Comparative genomics explains the evolutionary success of reef-forming corals

Bhattacharya, Debashish; Agrawal, Shobhit; Aranda, Manuel; Baumgarten, Sebastian; Belcaid, Mahdi; Drake, Jeana L.; Erwin, Douglas H.; Foret, Sylvian; Gates, Ruth D.; Gruber, David F.; Kamel, Bishoy; Lesser, Michael P.; Levy, Oren; Liew, Yi Jin; MacManes, Matthew D.; Mass, Tali; Medina, Mónica; Mehr, Shaadi; Meyer, Eli; Price, Dana C.; Putnam, Hollie M.; Qiu, Huan; Shinzato, Chuya; Shoguchi, Eiichi; Stokes, Alexander J.; Tambutté, Sylvie; Tchernov, Dan; Voolstra, Christian R.; Wagner, Nicole; Walker, Charles W.; Weber, Andreas P.M.; Weis, Virginia M.; Zelzion, Ehud; Zoccola, Didier; Falkowski, Paul G.

doi:10.7554/elife.13288

Cited by 177 publications

(174 citation statements)

References 110 publications

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“…We compared the amount of ammonium transporter domains between Symbiodinium and the genomes of three symbiotic cnidarians, i.e. the scleractinian corals Stylophora pistillata 4243 and Acropora digitifera 44 as well as the symbiotic anemone Aiptasia 45 (Dataset S1.2). While the cnidarian genomes appear to encode for 18, 7, and 15 ammonium transporter domains respectively, we identified 68, 42, and 46 such domains in the genomes of S. microadriaticum , S. minutum, and S. kawagutii .…”

Section: Resultsmentioning

confidence: 99%

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

Aranda

Liew

et al. 2016

Sci Rep

313

346

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Despite half a century of research, the biology of dinoflagellates remains enigmatic: they defy many functional and genetic traits attributed to typical eukaryotic cells. Genomic approaches to study dinoflagellates are often stymied due to their large, multi-gigabase genomes. Members of the genus Symbiodinium are photosynthetic endosymbionts of stony corals that provide the foundation of coral reef ecosystems. Their smaller genome sizes provide an opportunity to interrogate evolution and functionality of dinoflagellate genomes and endosymbiosis. We sequenced the genome of the ancestral Symbiodinium microadriaticum and compared it to the genomes of the more derived Symbiodinium minutum and Symbiodinium kawagutii and eukaryote model systems as well as transcriptomes from other dinoflagellates. Comparative analyses of genome and transcriptome protein sets show that all dinoflagellates, not only Symbiodinium, possess significantly more transmembrane transporters involved in the exchange of amino acids, lipids, and glycerol than other eukaryotes. Importantly, we find that only Symbiodinium harbor an extensive transporter repertoire associated with the provisioning of carbon and nitrogen. Analyses of these transporters show species-specific expansions, which provides a genomic basis to explain differential compatibilities to an array of hosts and environments, and highlights the putative importance of gene duplications as an evolutionary mechanism in dinoflagellates and Symbiodinium.

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Section: Resultsmentioning

confidence: 99%

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

Aranda

Liew

et al. 2016

Sci Rep

313

346

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“…In particular, horizontal gene transfer between the coral host and the microbial community [19] may reduce binning accuracy, especially in composition-based approaches and underrepresented taxa [27]. A possibility to address this issue is to generate subtraction reference genomic libraries of Symbiodinium symbionts, as recently implemented [25].…”

Section: Discussionmentioning

confidence: 99%

“…Completeness was estimated by calculating the content of metazoan BUSCOs (e-value: 0.001, dataset v.3.0.2) [72] in the genome and the gene datasets and by determining the presence of orthologs previously described within a comparative genomic framework of reef cnidarians at various taxonomic levels (Reef Genomics database [19]) using BLASTx (e-value: 0.001, blast v.2.2.30 [73]). Finally, the usefulness was estimated by the percentage of genome size in scaffolds higher or equal to the average gene size of invertebrate model organisms, following Bradnam et al [36] and using the latest protein-coding annotations of the Ensembl 89 Genes dataset [74] for Caenorhabditis elegans (WBcel235), Ciona intestinalis (KH), Ciona savignyi (CSAV 2.0), Drosophila melanogaster (BDGP6), and Saccharomyces cerevisiae (R64–1-1).…”

Section: Methodsmentioning

confidence: 99%

“…Reasons include the high taxonomic diversity of the hologenome [12], the firm integration of most endosymbionts into host tissues [8, 11, 15], the often high density of in hospite symbiont cells [8], and the large size of some symbiont genomes, such as those of zooxanthellae, which may be considerably larger than the coral host genome [16–18]. As a consequence, whole genome-based studies of scleractinian corals (and other holobionts) are still scarce [16, 19]. The low number of reference genomes, in turn, further hampers the assembly of novel genomes and the development of other approaches that rely on the information they contain.…”

Section: Introductionmentioning

confidence: 99%

“…Whereas these studies have pioneered whole-genome sequencing in cnidarians, the respective approaches might not be applicable to the vast majority of stony coral species for ecological (e.g., most species are zooxanthellate [24], making it difficult to obtain aposymbiotic tissues [25]) and/or physiological reasons (e.g., constraints in reproductive cycles, spawning time, and developmental stages). Moreover, given that the hologenome serves as an integrated network of gene functions with horizontal gene transfer reported for cnidarians [19], symbiont-free DNA from host organisms may only explain one side of molecular evolution. Therefore, a better understanding of the function of the coral holobiont requires approaches based on hologenome and holotranscriptome analyses.…”

Section: Introductionmentioning

confidence: 99%

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Binning enables efficient host genome reconstruction in cnidarian holobionts

et al. 2018

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BackgroundMany cnidarians, including stony corals, engage in complex symbiotic associations, comprising the eukaryotic host, photosynthetic algae, and highly diverse microbial communities—together referred to as holobiont. This taxonomic complexity makes sequencing and assembling coral host genomes extremely challenging. Therefore, previous cnidarian genomic projects were based on symbiont-free tissue samples. However, this approach may not be applicable to the majority of cnidarian species for ecological reasons. We therefore evaluated the performance of an alternative method based on sequence binning for reconstructing the genome of the stony coral Porites rus from a hologenomic sample and compared it to traditional approaches.ResultsOur results demonstrate that binning performs well for hologenomic data, producing sufficient reads for assembling the draft genome of P. rus. An assembly evaluation based on operational criteria showed results that were comparable to symbiont-free approaches in terms of completeness and usefulness, despite a high degree of fragmentation in our assembly. In addition, we found that binning provides sufficient data for exploratory k-mer estimation of genomic features, such as genome size and heterozygosity.ConclusionsBinning constitutes a powerful approach for disentangling taxonomically complex coral hologenomes. Considering the recent decline of coral reefs on the one hand and previous limitations to coral genome sequencing on the other hand, binning may facilitate rapid and reliable genome assembly. This study also provides an important milestone in advancing binning from the metagenomic to the hologenomic and from the prokaryotic to the eukaryotic level.

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Specific plasmid patterns and high rates of bacterial co‐occurrence within the coral holobiont

Leite

Salles

Calderón

et al. 2018

Ecology and Evolution

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Despite the importance of coral microbiomes for holobiont persistence, the interactions among these are not well understood. In particular, knowledge of the co‐occurrence and taxonomic importance of specific members of the microbial core, as well as patterns of specific mobile genetic elements (MGEs), is lacking. We used seawater and mucus samples collected from Mussismilia hispida colonies on two reefs located in Bahia, Brazil, to disentangle their associated bacterial communities, intertaxa correlations, and plasmid patterns. Proxies for two broad‐host‐range (BHR) plasmid groups, IncP‐1β and PromA, were screened. Both groups were significantly (up to 252 and 100%, respectively) more abundant in coral mucus than in seawater. Notably, the PromA plasmid group was detected only in coral mucus samples. The core bacteriome of M. hispida mucus was composed primarily of members of the Proteobacteria, followed by those of Firmicutes. Significant host specificity and co‐occurrences among different groups of the dominant phyla (e.g., Bacillaceae and Pseudoalteromonadaceae and the genera Pseudomonas, Bacillus, and Vibrio) were detected. These relationships were observed for both the most abundant phyla and the bacteriome core, in which most of the operational taxonomic units showed intertaxa correlations. The observed evidence of host‐specific bacteriome and co‐occurrence (and potential symbioses or niche space co‐dominance) among the most dominant members indicates a taxonomic selection of members of the stable bacterial community. In parallel, host‐specific plasmid patterns could also be, independently, related to the assembly of members of the coral microbiome.

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Comparative genomics explains the evolutionary success of reef-forming corals

Cited by 177 publications

References 110 publications

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

Binning enables efficient host genome reconstruction in cnidarian holobionts

Specific plasmid patterns and high rates of bacterial co‐occurrence within the coral holobiont

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