of these stages is partially determined by environmental factors, e.g., photoperiodicity. As none of the existing genera of free-living or parasitic algae are wholly applicable to this organism, a new genus, Symbiodinium, is proposed. The type species, S. microadriaticum, is described.
Article
Two species of the colonial green flagellate family Volvocaceae are worldwide in distribution yet exhibit contrasting species structure. Geographically disparate isolates of Gonium pectorale Mueller can interbreed while isolates of Pandorina morum Bory behave quite differently. More than 20 sexually isolated subpopulations occur within this species; these have been termed “syngens” (sensu Sonneborn). Because prezygotic barriers to mating cause intersyngen pairings to fail, breeding analyses cannot be used to estimate genetic relatedness among the syngens of P. morum. DNA comparisons provide an alternative method of assessing genetic relatedness. We compared the nucleotide sequence of the internal transcribed spacer (ITS) region of the nuclear ribosomal repeat among clones of P. morum and of G. pectorale. Members of syngens of P. morum with distribution restricted to one small geographical area show great similarity. Likewise, members of any syngen of worldwide distribution show near uniformity, even those from different continents. However, the ITS sequence of each syngen differs from that of other syngens. In contrast, G. pectorale, which has an ITS region that is remarkably uniform throughout the world, appears to consist of a single syngen within North America and Europe by mating tests. The molecular data are in complete conformity with previous syngen assignment. Because the latter is based on mating affinity, with two complementary mating types per syngen, the evolution of new mating type pairs appears to be the basis of microevolution in these algae. We infer that either P. morum is a more ancient species than G. pectorale or that P. morum has a less stable genome. In either case, the biogeographic distribution of certain syngens may reflect climatological changes of the past.
Article
We examined zooxanthellae diversity in scleractinian corals from southern Taiwan and the Penghu Archipelago, a tropical coral reef and a subtropical non-reefal community, respectively. Zooxanthellae diversity was investigated in 52 species of scleractinian corals from 26 genera and 13 families, using restriction fragment length polymorphism (RFLP), and phylogenetic analyses of the nuclear small-subunit ribosomal DNA (nssrDNA) and large-subunit ribosomal DNA (nlsrDNA). RFLP and phylogenetic analyses of nuclear-encoded ribosomal RNA genes showed that Symbiodinium clade C was the dominant zooxanthellae in scleractinian corals in the seas around Taiwan; Symbiodinium clade D was also found in some species. Both Symbiodinium clade C and D were found in colonies of seven species of scleractinian corals. Symbiodinium clade D was associated with corals that inhabit either shallow water or the reef edge in deep water, supporting the hypothesis that Symbiodinium clade D is a relatively stress-tolerant zooxanthellae found in marginal habitats.
Article
Large-scale coral bleaching episodes are potentially major disturbances to coral reef systems, yet a definitive picture of variation in assemblage response and species susceptibilities is still being compiled. Here, we provide a detailed analysis of the bleaching response of 4160 coral colonies, representing 45 genera and 15 families, from two depths at four sites on reefs fringing inshore islands on the Great Barrier Reef. Six weeks after the onset of large-scale bleaching in 1998, between 11 and 83% of colonies along replicate transects were affected by bleaching, and mortality was 1 to 16%. There were significant differences in bleaching response between sites, depths and taxa. Cyphastrea, Turbinaria and Galaxea were relatively unaffected by bleaching, while most acroporids and pocilloporids were highly susceptible. The hydrocorals (Millepora spp.) were the most susceptible taxa, with 85% mortality. Spatial variation in assemblage response was linked to the taxonomic composition of reef sites and their bleaching history. We suggest, therefore, that much of the spatial variation in bleaching response was due to assemblage composition and thermal acclimation.
Article
Since 2005, advances in next-generation sequencing technologies have revolutionized biological science. The analysis of environmental DNA through the use of specific gene markers such as species-specific DNA barcodes has been a key application of next-generation sequencing technologies in ecological and environmental research. Access to parallel, massive amounts of sequencing data, as well as subsequent improvements in read length and throughput of different sequencing platforms, is leading to a better representation of sample diversity at a reasonable cost. New technologies are being developed rapidly and have the potential to dramatically accelerate ecological and environmental research. The fast pace of development and improvements in next-generation sequencing technologies can reflect on broader and more robust applications in environmental DNA research. Here, we review the advantages and limitations of current next-generation sequencing technologies in regard to their application for environmental DNA analysis.
Article
Marine invertebrates representing at least five phyla are symbiotic with dinoflagellates from the genus Symbiodinium. This group of single-celled protists was once considered to be a single pandemic species, Symbiodinium microadriaticum. Molecular investigations over the past 25 years have revealed, however, that Symbiodinium is a diverse group of organisms with at least eight (A–H) divergent clades that in turn contain multiple molecular subclade types. The diversity within this genus may subsequently determine the response of corals to normal and stressful conditions, leading to the proposal that the symbiosis may impart unusually rapid adaptation to environmental change by the metazoan host. These questions have added importance due to the critical challenges that corals and the reefs they build face as a consequence of current rapid climate change. This review outlines our current understanding of the diverse genus Symbiodinium and explores the ability of this genus and its symbioses to adapt to rapid environmental change.
Article
The study of symbiont cells lost from bleached scleractinian corals Acropora hyacinthus, Favites complanata, and Porites solida and octocorals Sarcophyton ehrenbergi, Sinularia sp., and Xenia sp. using flow cytometry shows that Symbiodinium die from either apoptosis or necrosis. Despite the majority of lost Symbiodinium cells being viable at 28 °C, the predominance of apoptotic and necrotic symbiont cells at higher temperatures indicates that the proportion of live cells decreases with increasing temperature. This implies that reinfection of corals at high temperatures by Symbiodinium lost from scleractinian corals may be less frequent than previously described, since many of the symbiont cells exhibit nonreversible symptoms of approaching cell death. The fraction of viable Symbiodinium cells lost from S. ehrenbergi, Xenia sp., and Sinularia at 32 °C was greater than that at 28 °C. At 34 °C, the fraction of viable cells lost from S. ehrenbergi and Xenia sp. fell but not from Sinularia sp., which suggests that their symbionts have higher temperature tolerances. Thus, Symbiodinium from octocorals may represent “pools” of genetically resistant symbionts available for reinfection of other reef organisms. This has been proposed previously for Symbiodinium in some scleractinian corals, but this is the first evidence for such, particularly for an octocoral. Many of the viable cells, determined using Trypan blue staining techniques, are in fact actually undergoing apoptosis or necrosis, when examined using Annexin V-fluor and propidium iodide staining profiles. The characterization of more apoptotic and necrotic cells than viable cells is critical, as this indicates that the loss of Symbiodinium cells cannot be beneficial to other bleached corals for symbiotic reassociation.
Article
A detailed understanding of how diversity in endosymbiotic dinoflagellate communities maps onto the physiological range of coral hosts is critical to predicting how coral reef ecosystems will respond to climate change. Species-level taxonomy of the dinoflagellate genus Symbiodinium has been predominantly examined using the internal transcribed spacer (ITS) region of the nuclear ribosomal array (rDNA ITS2) and downstream screening for dominant types using denaturing gradient gel electrophoresis (DGGE). Here, ITS2 diversity in the communities of Symbiodinium harboured by two Hawaiian coral species was explored using direct sequencing of clone libraries. We resolved sixfold to eightfold greater diversity per coral species than previously reported, the majority of which corresponds to a novel and distinct phylogenetic lineage. We evaluated how these sequences migrate in DGGE and demonstrate that this method does not effectively resolve this diversity. We conclude that the Porites spp. examined here harbour diverse assemblages of novel Symbiodinium types and that cloning and sequencing is an effective methodological approach for resolving the complexity of endosymbiotic dinoflagellate communities harboured by reef corals.
Article
Aim This study examines the importance of geographic proximity, host life history and regional and local differences in environment (temperature and water clarity) in driving the ecological and evolutionary processes underpinning the global patterns of diversity and distribution of symbiotic dinoflagellates. By comparing and contrasting coral–algal symbioses from isolated regions with differing environmental conditions, we may assess the potential of coral communities to respond to significant changes in climate.
Article
The diversity of symbiotic dinoflagellates (Symbiodinium) in pocilloporid corals originating from various reef habitats surrounding Heron Island, southern Great Barrier Reef, was examined by targeting ribosomal, mitochondrial, and chloroplast genes using six methods that analyse for sequence differences. The ability of each of 13 genetic analyses to characterize eight ecologically distinct Symbiodinium spp. was dependent on the level of conservation of the gene region targeted and the technique used. Other than differences in resolution, phylogenetic reconstructions using nuclear and organelle gene sequences were complementary and when combined produced a well-resolved phylogeny. Analysis of the ribosomal internal transcribed spacers using denaturing gradient gel electrophoresis fingerprinting in combination with sequencing of dominant bands provided a precise method for rapidly resolving and characterizing symbionts into ecologically and evolutionarily distinct units of diversity. Single-stranded conformation polymorphisms of the nuclear ribosomal large subunit (D1/D2 domain) identified the same number of ecologically distinct Symbiodinium spp., but profiles were less distinctive. The repetitive sequencing of bacterially cloned ITS2 polymerase chain reaction amplifications generated numerous sequence variants that clustered together according to the symbiont under analysis. The phylogenetic relationships between these clusters show how intragenomic variation in the ribosomal array diverges among closely related eukaryotic genomes. The strong correlation between phylogenetically independent lineages with different ecological and physiological attributes establishes a clear basis for assigning species designations to members of the genus Symbiodinium.
Article
Zooxanthellae are unicellular algae that occur as endosymbionts in many hundreds of common marine invertebrates. The issue of zooxanthella diversity has been difficult to address. Most zooxanthellae have been placed in the dinoflagellate genus Symbiodinium as one or several species that are not easily distinguished. We compared Symbiodinium and nonsymbiotic dinoflagellates using small ribosomal subunit RNA sequences. Surprisingly, small ribosomal subunit RNA diversity within the genus Symbiodinium is comparable to that observed among different orders of nonsymbiotic dinoflagellates. These data reinforce the conclusion that Symbiodinium-like zooxanthellae represent a collection of distinct species and provide a precedent for a molecular genetic taxonomy of the genus Symbiodinium.
Article
Coral reefs, with their millions of species, have changed profoundly because of the effects of people, and will continue to do so for the foreseeable future. Reefs are subject to many of the same processes that affect other human-dominated ecosystems, but some special features merit emphasis: (i) Many dominant reef builders spawn eggs and sperm into the water column, where fertilization occurs. They are thus particularly vulnerable to Allee effects, including potential extinction associated with chronic reproductive failure. (ii) The corals likely to be most resistant to the effects of habitat degradation are small, short-lived "weedy" corals that have limited dispersal capabilities at the larval stage. Habitat degradation, together with habitat fragmentation, will therefore lead to the establishment of genetically isolated clusters of inbreeding corals. (iii) Increases in average sea temperatures by as little as 1 degrees C, a likely result of global climate change, can cause coral "bleaching" (the breakdown of coral-algal symbiosis), changes in symbiont communities, and coral death. (iv) The activities of people near reefs increase both fishing pressure and nutrient inputs. In general, these processes favor more rapidly growing competitors, often fleshy seaweeds, and may also result in explosions of predator populations. (v) Combinations of stress appear to be associated with threshold responses and ecological surprises, including devastating pathogen outbreaks. (vi) The fossil record suggests that corals as a group are more likely to suffer extinctions than some of the groups that associate with them, whose habitat requirements may be less stringent.
Article
The microbial community associated with the reef building coral Pocillopora damicornis located on the Great Barrier Reef was investigated using culture-independent molecular microbial techniques. The microbial communities of three separate coral colonies were assessed using clone library construction alongside restriction fragment length polymorphism and phylogenetic analysis. Diversity was also investigated spatially across six replicate samples within each single coral colony using 16S rDNA and rpoB-DGGE analysis. Clone libraries demonstrated that the majority of retrieved sequences from coral tissue slurry libraries affiliated with gamma-Proteobacteria. This contrasted with clone libraries of seawater and coral mucus, which were dominated by alpha-Proteobacteria. A number of retrieved clone sequences were conserved between coral colonies; a result consistent with previous studies suggesting a specific microbe-coral association. rpoB-DGGE patterns of replicate tissue slurry samples underestimated microbial diversity, but demonstrated that fingerprints were identical within the same coral. These fingerprints were also conserved across coral colonies. The 16S rDNA-DGGE patterns of replicate tissue slurry samples were more complex, although non-metric multidimensional scaling (nMDS) analysis showed groupings of these banding patterns indicating that some bacterial diversity was uniform within a coral colony. Sequence data retrieved from DGGE analysis support clone library data in that the majority of affiliations were within the gamma-Proteobacteria. Many sequences retrieved also affiliated closely with sequences derived from previous studies of microbial diversity of healthy corals in the Caribbean. Clones showing high 16S rDNA sequence identity to both Vibrio shiloi and Vibrio coralliilyticus were retrieved, suggesting that these may be opportunist pathogens. Comparisons of retrieved microbial diversity between two different sampling methods, a syringe extracted coral mucus sample and an airbrushed coral tissue slurry sample were also investigated. Non-metric multidimensional scaling of clone library data highlighted that clone diversity retrieved from a coral mucus library more closely reflected the diversity of surrounding seawater than a corresponding coral tissue clone library.
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Diversity of symbiotic algae of the genus
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Dong Zj, Huang H, Huang Lm, Li Yc. 2009. Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the
Community analysis of coral mucus-associated bacteria and impact Of temperature and Co2 changes On them (doctoral dissertation
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Fang JH. 2015. Community analysis of coral mucus-associated bacteria and impact Of temperature and Co2 changes On them (doctoral dissertation, Swinburne University Of Technology (Sarawak Campus).