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. 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. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.
Brüwer, Jan D.; Voolstra, Christian R.(PeerJ, PeerJ, 2018-03-01)[Article]
Current research posits that all multicellular organisms live in symbioses with associated microorganisms and form so-called metaorganisms or holobionts. Cnidarian metaorganisms are of specific interest given that stony corals provide the foundation of the globally threatened coral reef ecosystems. To gain first insight into viruses associated with the coral model system Aiptasia (sensu Exaiptasia pallida), we analyzed an existing RNA-Seq dataset of aposymbiotic, partially populated, and fully symbiotic Aiptasia CC7 anemones with Symbiodinium. Our approach included the selective removal of anemone host and algal endosymbiont sequences and subsequent microbial sequence annotation. Of a total of 297 million raw sequence reads, 8.6 million (∼3%) remained after host and endosymbiont sequence removal. Of these, 3,293 sequences could be assigned as of viral origin. Taxonomic annotation of these sequences suggests that Aiptasia is associated with a diverse viral community, comprising 116 viral taxa covering 40 families. The viral assemblage was dominated by viruses from the families Herpesviridae (12.00%), Partitiviridae (9.93%), and Picornaviridae (9.87%). Despite an overall stable viral assemblage, we found that some viral taxa exhibited significant changes in their relative abundance when Aiptasia engaged in a symbiotic relationship with Symbiodinium. Elucidation of viral taxa consistently present across all conditions revealed a core virome of 15 viral taxa from 11 viral families, encompassing many viruses previously reported as members of coral viromes. Despite the non-random selection of viral genetic material due to the nature of the sequencing data analyzed, our study provides a first insight into the viral community associated with Aiptasia. Similarities of the Aiptasia viral community with those of corals corroborate the application of Aiptasia as a model system to study coral holobionts. Further, the change in abundance of certain viral taxa across different symbiotic states suggests a role of viruses in the algal endosymbiosis, but the functional significance of this remains to be determined.
Pogoreutz, Claudia; Radecker, Nils; Cardenas, Anny; Gärdes, Astrid; Wild, Christian; Voolstra, Christian R.(Ecology and Evolution, Wiley, 2018-01-25)[Article]
The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host-microbe associations under adverse environmental conditions. To gain insight into the stability of coral host-microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora-associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.
Bayer, Till; Aranda, Manuel; Sunagawa, Shinichi; Yum, Lauren; Desalvo, Michael K; Lindquist, Erika; Coffroth, Mary Alice; Voolstra, Christian R.; Medina, Mónica(PLoS ONE, Public Library of Science (PLoS), 2012-04-18)[Article]
Dinoflagellates are unicellular algae that are ubiquitously abundant in aquatic environments. Species of the genus Symbiodinium form symbiotic relationships with reef-building corals and other marine invertebrates. Despite their ecologic importance, little is known about the genetics of dinoflagellates in general and Symbiodinium in particular. Here, we used 454 sequencing to generate transcriptome data from two Symbiodinium species from different clades (clade A and clade B). With more than 56,000 assembled sequences per species, these data represent the largest transcriptomic resource for dinoflagellates to date. Our results corroborate previous observations that dinoflagellates possess the complete nucleosome machinery. We found a complete set of core histones as well as several H3 variants and H2A.Z in one species. Furthermore, transcriptome analysis points toward a low number of transcription factors in Symbiodinium spp. that also differ in the distribution of DNA-binding domains relative to other eukaryotes. In particular the cold shock domain was predominant among transcription factors. Additionally, we found a high number of antioxidative genes in comparison to non-symbiotic but evolutionary related organisms. These findings might be of relevance in the context of the role that Symbiodinium spp. play as coral symbionts.Our data represent the most comprehensive dinoflagellate EST data set to date. This study provides a comprehensive resource to further analyze the genetic makeup, metabolic capacities, and gene repertoire of Symbiodinium and dinoflagellates. Overall, our findings indicate that Symbiodinium possesses some unique characteristics, in particular the transcriptional regulation in Symbiodinium may differ from the currently known mechanisms of eukaryotic gene regulation.
DeSalvo, MK; Sunagawa, S; Voolstra, Christian R.; Medina, M(Marine Ecology Progress Series, Inter-Research Science Center, 2010-03-08)[Article]
The emergence of genomic tools for reef-building corals and symbiotic anemones comes at a time when alarming losses in coral cover are being observed worldwide. These tools hold great promise in elucidating novel and unforeseen cellular processes underlying the successful mutualism between corals and their dinoflagellate endosymbionts Symbiodinium spp. Since thermal stress triggers a breakdown in the symbiosis (coral bleaching), measuring the transcriptomic response to thermal stress-induced bleaching offers an extraordinary view of cellular processes that are specific to coral–algal symbioses. In the present study, we utilized a cDNA microarray containing 2059 genes of the threatened Caribbean elkhorn coral Acropora palmata to identify genes that are differentially expressed upon thermal stress. Fragments from replicate colonies were exposed to elevated temperature for 2 d, and samples were frozen for microarray analysis after 24 and 48 h. Totals of 204 and 104 genes were differentially expressed in samples that were collected 1 and 2 d after thermal stress, respectively. Analysis of the differentially expressed genes indicates a cellular stress response in A. palmata involving (1) growth arrest, (2) chaperone activity, (3) nucleic acid stabilization and repair, and (4) removal of damaged macromolecules. Other differentially expressed processes include sensory perception, metabolite transfer between host and endosymbiont, nitric oxide signaling, and modifications to the actin cytoskeleton and extracellular matrix. The results are compared with those from a previous coral microarray study of thermal stress in Montastraea faveolata, and point to an overall evolutionary conserved bleaching response in scleractinian corals.
Voolstra, Christian R.; Sunagawa, Shinichi; Matz, Mikhail V; Bayer, Till; Aranda, Manuel; Buschiazzo, Emmanuel; Desalvo, Michael K; Lindquist, Erika; Szmant, Alina M; Coffroth, Mary Alice; Medina, Mónica(PLoS ONE, Public Library of Science (PLoS), 2011-05-25)[Article]
Corals worldwide are in decline due to climate change effects (e.g., rising seawater temperatures), pollution, and exploitation. The ability of corals to cope with these stressors in the long run depends on the evolvability of the underlying genetic networks and proteins, which remain largely unknown. A genome-wide scan for positively selected genes between related coral species can help to narrow down the search space considerably.
Polato, Nicholas R; Voolstra, Christian R.; Schnetzer, Julia; DeSalvo, Michael K; Randall, Carly J; Szmant, Alina M; Medina, Mónica; Baums, Iliana B(PLoS ONE, Public Library of Science (PLoS), 2010-06-23)[Article]
The potential to adapt to a changing climate depends in part upon the standing genetic variation present in wild populations. In corals, the dispersive larval phase is particularly vulnerable to the effects of environmental stress. Larval survival and response to stress during dispersal and settlement will play a key role in the persistence of coral populations.
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