Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective

Mohamed, Amin R.; Andrade, N. P. C.; Moya, Aurélie; Chan, Cheong Xin; Negri, Andrew P.; Bourne, David G.; Ball, Eldon E.; Miller, David J.

doi:10.1101/652131

Cited by 9 publications

(10 citation statements)

References 67 publications

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“…Of these 20 families, one (OG0000004) putatively encodes protein kinases and glycosyltransferases that are necessary for the biosynthesis of glycoproteins, and another (OG0000013) encodes ankyrin and transport proteins (Supplementary Table 7). These functions are important for the recognition of and interaction with the host among symbiodiniacean symbionts 37–39 . In comparison, five gene families were significantly larger in S. natans than in S. tridacnidorum , of which one (OG0000003) encodes for a sodium-transporter and another (OG0000034) for a transmembrane protein.…”

Section: Resultsmentioning

confidence: 99%

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

González‐Pech¹,

Stephens²,

Chen³

et al. 2019

Preprint

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16Symbiodiniaceae are predominantly symbiotic dinoflagellates critical to corals and other reef 17 organisms. Symbiodinium is a basal symbiodiniacean lineage and includes symbiotic and free-living 18 taxa. However, the molecular mechanisms underpinning these distinct lifestyles remain little 19 known. Here, we present high-quality de novo genome assemblies for the symbiotic Symbiodinium 20 tridacnidorum CCMP2592 (genome size 1.3 Gbp) and the free-living Symbiodinium natans 21 CCMP2548 (genome size 0.74 Gbp). These genomes display extensive sequence divergence, 22sharing only ~1.5% conserved regions (≥90% identity). We predicted 45,474 and 35,270 genes for 23 S. tridacnidorum and S. natans, respectively; of the 58,541 homologous gene families, 28.5% are 24 common to both genomes. We recovered a greater extent of gene duplication and higher abundance 25 of repeats, transposable elements and pseudogenes in the genome of S. tridacnidorum than in that of 26 S. natans. These findings demonstrate that genome structural rearrangements are pertinent to 27 distinct lifestyles in Symbiodinium, and may contribute to the vast genetic diversity within the 28 genus, and more broadly in Symbiodiniaceae. Moreover, the results from our whole-genome 29 comparisons against a free-living outgroup support the notion that the symbiotic lifestyle is a 30 derived trait in, and that the free-living lifestyle is ancestral to, Symbiodinium. 31 with the potential to shift between a free-living motile stage (i.e. mastigote form) and a spherical 56 symbiotic stage (i.e. coccoid form). The genomes of facultative and recent intracellular symbionts 57 and parasites are usually very unstable, with extensive structural rearrangements, intensified activity 58 of transposable elements (TEs) and exacerbated gene duplication that leads to the accumulation of 59 pseudogenes 19,20 . Symbiotic Symbiodiniaceae are thus expected to display similar genomic features. 60In this study, we present draft de novo genome assemblies of S. tridacnidorum CCMP2592 and S. 61 natans CCMP2548. Using a comparative genomic approach, we found extensive genome-sequence 62 divergence and few shared families of predicted genes between the two species. A greater extent of 63 gene duplication, and the higher abundance of TEs and pseudogenes in S. tridacnidorum relative to 64 S. natans suggest that duplication and transposition underpin genome divergence between these 65 species. 66 5

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Section: Resultsmentioning

confidence: 99%

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

González‐Pech¹,

Stephens²,

Chen³

et al. 2019

Preprint

Self Cite

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“…the free-living stage in other Symbiodiniaceae species. Transcriptional changes were described in the algal symbiont Cladocopium goreaui after infecting planula larvae of the coral Acropora tenuis (Mohamed et al, 2019). The transcriptomic response of C. goreaui to the symbiotic state was complex, and the most obvious feature was extensive suppression of gene expression that included down-regulation of genes related to protein synthesis, N-glycan biosynthesis, and a range of stress response and immune-related genes.…”

Section: Previous Omics Studies That Compared In Hospite and Culturmentioning

confidence: 99%

“…In contrast, genes implicated in metabolism were up-regulated in the symbiotic state. The transcriptomic response of C. goreaui to symbiosis implied that the mutualistic relationship, including translocation of metabolites, can be established already at the larval stage (Mohamed et al, 2019). Bellantuono et al (2018) compared the transcriptomes of Durusdinium trenchii in hospite versus.…”

Section: Previous Omics Studies That Compared In Hospite and Culturmentioning

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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“…These authors concluded that while minimal translocation was observed, this was in quantities which would negligibly contribute to larval energetic demands (Kopp et al, 2016). Despite demonstrations of increased lipid utilization and decreased survival in darkness (Harii, Yamamoto, & Hoegh-Guldberg, 2010), and changes in symbiont transcriptome upon larval infection (Mohamed et al, 2019), these data do not prove translocation per se and therefore a recent review of the topic concluded that during the larval phase a "mutualistic relationship cannot be unequivocally confirmed" (Mies, Sumida, Rädecker, & Voolstra, 2017). Additionally, there were no isotopic signatures of feeding found in planulae of Red Sea coral Stylophora pistillata ).…”

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confidence: 99%

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata

Bellworthy

Spangenberg

Fine

2019

Ecology and Evolution

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Successful reproductive output and recruitment is crucial to coral persistence and recovery following anthropogenic stress. Feeding is known to alter coral physiology and increase resilience to bleaching.The goal of the study was to address the knowledge gap of the influence of feeding on reproductive output and offspring phenotype.Colonies of Stylophora pistillata from the Northern Gulf of Aqaba (Red Sea) were fed an Artemia diet or unfed for 5 months during gametogenesis, fertilization, and brooding. In addition, time to settlement and mortality of planulae were assessed at water temperatures ranging from winter temperature (22°C) to three degrees above average peak summer temperature (31°C). A range of physiological parameters was measured in parents and offspring.In brooding parents, feeding significantly increased protein concentration and more than tripled the number of released planulae. Planulae from unfed colonies had higher chlorophyll per symbiont concentration and concomitantly higher photosynthetic efficiency compared to planulae from fed parents. In settlement assays, planulae showed a similar thermal resistance as known for this Red Sea adult population. Mortality was greater in planulae from unfed parents at ambient and 3°C above ambient temperature despite higher per offspring investment in terms of total fatty acid content. Fatty acid profiles and relative abundances were generally conserved between different fed and unfed colonies but planulae were enriched in monounsaturated fatty acids relative to adults, that is, 16:1, 18:1, 20:1, 22:1, and 24:1 isomers.Ultimately the availability of zooplankton could influence population physiology and recruitment in corals.

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Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective

Cited by 9 publications

References 67 publications

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

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

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata

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