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Evolution and adaptation of non-symbiotic Symbiodiniaceae

Authors: Sarah Shah;

Evolution and adaptation of non-symbiotic Symbiodiniaceae

Abstract

Reef-building corals are critically sustained by symbiosis between corals and dinoflagellates of the Family Symbiodiniaceae. The Symbiodiniaceae progenitor, however, is thought to have been free-living, suggesting that the establishment of symbiosis, i.e., symbiogenesis, occurred after or along with the diversification of the Family. Previous studies of genome-scale data largely focused on the symbiotic lineages, and revealed lineage-specific functional innovations and differential gene expression in response to heat stress or in symbiosis with hosts. This thesis work aimed to investigate the impact of symbiogenesis in Symbiodiniaceae genome evolution by incorporating new genome data from non-symbiotic members as a reference. Specifically, this research focused on the early-diverging, free-living symbiodiniacean genus of Effrenium, which is expected to not have been impacted by symbiogenesis. De novo genome assemblies and associated transcriptomes were generated from three isolates of Effrenium voratum, the only known species of Effrenium. Comparing the genomes and gene features of E. voratum to other dinoflagellates (including its symbiotic sisters in the Family and the psychrophilic free-living Polarella glacialis as outgroup) led to evidence that a massive genome reduction likely occurred before the diversification of Symbiodiniaceae and the emergence of symbiogenesis. Large numbers of protein families (~3,000) were found to have likely arisen from convergent evolution in the symbiotic lineages of Symbiodiniaceae, and E. voratum uniquely conserved genomic hallmarks (e.g., large introns, low pseudogenisation) that are common in other free-living dinoflagellates. Analysis of genome data from multiple isolates revealed that Symbiodiniaceae taxa share greater intraspecific divergence, at both sequence and structural levels, than the outgroup P. glacialis. Compared to symbiotic species, genomes of E. voratum and outgroup P. glacialis are rife with tandemly duplicated genes, many of which were single-exonic, suggesting that tandem duplication of genes played a prominent role in adaptation of free-living species. A comprehensive analysis of genome and transcriptome data from 21 Symbiodiniaceae taxa further revealed conservation of key genes associated with meiosis, suggesting that these taxa possessed capacity for sexual reproduction, potentially via a non-canonical machinery analogous to synaptonemal complex common in eukaryotes. These results in combination demonstrate how symbiogenesis has shaped the genome evolution and diversification of Symbiodiniaceae by modulating gene duplication and pseudogenisation, and clear genomic evidence for sexual reproduction in generating genomic diversity of these taxa. The data and knowledge generated from this thesis research provide a foundational reference for future research in dinoflagellates and microbial eukaryotes, and novel insights into how symbiosis has shaped the evolution and ecologically success of diverse organisms.

Keywords

3101 Biochemistry and cell biology, School of Chemistry and Molecular Biosciences, Bioinformatics, 310204 Genomics and transcriptomics, Genomics, Symbionts, Phylogenetics, 310208 Translational and applied bioinformatics, 310799 Microbiology not elsewhere classified, Coral reef ecology, 310199 Biochemistry and cell biology not elsewhere classified, Genetics, 3102 Bioinformatics and computational biology, 3104 Evolutionary biology

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selected citations
These citations are derived from selected sources.
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
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Average
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