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1. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium

   https://doi.org/10.1186/s12915-021-00994-6  

   González-Pech, Raúl A. ; Stephens, Timothy G. ; Chen, Yibi ; Mohamed, Amin R. ; Cheng, Yuanyuan ; Shah, Sarah ; Dougan, Katherine E. ; Fortuin, Michael D. ; Lagorce, Rémi ; Burt, David W. ; et al ( December 2021 , BMC Biology)

   Abstract Background Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Breakdown of the coral-dinoflagellate symbiosis due to environmental stress (i.e. coral bleaching) can lead to coral death and the potential collapse of reef ecosystems. However, evolution of Symbiodiniaceae genomes, and its implications for the coral, is little understood. Genome sequences of Symbiodiniaceae remain scarce due in part to their large genome sizes (1–5 Gbp) and idiosyncratic genome features. Results Here, we present de novo genome assemblies of seven members of the genus Symbiodinium , of which two are free-living,more »one is an opportunistic symbiont, and the remainder are mutualistic symbionts. Integrating other available data, we compare 15 dinoflagellate genomes revealing high sequence and structural divergence. Divergence among some Symbiodinium isolates is comparable to that among distinct genera of Symbiodiniaceae. We also recovered hundreds of gene families specific to each lineage, many of which encode unknown functions. An in-depth comparison between the genomes of the symbiotic Symbiodinium tridacnidorum (isolated from a coral) and the free-living Symbiodinium natans reveals a greater prevalence of transposable elements, genetic duplication, structural rearrangements, and pseudogenisation in the symbiotic species. Conclusions Our results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome divergence, and the diversification of Symbiodinium and Symbiodiniaceae. The divergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history.« less
2. Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single exon genes with adaptive functions

   https://doi.org/10.1186/s12915-020-00782-8  

   Stephens, T. G. ; González-Pech, R. A. ; Cheng, Y. ; Mohamed, A. R. ; Burt, D. W. ; Bhattacharya, D. ; Ragan, M. A. ; Chan, C. X. ( January 2020 , BMC biology)

   Background: Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxamore »that have smaller genome size ranges, while genomic information from more diverse free living species is still lacking. Results: Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which ~40% are in unidirectional gene clusters and ~25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates. Conclusions: Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution.« less
3. Alignment-Free Analysis of Whole-Genome Sequences From Symbiodiniaceae Reveals Different Phylogenetic Signals in Distinct Regions

   https://doi.org/10.3389/fpls.2022.815714  

   Lo, Rosalyn ; Dougan, Katherine E. ; Chen, Yibi ; Shah, Sarah ; Bhattacharya, Debashish ; Chan, Cheong Xin ( April 2022 , Frontiers in Plant Science)

   Dinoflagellates of the family Symbiodiniaceae are predominantly essential symbionts of corals and other marine organisms. Recent research reveals extensive genome sequence divergence among Symbiodiniaceae taxa and high phylogenetic diversity hidden behind subtly different cell morphologies. Using an alignment-free phylogenetic approach based on sub-sequences of fixed length k (i.e. k -mers), we assessed the phylogenetic signal among whole-genome sequences from 16 Symbiodiniaceae taxa (including the genera of Symbiodinium , Breviolum , Cladocopium , Durusdinium and Fugacium ) and two strains of Polarella glacialis as outgroup. Based on phylogenetic trees inferred from k -mers in distinct genomic regions (i.e. repeat-masked genome sequences,more »protein-coding sequences, introns and repeats) and in protein sequences, the phylogenetic signal associated with protein-coding DNA and the encoded amino acids is largely consistent with the Symbiodiniaceae phylogeny based on established markers, such as large subunit rRNA. The other genome sequences (introns and repeats) exhibit distinct phylogenetic signals, supporting the expected differential evolutionary pressure acting on these regions. Our analysis of conserved core k -mers revealed the prevalence of conserved k -mers (>95% core 23-mers among all 18 genomes) in annotated repeats and non-genic regions of the genomes. We observed 180 distinct repeat types that are significantly enriched in genomes of the symbiotic versus free-living Symbiodinium taxa, suggesting an enhanced activity of transposable elements linked to the symbiotic lifestyle. We provide evidence that representation of alignment-free phylogenies as dynamic networks enhances the ability to generate new hypotheses about genome evolution in Symbiodiniaceae. These results demonstrate the potential of alignment-free phylogenetic methods as a scalable approach for inferring comprehensive, unbiased whole-genome phylogenies of dinoflagellates and more broadly of microbial eukaryotes.« less
4. Genome Evolution of Coral Reef Symbionts as Intracellular Residents

   https://doi.org/10.1016/j.tree.2019.04.010  

   González-Pech, R. A. ; Bhattacharya, D. ; Ragan, M. A. ; Chan, C. X. ( January 2019 , Trends in ecology evolution)

   Coral reefs are sustained by symbioses between corals and symbiodiniacean dinoflagellates. These symbioses vary in the extent of their permanence in and specificity to the host. Although dinoflagellates are primarily free-living, Symbiodiniaceae diversified mainly as symbiotic lineages. Their genomes reveal conserved symbiosis-related gene functions and high sequence divergence. However, the evolutionary mechanisms that underpin the transition from the free-living lifestyle to symbiosis remain poorly understood. Here, we discuss the genome evolution of Symbiodiniaceae in diverse ecological niches across the broad spectrum of symbiotic associations, from free-living to putative obligate symbionts. We pose key questions regarding genome evolution vis-à-vis the transitionmore »of dinoflagellates from free-living to symbiotic and propose strategies for future research to better understand coral-dinoflagellate and other eukaryote-eukaryote symbioses.« less
5. Heat Stress of Algal Partner Hinders Colonization Success and Alters the Algal Cell Surface Glycome in a Cnidarian-Algal Symbiosis

   https://doi.org/10.1128/spectrum.01567-22  

   Maruyama, Shumpei ; Mandelare-Ruiz, Paige E. ; McCauley, Mark ; Peng, Wenjing ; Cho, Byeong Gwan ; Wang, Junyao ; Mechref, Yehia ; Loesgen, Sandra ; Weis, Virginia M. ( May 2022 , Microbiology Spectrum)

   Kormas, Konstantinos Aristomenis (Ed.)

   ABSTRACT Corals owe their ecological success to their symbiotic relationship with dinoflagellate algae (family Symbiodiniaceae). While the negative effects of heat stress on this symbiosis are well studied, how heat stress affects the onset of symbiosis and symbiont specificity is less explored. In this work, we used the model sea anemone, Exaiptasia diaphana (commonly referred to as Aiptasia), and its native symbiont, Breviolum minutum , to study the effects of heat stress on the colonization of Aiptasia by algae and the algal cell-surface glycome. Heat stress caused a decrease in the colonization of Aiptasia by algae that were not duemore »to confounding variables such as algal motility or oxidative stress. With mass spectrometric analysis and lectin staining, a thermally induced enrichment of glycans previously found to be associated with free-living strains of algae (high-mannoside glycans) and a concomitant reduction in glycans putatively associated with symbiotic strains of algae (galactosylated glycans) were identified. Differential enrichment of specific sialic acid glycans was also identified, although their role in this symbiosis remains unclear. We also discuss the methods used to analyze the cell-surface glycome of algae, evaluate current limitations, and provide suggestions for future work in algal-coral glycobiology. Overall, this study provided insight into how stress may affect the symbiosis between cnidarians and their algal symbionts by altering the glycome of the symbiodinian partner. IMPORTANCE Coral reefs are under threat from global climate change. Their decline is mainly caused by the fragility of their symbiotic relationship with dinoflagellate algae which they rely upon for their ecological success. To better understand coral biology, researchers used the sea anemone, Aiptasia, a model system for the study of coral-algal symbiosis, and characterized how heat stress can alter the algae's ability to communicate to the coral host. This study found that heat stress caused a decline in algal colonization success and impacted the cell surface molecules of the algae such that it became more like that of nonsymbiotic species of algae. This work adds to our understanding of the molecular signals involved in coral-algal symbiosis and how it breaks down during heat stress.« less