Detecting Photosymbiosis in Fossil Scleractinian Corals.
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ABSTRACT:
SUBMITTER: Tornabene C
PROVIDER: S-EPMC5572714 | biostudies-literature | 2017 Aug
REPOSITORIES: biostudies-literature
Publications
Detecting Photosymbiosis in Fossil Scleractinian Corals.
Tornabene Chiara C Martindale Rowan C RC Wang Xingchen T XT Schaller Morgan F MF
Scientific reports 20170825 1
The evolutionary success of reef-building corals is often attributed to photosymbiosis, a mutualistic relationship scleractinian corals developed with zooxanthellae; however, because zooxanthellae are not fossilized, it is difficult (and contentious) to determine whether ancient corals harbored symbionts. In this study, we analyze the δ<sup>15</sup>N of skeletal organic matrix in a suite of modern and fossil scleractinian corals (zooxanthellate- and azooxanthellate-like) with varying levels of d ...[more]
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Project description:During the Carnian, oligotrophic shallow-water regions of the western Tethys were occupied by small, coral-rich patch reefs. Scleractinian corals, which already contributed to the formation of the reef structure, owed their position most probably to the symbiosis with dinoflagellate algae (zooxanthellae). Using microstructural (regularity of growth increments) and geochemical (oxygen and carbon stable isotopes) criteria of zooxanthellae symbiosis, we investigated whether this partnership was widespread among Carnian scleractinians from the Italian Dolomites (locality Alpe di Specie). Although corals from this locality are renowned from excellent mineralogical preservation (aragonite), their skeletons were rigorously tested against traces of diagenesis Irrespective of their growth forms, well preserved skeletons of corals from the Dolomites, most frequently revealed regular growth bands (low values of coefficient of variation) typical of modern zooxanthellate corals. Paradoxically, some Carnian taxa (Thamnasteriomorpha frechi and Thamnasteriomorphasp.)with highly integrated thamnasterioid colonies which today are formed exclusively by zooxanthellate corals, showed irregular fine-scale growth bands (coefficient of variation of 40% and 41% respectively) that could suggest their asymbiotic status. However, similar irregular skeletal banding is known also in some modern agariciids (Leptoseris fragilis) which are symbiotic with zooxanthellae. This may point to a similar ecological adaptation of Triassic taxa with thamnasterioid colonies. Contrary to occasionally ambiguous interpretation of growth banding, all examined Carnian corals exhibited lack of distinct correlation between carbon (δ 13C range between 0.81‰ and 5.81‰) and oxygen (δ 18O values range between -4.21‰ and -1.06‰) isotope composition of the skeleton which is consistent with similar pattern in modern zooxanthellates. It is therefore highly likely, that Carnian scleractinian corals exhibited analogous ecological adaptations as modern symbiotic corals and that coral-algal symbiosis that spread across various clades of Scleractinia preceded the reef bloom at the end of the Triassic.
| S-EPMC7977380 | biostudies-literature
Project description:Understanding the evolution of scleractinian corals on geological timescales is key to predict how modern reef ecosystems will react to changing environmental conditions in the future. Important to such efforts has been the development of several skeleton-based criteria to distinguish between the two major ecological groups of scleractinians: zooxanthellates, which live in symbiosis with dinoflagellate algae, and azooxanthellates, which lack endosymbiotic dinoflagellates. Existing criteria are based on overall skeletal morphology and bio/geo-chemical indicators-none of them being particularly robust. Here we explore another skeletal feature, namely fine-scale growth banding, which differs between these two groups of corals. Using various ultra-structural imaging techniques (e.g., TEM, SEM, and NanoSIMS) we have characterized skeletal growth increments, composed of doublets of optically light and dark bands, in a broad selection of extant symbiotic and asymbiotic corals. Skeletons of zooxanthellate corals are characterized by regular growth banding, whereas in skeletons of azooxanthellate corals the growth banding is irregular. Importantly, the regularity of growth bands can be easily quantified with a coefficient of variation obtained by measuring bandwidths on SEM images of polished and etched skeletal surfaces of septa and/or walls. We find that this coefficient of variation (lower values indicate higher regularity) ranges from ~40 to ~90% in azooxanthellate corals and from ~5 to ~15% in symbiotic species. With more than 90% (28 out of 31) of the studied corals conforming to this microstructural criterion, it represents an easy and robust method to discriminate between zooxanthellate and azooxanthellate corals. This microstructural criterion has been applied to the exceptionally preserved skeleton of the Triassic (Norian, ca. 215 Ma) scleractinian Volzeia sp., which contains the first example of regular, fine-scale banding of thickening deposits in a fossil coral of this age. The regularity of its growth banding strongly suggests that the coral was symbiotic with zooxanthellates.
| S-EPMC4713449 | biostudies-literature
Project description:Roughly 240 million years ago (Ma), scleractinian corals rapidly expanded and diversified across shallow marine environments. The main driver behind this evolution is uncertain, but the ecological success of modern reef-building corals is attributed to their nutritional symbiosis with photosynthesizing dinoflagellate algae. We show that a suite of exceptionally preserved Late Triassic (ca. 212 Ma) coral skeletons from Antalya (Turkey) have microstructures, carbonate 13C/12C and 18O/16O, and intracrystalline skeletal organic matter 15N/14N all indicating symbiosis. This includes species with growth forms conventionally considered asymbiotic. The nitrogen isotopes further suggest that their Tethys Sea habitat was a nutrient-poor, low-productivity marine environment in which photosymbiosis would be highly advantageous. Thus, coral-dinoflagellate symbiosis was likely a key driver in the evolution and expansion of shallow-water scleractinians.
| S-EPMC5099983 | biostudies-literature
Project description:Animals rely on their diet for amino acids that they are incapable either of synthesizing or of synthesizing in sufficient quantities to meet metabolic needs. These are the so-called 'essential amino acids'. This set of amino acids is similar among the vertebrates and many of the invertebrates. Previously, no information was available for amino acid synthesis by the most primitive invertebrates, the Cnidaria. The purpose of this study was to examine amino acid synthesis by representative cnidarians within the Order Scleractinia. Three species of zooxanthellate reef coral, Montastraea faveolata, Acropora cervicornis and Porites divaricata, and two species of non-zooxanthellate coral, Tubastrea coccinea and Astrangia poculata, were incubated with 14C-labelled glucose or with the 14C-labelled amino acids glutamic acid, lysine or valine. Radiolabel tracer was followed into protein amino acids. A total of 17 amino acids, including hydroxyproline, were distinguishable by the techniques used. Of these, only threonine was not found radiolabelled in any of the samples. We could not detect tryptophan or cysteine, nor distinguish between the amino acid pairs glutamic acid and glutamine, or aspartic acid and asparagine. Eight amino acids normally considered essential for animals were made by the five corals tested, although some of them were made only in small quantities. These eight amino acids are valine, isoleucine, leucine, tyrosine, phenylalanine histidine, methionine and lysine. The ability of cnidarians to synthesize these amino acids could be yet another indicator of a separate evolutionary history of the cnidarians from the rest of the Metazoa.
| S-EPMC1218179 | biostudies-other
Project description:Background Coral reefs belong to the most ecologically and economically important ecosystems on our planet. Yet, they are under steady decline worldwide due to rising sea surface temperatures, disease, and pollution. Understanding the molecular impact of these stressors on different coral species is imperative in order to predict how coral populations will respond to this continued disturbance. The use of molecular tools such as microarrays has provided deep insight into the molecular stress response of corals. Here, we have performed comparative genomic hybridizations (CGH) with different coral species to an Acropora palmata microarray platform containing 13,546 cDNA clones in order to identify potentially rapidly evolving genes and to determine the suitability of existing microarray platforms for use in gene expression studies (via heterologous hybridization). Results Our results showed that the current microarray platform for A. palmata is able to provide biological relevant information for a wide variety of coral species covering both the complex clade as well the robust clade. Analysis of the fraction of highly diverged genes showed a significantly higher amount of genes without annotation corroborating previous findings that point towards a higher rate of divergence for taxonomically restricted genes. Among the genes with annotation, we found many mitochondrial genes to be highly diverged in M. faveolata when compared to A. palmata, while the majority of nuclear encoded genes maintained an average divergence rate. Conclusions The use of present microarray platforms for transcriptional analyses in different coral species will greatly enhance the understanding of the molecular basis of stress and health and highlight evolutionary differences between scleractinian coral species. On a genomic basis, we show that cDNA arrays can be used to identify patterns of divergence. Mitochondrion-encoded genes seem to have diverged faster than nuclear encoded genes in robust corals. Accordingly, this needs to be taken into account when using mitochondrial markers for scleractinian phylogenies.
2012-11-22 | GSE37279 | GEO
Project description:While recent strides have been made in understanding the biological process by which stony corals calcify, much remains to be revealed, including the ubiquity across taxa of specific biomolecules involved. Several proteins associated with this process have been identified through proteomic profiling of the skeletal organic matrix (SOM) extracted from three scleractinian species. However, the evolutionary history of this putative "biomineralization toolkit," including the appearance of these proteins' throughout metazoan evolution, remains to be resolved. Here we used a phylogenetic approach to examine the evolution of the known scleractinians' SOM proteins across the Metazoa. Our analysis reveals an evolutionary process dominated by the co-option of genes that originated before the cnidarian diversification. Each one of the three species appears to express a unique set of the more ancient genes, representing the independent co-option of SOM proteins, as well as a substantial proportion of proteins that evolved independently. In addition, in some instances, the different species expressed multiple orthologous proteins sharing the same evolutionary history. Furthermore, the non-random clustering of multiple SOM proteins within scleractinian-specific branches suggests the conservation of protein function between distinct species for what we posit is part of the scleractinian "core biomineralization toolkit." This "core set" contains proteins that are likely fundamental to the scleractinian biomineralization mechanism. From this analysis, we infer that the scleractinians' ability to calcify was achieved primarily through multiple lineage-specific protein expansions, which resulted in a new functional role that was not present in the parent gene.
| S-EPMC7902050 | biostudies-literature
Project description:Background Coral reefs belong to the most ecologically and economically important ecosystems on our planet. Yet, they are under steady decline worldwide due to rising sea surface temperatures, disease, and pollution. Understanding the molecular impact of these stressors on different coral species is imperative in order to predict how coral populations will respond to this continued disturbance. The use of molecular tools such as microarrays has provided deep insight into the molecular stress response of corals. Here, we have performed comparative genomic hybridizations (CGH) with different coral species to an Acropora palmata microarray platform containing 13,546 cDNA clones in order to identify potentially rapidly evolving genes and to determine the suitability of existing microarray platforms for use in gene expression studies (via heterologous hybridization). Results Our results showed that the current microarray platform for A. palmata is able to provide biological relevant information for a wide variety of coral species covering both the complex clade as well the robust clade. Analysis of the fraction of highly diverged genes showed a significantly higher amount of genes without annotation corroborating previous findings that point towards a higher rate of divergence for taxonomically restricted genes. Among the genes with annotation, we found many mitochondrial genes to be highly diverged in M. faveolata when compared to A. palmata, while the majority of nuclear encoded genes maintained an average divergence rate. Conclusions The use of present microarray platforms for transcriptional analyses in different coral species will greatly enhance the understanding of the molecular basis of stress and health and highlight evolutionary differences between scleractinian coral species. On a genomic basis, we show that cDNA arrays can be used to identify patterns of divergence. Mitochondrion-encoded genes seem to have diverged faster than nuclear encoded genes in robust corals. Accordingly, this needs to be taken into account when using mitochondrial markers for scleractinian phylogenies. Microarray experiments were performed as follows. Appropriate Cy3 and Cy5 labeled DNAs were mixed together in a hybridization buffer containing 0.25% SDS, 25 mM HEPES and 3 × SSC, resulting in a final volume of 70?l. The hybridization mixtures were boiled for 2 min at 99°C and allowed to cool at room temperature for 5 min. The cooled hybridization mixtures were pipetted under an mSeries Lifterslip (Erie Scientific), and hybridization took place in Corning hybridization chambers overnight at 55°C. Microarrays were washed once in 2 × SSC, 0.03% SDS heated to 55 °C for 5 min. followed by one wash in 1 x SSC and another wash in 0.2 x SSC for 5 min each. The slides were kept in 0.2 × SSC until analysis. Slides were dried via centrifugation and scanned using an Axon 4000B scanner. The experimental setup followed a reference design, i.e., all samples were hybridized against the same pool of labeled A. palmata DNA. For each species, a total of four hybridizations were performed, including two dye swap hybridizations in order to account for potential dye bias i.e. two hybridizations with Cy3 labeled M. faveolata DNA against a Cy5 labeled A. palmata reference and two hybridizations with Cy5 labeled M. faveolata DNA against a Cy3 labeled Cy3 A. palmata reference were performed. The same hybridization scheme was used for A. cervicornis and S. radians.
2012-11-22 | E-GEOD-37279 | biostudies-arrayexpress
Project description:Flexibility in biological systems is seen as an important driver of macro-ecosystem function and stability. Spatially constrained endosymbiotic settings, however, are less studied, although environmental thresholds of symbiotic corals are linked to the function of their endosymbiotic dinoflagellate communities. Symbiotic flexibility is a hypothesized mechanism that corals may exploit to adapt to climate change. This study explores the flexibility of the coral-Symbiodinium symbiosis through quantification of Symbiodinium ITS2 sequence assemblages in a range of coral species and genera. Sequence assemblages are expressed as an index of flexibility incorporating phylogenetic divergence and relative abundance of Symbiodinium sequences recovered from the host. This comparative analysis reveals profound differences in the flexibility of corals for Symbiodinium, thereby classifying corals as generalists or specifists. Generalists such as Acropora and Pocillopora exhibit high intra- and inter-species flexibility in their Symbiodinium assemblages and are some of the most environmentally sensitive corals. Conversely, specifists such as massive Porites colonies exhibit low flexibility, harbour taxonomically narrow Symbiodinium assemblages, and are environmentally resistant corals. Collectively, these findings challenge the paradigm that symbiotic flexibility enhances holobiont resilience. This underscores the need for a deeper examination of the extent and duration of the functional benefits associated with endosymbiotic diversity and flexibility under environmental stress.
| S-EPMC3479799 | biostudies-literature
Project description:BACKGROUND: Coral reefs belong to the most ecologically and economically important ecosystems on our planet. Yet, they are under steady decline worldwide due to rising sea surface temperatures, disease, and pollution. Understanding the molecular impact of these stressors on different coral species is imperative in order to predict how coral populations will respond to this continued disturbance. The use of molecular tools such as microarrays has provided deep insight into the molecular stress response of corals. Here, we have performed comparative genomic hybridizations (CGH) with different coral species to an Acropora palmata microarray platform containing 13,546 cDNA clones in order to identify potentially rapidly evolving genes and to determine the suitability of existing microarray platforms for use in gene expression studies (via heterologous hybridization). RESULTS: Our results showed that the current microarray platform for A. palmata is able to provide biological relevant information for a wide variety of coral species covering both the complex clade as well the robust clade. Analysis of the fraction of highly diverged genes showed a significantly higher amount of genes without annotation corroborating previous findings that point towards a higher rate of divergence for taxonomically restricted genes. Among the genes with annotation, we found many mitochondrial genes to be highly diverged in M. faveolata when compared to A. palmata, while the majority of nuclear encoded genes maintained an average divergence rate. CONCLUSIONS: The use of present microarray platforms for transcriptional analyses in different coral species will greatly enhance the understanding of the molecular basis of stress and health and highlight evolutionary differences between scleractinian coral species. On a genomic basis, we show that cDNA arrays can be used to identify patterns of divergence. Mitochondrion-encoded genes seem to have diverged faster than nuclear encoded genes in robust corals. Accordingly, this needs to be taken into account when using mitochondrial markers for scleractinian phylogenies.
| S-EPMC3469353 | biostudies-literature
Project description:The combination of coloniality and symbiosis in Scleractinia is thought to confer competitive advantage over other benthic invertebrates, and it is likely the key factor for the dominance of corals in tropical reefs. However, the extant Scleractinia are evenly split between zooxanthellate and azooxanthellate species. Most azooxanthellate species are solitary and nearly absent from reefs, but have much wider geographic and bathymetric distributions than reef corals. Molecular phylogenetic analyses have repeatedly recovered clades formed by colonial/zooxanthellate and solitary/azooxanthellate taxa, suggesting that coloniality and symbiosis were repeatedly acquired and/or lost throughout the history of the Scleractinia. Using Bayesian ancestral state reconstruction, we found that symbiosis was lost at least three times and coloniality lost at least six times, and at least two instances in which both characters were lost. All of the azooxanthellate lineages originated from ancestors that were reconstructed as symbiotic, corroborating the onshore-offshore diversification trend recorded in marine taxa. Symbiotic sister taxa of two of these descendant lineages are extant in Caribbean reefs but disappeared from the Mediterranean before the end of the Miocene, whereas extant azooxanthellate lineages have trans-Atlantic distributions. Thus, the phyletic link between reef and nonreef communities may have played an important role in the dynamics of extinction and recovery that marks the evolutionary history of scleractinians, and some reef lineages may have escaped local extinction by diversifying into offshore environments. However, this macroevolutionary mechanism offers no hope of mitigating the effects of climate change on coral reefs in the next century.
| S-EPMC2900674 | biostudies-literature