ORCID Profile
0000-0001-9052-2379
Current Organisation
University of Queensland
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Publisher: Oxford University Press (OUP)
Date: 11-2016
DOI: 10.1093/GBE/EVW255
Publisher: Cold Spring Harbor Laboratory
Date: 11-04-2022
DOI: 10.1101/2022.04.10.487810
Abstract: Coral reefs are fundamentally sustained by symbioses involving dinoflagellate algae in the Family Symbiodiniaceae. The coral symbiont Durusdinium trenchii is notable for enhancing the resilience of coral holobionts under thermal stress. Believed to have experienced whole-genome duplication (WGD), D. trenchii offers a valuable model system to understand how selection acts on the genome of a facultative symbiont after WGD. We present genome assemblies for two isolates of D. trenchii and confirm WGD in these taxa, providing the first ex le of this phenomenon in a single-celled eukaryotic symbiont. We assess how the facultative lifestyle has contributed to the retention and ergence of duplicated genes, and how these results intersect with the observed thermotolerance of corals hosting D. trenchii symbionts. Our findings reveal that the free-living lifestyle is the main driver of post-WGD evolution, however, they also implicate symbiosis in this process, with both lifestyles increasing algal fitness. Our results demonstrate that WGD, driven by selection in the free-living phase, has converted D. trenchii into a coral symbiont that serendipitously provides increased thermal stress protection to the host coral.
Publisher: Elsevier BV
Date: 09-2022
DOI: 10.1016/J.TIM.2022.02.001
Abstract: Modern microbial taxonomy generally relies on the use of single marker genes or sets of concatenated genes to generate a framework for the delineation and classification of organisms at different taxonomic levels. However, given that DNA is the 'blueprint of life', and hence the ultimate arbiter of taxonomy, classification systems should attempt to use as much of the blueprint as possible to capture a comprehensive phylogenetic signal. Recent analysis of whole-genome sequences from coral reef symbionts (dinoflagellates of the family Symbiodiniaceae) and other microalgal groups has uncovered extensive ergence not recognised by current algal taxonomic approaches. In the era of 'sequence everything', we argue that whole-genome data are pivotal to guide informed taxonomic inference, particularly for microbial eukaryotes.
Publisher: MDPI AG
Date: 17-08-2022
DOI: 10.3390/MICROORGANISMS10081662
Abstract: Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically erse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35–36% have putatively originated via horizontal gene transfer (HGT), predominantly (19–23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10–11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.
Publisher: Springer Science and Business Media LLC
Date: 13-04-2021
DOI: 10.1186/S12915-021-00994-6
Abstract: 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. Here, we present de novo genome assemblies of seven members of the genus Symbiodinium , of which two are free-living, 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 ergence. 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. Our results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome ergence, and the ersification of Symbiodinium and Symbiodiniaceae. The ergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history.
Publisher: Cold Spring Harbor Laboratory
Date: 25-03-2023
DOI: 10.1101/2023.03.24.534093
Abstract: Dinoflagellates in the Family Symbiodiniaceae (Order Suessiales) are erse, predominantly symbiotic lineages that associate with taxa such as corals and jellyfish. Their ancestor is believed to have been free-living, and the establishment of symbiosis (i.e., symbiogenesis) is hypothesised to have occurred multiple times during Symbiodiniaceae evolution. Among Symbiodiniaceae taxa, the genus Effrenium is an early erging, free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here we present de novo assembled genomes and associated transcriptome data from three isolates of Effrenium voratum . We compared the Effrenium genomes (1.2-1.9 Gbp in size) and gene features with those of 16 Symbiodiniaceae taxa and other outgroup dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. We postulate that adaptation to an extreme habitat (e.g., as in Polarella glacialis ) or life in oligotrophic conditions resulted in the Suessiales ancestor having a haploid genome size 2Gbp, which was retained (or reduced) among all extant algae in this lineage. Nonetheless, our data reveal that the free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (∼30%) lineage-specific gene families, and lower (∼10%) level of pseudogenisation. These results demonstrate how genome reduction and the adaptation to symbiotic versus free-living lifestyles intersect, and have driven the ersification and genome evolution of Symbiodiniaceae.
Publisher: Frontiers Media SA
Date: 26-04-2022
Abstract: Dinoflagellates of the family Symbiodiniaceae are predominantly essential symbionts of corals and other marine organisms. Recent research reveals extensive genome sequence ergence among Symbiodiniaceae taxa and high phylogenetic ersity 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, 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 (& % 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.
Publisher: Cold Spring Harbor Laboratory
Date: 20-07-2022
DOI: 10.1101/2022.07.19.500725
Abstract: Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these algae, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with earlier generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui , and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 broadly s led eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5,246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35-36% have putatively originated via horizontal gene transfer (HGT), predominantly (19-23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10-11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.
Publisher: Elsevier BV
Date: 09-2021
Publisher: Cold Spring Harbor Laboratory
Date: 10-10-2019
DOI: 10.1101/800482
Abstract: Dinoflagellates of the family Symbiodiniaceae (Order Suessiales) are predominantly symbiotic, and many are known for their association with corals. The genetic and functional ersity among Symbiodiniaceae is well acknowledged, but the genome-wide sequence ergence among these lineages remains little known. Here, we present de novo genome assemblies of five isolates from the basal genus Symbiodinium , encompassing distinct ecological niches. Incorporating existing data from Symbiodiniaceae and other Suessiales (15 genome datasets in total), we investigated genome features that are common or unique to these Symbiodiniaceae, to genus Symbiodinium , and to the in idual species S. microadriaticum and S. tridacnidorum . Our whole-genome comparisons reveal extensive sequence ergence, with no sequence regions common to all 15. Based on similarity of k -mers from whole-genome sequences, the distances among Symbiodinium isolates are similar to those between isolates of distinct genera. We observed extensive structural rearrangements among symbiodiniacean genomes those from two distinct Symbiodinium species share the most (853) syntenic gene blocks. Functions enriched in genes core to Symbiodiniaceae are also enriched in those core to Symbiodinium. Gene functions related to symbiosis and stress response exhibit similar relative abundance in all analysed genomes. Our results suggest that structural rearrangements contribute to genome sequence ergence in Symbiodiniaceae even within a same species, but the gene functions have remained largely conserved in Suessiales. This is the first comprehensive comparison of Symbiodiniaceae based on whole-genome sequence data, including comparisons at the intra-genus and intra-species levels.
Publisher: Springer Science and Business Media LLC
Date: 17-06-2020
DOI: 10.1038/S41598-020-66429-4
Abstract: Dinoflagellates of the Symbiodiniaceae family encompass erse symbionts that are critical to corals and other species living in coral reefs. It is well known that sexual reproduction enhances adaptive evolution in changing environments. Although genes related to meiotic functions were reported in Symbiodiniaceae, cytological evidence of meiosis and fertilisation are however yet to be observed in these taxa. Using transcriptome and genome data from 21 Symbiodiniaceae isolates, we studied genes that encode proteins associated with distinct stages of meiosis and syngamy. We report the absence of genes that encode main components of the synaptonemal complex (SC), a protein structure that mediates homologous chromosomal pairing and class I crossovers. This result suggests an independent loss of canonical SCs in the alveolates, that also includes the SC-lacking ciliates. We hypothesise that this loss was due in part to permanently condensed chromosomes and repeat-rich sequences in Symbiodiniaceae (and other dinoflagellates) which favoured the SC-independent class II crossover pathway. Our results reveal novel insights into evolution of the meiotic molecular machinery in the ecologically important Symbiodiniaceae and in other eukaryotes.
Publisher: Frontiers Media SA
Date: 29-06-2022
Abstract: Herbicides are commonly deployed as the front-line treatment to control infestations of weeds in native ecosystems and among crop plants in agriculture. However, the prevalence of herbicide resistance in many species is a major global challenge. The specificity and effectiveness of herbicides acting on erse weed species are tightly linked to targeted proteins. The conservation and variance at these sites among different weed species remain largely unexplored. Using novel genome data in a genome-guided approach, 12 common herbicide-target genes and their coded proteins were identified from seven species of Weeds of National Significance in Australia: Alternanthera philoxeroides (alligator weed), Lycium ferocissimum (African boxthorn), Senecio madagascariensis (fireweed), Lantana camara (lantana), Parthenium hysterophorus (parthenium), Cryptostegia grandiflora (rubber vine), and Eichhornia crassipes (water hyacinth). Gene and protein sequences targeted by the acetolactate synthase (ALS) inhibitors and glyphosate were recovered. Compared to structurally resolved homologous proteins as reference, high sequence conservation was observed at the herbicide-target sites in the ALS (target for ALS inhibitors), and in 5-enolpyruvylshikimate-3-phosphate (EPSP) synthase (target for glyphosate). Although the sequences are largely conserved in the seven phylogenetically erse species, mutations observed in the ALS proteins of fireweed and parthenium suggest resistance of these weeds to ALS-inhibiting and other herbicides. These protein sites remain as attractive targets for the development of novel inhibitors and herbicides. This notion is reinforced by the results from the phylogenetic analysis of the 12 proteins, which reveal a largely consistent vertical inheritance in their evolutionary histories. These results demonstrate the utility of high-throughput genome sequencing to rapidly identify and characterize gene targets by computational methods, bypassing the experimental characterization of in idual genes. Data generated from this study provide a useful reference for future investigations in herbicide discovery and development.
Publisher: Cold Spring Harbor Laboratory
Date: 29-03-2023
DOI: 10.1101/2023.03.28.534646
Abstract: Dinoflagellates of Order Suessiales include the erse Family Symbiodiniaceae known for their role as essential coral reef symbionts, and the cold-adapted Polarella glacialis . These taxa inhabit a broad range of ecological niches and exhibit extensive genomic ergence, although their genomes are in the smaller size ranges (haploid size 3 Gbp) compared to most other dinoflagellates. Different isolates of a species are known to form symbiosis with distinct hosts and exhibit different regimes of gene expression, but intraspecies whole-genome ergence remains little known. Focusing on three Symbiodiniaceae species (the free-living Effrenium voratum , and the symbiotic Symbiodinium microadriaticum and Durusdinium trenchii ) and the free-living outgroup P. glacialis , all for which whole-genome data from multiple isolates are available, we assessed intraspecies genomic ergence at sequence and structural levels. Our analysis based on alignment and alignment-free methods revealed greater extent of intraspecies sequence ergence in symbiodiniacean species than in P. glacialis . Our results also reveal the implications of gene duplication in generating functional innovation and ersification of Symbiodiniaceae, particularly in D. trenchii for which whole-genome duplication was involved. Interestingly, tandem duplication of single-exon genes was found to be more prevalent in genomes of free-living species than in those of symbiotic species. These results in combination demonstrate the remarkable intraspecies genomic ergence in dinoflagellates under the constraint of reduced genome sizes, shaped by genetic duplications and symbiogenesis events during ersification of Symbiodiniaceae.
Publisher: The Royal Society
Date: 09-2023
DOI: 10.1098/RSOB.230182
No related grants have been discovered for Sarah Shah.