A genomic view of the reef-building coral Porites lutea and its microbial symbionts

Ball, Eldon E.; Beeden, Roger; Berumen, Michael L.; Aranda, Manuel; Ravasi, Timothy; Bongaerts, Pim; Hoegh‐Guldberg, Ove; Cooke, Ira; Leggat, Bill; Sprungala, Susan; Fitzgerald, Anna; Shang, Catherine A.; Lundgren, Petra; Fyffe, Theresa; Rubino, Francesco; Oppen, Madeleine J. H. van; Weynberg, Karen D.; Robbins, Steven J.; Singleton, Caitlin M.; Chan, Cheong Xin; Messer, Lauren F.; Geers, Aileen U.; Ying, Hua; Baker, Alexander; Bell, Sara C.; Morrow, Kathleen M.; Ragan, Mark A.; Miller, David J.; Fôret, Sylvain; Voolstra, Christian R.; Tyson, Gene W.; Bourne, David G.

doi:10.1038/s41564-019-0532-4

Cited by 207 publications

(235 citation statements)

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“…These findings suggest that Endozoicomonas can transition between different symbiotic lifestyles. We identified a high number of eukaryotic repeat proteins in E. acroporae genomes ( Supplementary Table S7); our results are similar to a recent study on Porites lutea microbial symbionts, which identified >50 copies of eukaryotic repeat proteins in a metagenome-derived Endozoicomonas genome [80], suggesting a symbiotic relationship. Furthermore, we also identified a high count of secretory (T3SS and T4SS) proteins in the genomes of E. acroporae strains (Supplementary Table S6) that may help transport organic macromolecules and effector proteins between the host and symbiont.…”

Section: Genome Architecture Of Endozoicomonas Species and Putative Rsupporting

confidence: 89%

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP)

et al. 2020

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Dominant coral-associated Endozoicomonas bacteria species are hypothesized to play a role in the coral sulfur cycle by metabolizing dimethylsulfoniopropionate (DMSP) into dimethylsulfide (DMS); however, no sequenced genome to date harbors genes for this process. In this study, we assembled high-quality (>95% complete) draft genomes of strains of the recently added species Endozoicomonas acroporae (Acr-14 T , Acr-1, and Acr-5) isolated from the coral Acropora sp. and performed a comparative genomic analysis on the genus Endozoicomonas. We identified DMSP CoA-transferase/lyase-a dddD gene homolog in all sequenced genomes of E. acroporae strains-and functionally characterized bacteria capable of metabolizing DMSP into DMS via the DddD cleavage pathway using RT-qPCR and gas chromatography (GC). Furthermore, we demonstrated that E. acroporae strains can use DMSP as a carbon source and have genes arranged in an operon-like manner to link DMSP metabolism to the central carbon cycle. This study confirms the role of Endozoicomonas in the coral sulfur cycle.

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Section: Genome Architecture Of Endozoicomonas Species and Putative Rsupporting

confidence: 89%

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP)

et al. 2020

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“…One hypothesis to account for this is that nitrate enters the coral cytoplasm under a non-specific mechanism or as a mimic of a “normal” metabolite. Another scenario is that nitrate and/or nitrite may be produced by prokaryotes or other single celled microbes that are intimately associated with the hosts; metagenomic analysis of the Porites lutea association gives this idea some credibility (Robbins et al, in press). It is likely that symbiont / host exchanges involving organic nitrogen compounds such as amino acids also occur (Shinzato et al, 2014; Ying et al, 2018), and the upregulation of several solute carrier proteins in symbiotic Cladocopium reported here provides the first direct evidence supporting this.…”

Section: Discussionmentioning

confidence: 99%

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

Mohamed

Andrade

Moya

et al. 2019

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Despite the ecological significance of the mutualistic relationship between Symbiodiniaceae and reef-building corals, the molecular machinery underpinning the establishment of this relationship is not well understood. This is especially true of the symbiont side, as previous attempts to understand the interaction between coral larvae and Symbiodiniaceae have focused nearly exclusively on the host. In the current study, Acropora tenuis planula larvae were exposed to a compatible strain of Symbiodiniaceae (Cladocopium) and the transcriptomic landscape of the symbiont profiled at 3, 12, 48 and 72 h post-exposure using RNA-Seq. The transcriptomic response of Cladocopium to the symbiotic state was complex, the most obvious feature being an extensive and generalised downregulation of gene expression. Included in this “symbiosis-derived transcriptional repression” were a range of stress response and immune-related genes. In contrast, genes implicated in metabolism were upregulated in the symbiotic state. Consistent with previous ecological studies, this transcriptomic response of Cladocopium implied that active translocation of metabolites to the host occurred, and thus that the mutualistic relationship can be established at the larval stage. This study provides novel insights into the transcriptomic remodelling that occurs in Symbiodiniaceae, with important implications for understanding the establishment of symbiosis between corals and their dinoflagellate partners.

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“…Coral reefs are especially vulnerable because their structural integrity depends on the symbiosis between corals and photosymbionts (family Symbiodiniaceae 4 ), but this relationship breaks down under stress leading to bleaching and widespread mortality during marine heatwaves 5,6 . The projected severity of these impacts therefore depends on whether coral holobionts (coral, photosymbionts and associated bacteria 7,8 ) can adapt fast enough to maintain the integrity of reef ecosystems 9,10 . A key factor that might improve the adaptive outlook for corals is the existence of stress-tolerant populations which could fuel adaptation in conspecifics through assisted or natural gene flow [11][12][13][14] .…”

Section: Introductionmentioning

confidence: 99%

Signatures of selection in the coral holobiont reveal complex adaptations to inshore environments driven by Holocene climate change

Cooke

Ying

Fôret

et al. 2020

Preprint

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The inshore region of the Great Barrier Reef (GBR) became inundated at the start of the Holocene when sea levels rose. Like many inshore reefs worldwide it harbours extensive coral assemblages despite being subject to relatively high turbidity, freshwater input and thermal fluctuations. To investigate how the coral holobiont has adapted to these conditions we used shallow whole genome resequencing of 148 Acropora tenuis colonies from five inshore locations to model demographic history, identify signatures of selection and profile symbiont communities. We also assembled the genome of Acropora tenuis from long-read sequencing, providing one of the most contiguous and complete coral genomes to date. We show that corals from Magnetic Island are genetically distinct from reefs further north reflecting a Pleistocene (250-600Kya) split, whereas photosymbiont genotypes differed between reefs in a pattern more likely to reflect contemporary (Holocene) conditions. We also identified loci in the coral host genome with signatures of positive selection in the northern population and demonstrate using coalescent simulations that these are unlikely to be accounted for by demographic history. Associated with these we find genes with roles in a complex range of processes including heterotrophy, osmotic regulation, skeletal development and establishment and maintenance of symbiosis. Our results show that A. tenuis holobionts from the inshore GBR have been significantly shaped by their environment and provide an example of complex adaptations in response to past climate change.

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A genomic view of the reef-building coral Porites lutea and its microbial symbionts

Cited by 207 publications

References 100 publications

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP)

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP)

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

Signatures of selection in the coral holobiont reveal complex adaptations to inshore environments driven by Holocene climate change

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