Biology subjects

Voolstra, C. R.

Publications and source records attributed to Voolstra, C. R..

6 recordsLinked to original sources

bioRxiv2017

Aiptasia as a model to study metabolic diversity and specificity in cnidarian-dinoflagellate symbioses

The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis. However, deciphering the individual role of host and algal partners in the uptake and cycling of nutrients has proven difficult, given the endosymbiotic nature of this relationship. In this study, we highlight the advantages of the emerging model system Aiptasia to investigate the metabolic diversity and specificity of cnidarian - dinoflagellate symbiosis. For this, we combined traditional measurements with nano-scale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate carbon and nitrogen cycling both at the organismal scale and the cellular scale. Our results suggest that the individual nutrient assimilation by hosts and symbionts depends on the identity of their respective symbiotic partner. Further,{delta} 13C enrichment patterns revealed that alterations in carbon fixation rates only affected carbon assimilation in the cnidarian host but not the algal symbiont, suggesting a selfish character of this symbiotic association. Based on our findings, we identify new venues for future research regarding the role and regulation of nutrient exchange in the cnidarian - dinoflagellate symbiosis. In this context, the model system approach outlined in this study constitutes a powerful tool set to address these questions.

physiology↗

bioRxiv2017

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research is focusing on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, which have been implicated in transcriptional regulation and acclimation to environmental change, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We find methylated genes are marked by histone H3K36me3 and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes such as immunity, apoptosis, phagocytosis recognition and phagosome formation, and unveil intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis during symbiosis.

ecology↗

bioRxiv2017

Coral reef carbonate budgets and ecological drivers in the naturally high temperature and high alkalinity environment of the Red Sea

The coral structural framework is crucial for maintaining reef ecosystem function and services. In the central Red Sea, a naturally high alkalinity is beneficial to reef growth, but rising water temperatures impair the calcification capacity of reef-building organisms. However, it is currently unknown how beneficial and detrimental factors affect the balance between calcification and erosion, and thereby the overall growth of the reef framework. To provide insight into present-day carbonate budgets and reef growth dynamics in the central Red Sea, we measured in situ net-accretion and net-erosion rates (Gnet) by deployment of limestone blocks and estimated census-based carbonate budgets (Gbudget) in four reef sites along a cross-shelf gradient (25 km). We assessed abiotic variables (i.e., temperature, inorganic nutrients, and carbonate system variables) and biotic drivers (i.e., calcifier and bioeroder abundances). On average, total alkalinity AT (2346 - 2431 mol kg-1), aragonite saturation state (4.5 - 5.2 {Omega}a), and pCO2 (283 -315 atm) were close to estimates of pre-industrial global ocean surface waters. Despite these calcification-favorable carbonate system conditions, Gnet and Gbudget encompassed positive (offshore) and negative net-production (midshore-lagoon and exposed nearshore site) estimates. Notably, Gbudget maxima were lower compared to reef growth from pristine Indian Ocean sites. Yet, a comparison with historical data from the northern Red Sea suggests that overall reef growth in the Red Sea has likely remained similar since 1995. When assessing sites across the shelf gradient, AT correlated well with reef growth rates ({rho} = 0.89), while temperature was a weaker, negative correlate ({rho} = -0.71). Further, AT explained about 65 % of Gbudget in a best fitting distance-based linear model. Interestingly, parrotfish abundances added up to 82% of explained variation, further substantiating recent studies highlighting the importance of parrotfish to reef ecosystem function. Our study provides a baseline that will be particularly useful in assessing future trajectories of reef growth capacities in the Red Sea under continuous ocean warming and acidification.

ecology↗

bioRxiv2017

Symbiodinium genomes reveal adaptive evolution of functions related to symbiosis

Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the worlds coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp), previously sequenced as strain CCMP2468, to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identified extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding Symbiodinium biology and the coral-algal symbiosis.

genomics↗

bioRxiv2017

Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Similarly, genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Importantly, if the patterns elucidated here are representative of differences between corals from the robust and complex clade, the ability of a coral to respond to climate change may be dependent on its clade association.

genomics↗

bioRxiv2017

Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

Over the last century, the anthropogenic production of CO2 has led to warmer (+0.74 {degrees}C) and more acidic (-0.1 pH) oceans1, resulting in increasingly frequent and severe mass bleaching events worldwide that precipitate global coral reef decline2,3. To mitigate this decline, proposals to augment the stress tolerance of corals through genetic and non-genetic means have been gaining traction4. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization5,6. While DNA methylation has been observed in corals7-10, its potential role in phenotypic plasticity has not yet been described. Here, we show that, similar to findings in mice11, DNA methylation significantly reduces spurious transcription in the Red Sea coral Stylophora pistillata, suggesting the evolutionary conservation of this essential mechanism in corals. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the maintenance of linear extension rates under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization, providing corals with an additional mechanism to cope with climate change.

ecology↗