Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

Liu, Huanle; Stephens, Timothy G.; González‐Pech, Raúl A.; Beltran, Victor H.; Lapeyre, Bruno; Bongaerts, Pim; Cooke, Ira; Aranda, Manuel; Bourne, David G.; Fôret, Sylvain; Miller, David J.; Oppen, Madeleine J. H. van; Voolstra, Christian R.; Ragan, Mark A.; Chan, Cheong Xin

doi:10.1038/s42003-018-0098-3

Cited by 170 publications

(222 citation statements)

References 92 publications

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“…While Symbiodiniaceae meiosis has not been demonstrated in an experimental setting, others have identified evidence of recombination in population genetics studies (Baillie, Belda-Baillie, & Maruyama, 2000;LaJeunesse, 2001). Further, Symbiodinaceae genomes possess a virtually complete gene set for meiosis (Liu et al, 2018), suggesting that they have the potential for sexual reproduction.…”

Section: In Hospite Reduction In Sexual Reproductionmentioning

confidence: 99%

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

et al. 2019

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Reef‐building corals depend upon a nutritional endosymbiosis with photosynthetic dinoflagellates of the family Symbiodiniaceae for the majority of their energetic needs. While this mutualistic relationship is impacted by numerous stressors, warming oceans are a predominant threat to coral reefs, placing the future of the world's reefs in peril. Some Symbiodiniaceae species exhibit tolerance to thermal stress, but the in hospite symbiont response to thermal stress is underexplored. To describe the underpinnings of symbiosis and heat stress response, we compared in hospite and free‐living transcriptomes of Durusdinium trenchii, a pan‐tropical heat‐tolerant Symbiodiniaceae species, under stable temperature conditions and acute hyperthermal stress. We discovered that symbiotic state was a larger driver of the transcriptional landscape than heat stress. The majority of differentially expressed transcripts between in hospite and free‐living cells were downregulated, suggesting the in hospite condition is associated with the shutdown of numerous processes uniquely required for a free‐living lifestyle. In the free‐living state, we identified enrichment for numerous cell signalling pathways and other functions related to detecting and responding to a changing environment, as well as transcripts relating to mitosis, meiosis, and motility. In contrast, in hospite cells exhibited enhanced transcriptional activity for photosynthesis and carbohydrate transport as well as chromatin modifications and a disrupted circadian clock. Hyperthermal stress induced drastic alteration of transcriptional activity in hospite, suggesting symbiotic engagement with the host elicited an exacerbated stress response when compared to free‐living D. trenchii. Altogether, the dramatic differences in gene expression between in hospite and free‐living D. trenchii indicate the importance of considering symbiotic state in investigations of symbiosis and hyperthermal stress in Symbiodiniaceae.

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Section: In Hospite Reduction In Sexual Reproductionmentioning

confidence: 99%

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

et al. 2019

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“…Recent comparative analyses of genome, transcriptome, and protein sets showed that the family Symbiodiniaceae is enriched with domains involved in transmembrane transport when compared to other eukaryotes (Aranda et al, ) or even other dinoflagellates (Liu et al, ). Domains of bicarbonate transporters, carbonic anhydrase, and ammonium transporters are particularly enriched when compared to other dinoflagellates (Aranda et al, ), which suggests that expansion of transporters has occurred in Symbiodiniaceae as an adaptation to symbiotic lifestyle (Aranda et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…Domains of bicarbonate transporters, carbonic anhydrase, and ammonium transporters are particularly enriched when compared to other dinoflagellates (Aranda et al, ), which suggests that expansion of transporters has occurred in Symbiodiniaceae as an adaptation to symbiotic lifestyle (Aranda et al, ). Previous bioinformatic/phylogenetic studies have identified numerous transporter genes in Symbiodiniaceae (Aranda et al, ; González‐Pech, Ragan, & Chan, ; Liu et al, ; Sproles et al, ), but their roles in symbiosis are yet to be determined. Although the mutualistic symbiosis between corals and Symbiodiniaceae has been investigated since the late 1800s, the literature still has huge gaps in understanding how metabolic trafficking is taking place and which membrane transporters assist in the process.…”

Section: Introductionmentioning

confidence: 99%

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Maor-Landaw

Oppen

McFadden

2019

Ecology and Evolution

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Coral-dinoflagellate symbiosis underpins the evolutionary success of corals reefs. Successful exchange of molecules between the cnidarian host and the Symbiodiniaceae algae enables the mutualistic partnership. The algae translocate photosynthate to their host in exchange for nutrients and shelter. The photosynthate must traverse multiple membranes, most likely facilitated by transporters. Here, we compared gene expression profiles of cultured, free-living Breviolum minutum with those of the homologous symbionts freshly isolated from the sea anemone Exaiptasia diaphana, a widely used model for coral hosts. Additionally, we assessed expression levels of a list of candidate host transporters of interest in anemones with and without symbionts. Our transcriptome analyses highlight the distinctive nature of the two algal life stages, with many gene expression level changes correlating to the different morphologies, cell cycles, and metabolisms adopted in hospite versus free-living.Morphogenesis-related genes that likely underpin the metamorphosis process observed when symbionts enter a host cell were up-regulated. Conversely, many downregulated genes appear to be indicative of the protective and confined nature of the symbiosome. Our results emphasize the significance of transmembrane transport to the symbiosis, and in particular of ammonium and sugar transport. Further, we pinpoint and characterize candidate transporters-predicted to be localized variously to the algal plasma membrane, the host plasma membrane, and the symbiosome membrane-that likely serve pivotal roles in the interchange of material during symbiosis.Our study provides new insights that expand our understanding of the molecular exchanges that underpin the cnidarian-algal symbiotic relationship. K E Y W O R D S Breviolum minutum, Exaiptasia diaphana, free-living, in hospite, symbiosis, transporters S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Maor-Landaw K, van Oppen MJH, McFadden GI. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae).

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“…health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e.…”

mentioning

confidence: 99%

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Stephens

González‐Pech

Cheng

et al. 2019

Preprint

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Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp).Of all genes, ~40% are encoded unidirectionally, ~25% comprised of single exons. Multigenome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since 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 environments. health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e. 0.12-4.8 Gbp. In comparison, genomes of other free-living dinoflagellates are much larger in size, ranging from ~7 Gbp in the psychrophile Polarella glacialis, to over 200 Gbp in Prorocentrum sp. based on DAPI-staining of DNA content 18 .Repeat content has been estimated at >55% in the genome sequences of some free-living dinoflagellates 19,20 ; single-exon genes have also been described 21 . Given that most dinoflagellate lineages are free-living, whole genome sequences of these taxa are critical to understand the molecular mechanisms that underpin their successful diversification in specialised environmental niches.Polarella glacialis, a psychrophilic (cold-adapted) free-living species, represents an excellent system for genomic studies of dinoflagellates for three reasons. First, it is closely related to Symbiodiniaceae (both in Order Suessiales), the family that contains the coral reef symbionts, e.g. Symbiodinium and related genera. Second, P. glacialis has been reported only in polar regions. Studying the P. glacialis genome can thus provide a first glimpse into molecular mechanisms that underlie both the evolutionary transition of dinoflagellates from a free-living to a symbiotic lifestyle, and the adaptation to extreme environments. Third, the estimated genome size of P. glacialis is still in the smaller range (~7 Gbp 18 ) of all dinoflagellate taxa, which presents a technical advantage in terms of allowing efficient genome assembly and gene prediction.

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Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

Cited by 170 publications

References 92 publications

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

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