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A first genomic portrait of the deep-water azooxanthellate reef-building coral Madracis myriaster: genome size, repetitive elements, nuclear RNA gene operon, mitochondrial genome, and phylogenetic placement in the family Pocilloporidae

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Abstract

The coral Madracis myriaster is one of the most important reef builders in deep-water habitats of the Caribbean Sea, offering refuge to numerous species of fish and invertebrates. In this study, we developed genomic resources for M. myriaster. Using a low-coverage short read sequencing strategy, this study estimated the genome size, repetitive genome content, annotated and quantified repetitive elements, assembled the 45S rRNA DNA operon, and characterized in detail the mitochondrial genome of M. myriaster. The haploid genome size estimated using a k-mer strategy was 615–697 Mbp, which is within the range reported for scleractinian corals. Repetitive genome content estimates using different word sizes (= k-mers) indicated that 53–65% of the genome of M. myriaster comprised repetitive elements. A relatively large number of the discovered repetitive elements could not be annotated. Taking into account only annotated repetitive elements, the most common were classified as Satellite DNA which were more abundant than Class I-LINE, Class I—Penelope, and Class II (DNA transposons)—Subclass 2 Maverick mobile elements. Less abundant repeat element families included Class I-LTR Ty3 retrotransposons, Class II-Subclass 2-Helitron mobile elements, Class I-LTR-Bel-Pao, and Class I-DIRS mobile elements. The nuclear ribosomal operon of M. myriaster was assembled into a single contig that contains, in the following order: a 5′ ETS [length = 1200 bp (partially assembled)], ssrDNA (1800 bp), ITS1 (233 bp), 5.8S rDNA (158 bp), ITS2 (204 bp), lsrDNA (3616 bp), and 3′ ETS [827 bp (partial sequence)]. The mitochondrial genome of M. myriaster is 17,044 bp long and encodes 13 protein-coding genes, 2 transfer RNAs, and two ribosomal genes. Based on protein-coding genes, the phylogenetic position of M. myriaster was examined. These new genomic resources are of utmost relevance to improve the understanding of the biology of M. myriaster and for the development of conservation plans in this reef-forming deep-water coral.

Resumen

El coral Madracis myriaster es uno de los formadores de arrecifes más importantes en hábitats de aguas profundas del Mar Caribe, ofreciendo refugio a numerosas especies de peces e invertebrados. En este estudio, desarrollamos recursos genómicos para M. myriaster. Utilizando una estrategia de secuenciación de lectura corta de baja cobertura, nuestro estudio estimo el tamaño del genoma, su contenido repetitivo, anotó y cuantificó elementos repetitivos, ensambló el operón de ADN-ARNr 45S y caracterizó en detalle el genoma mitocondrial de M. myriaster. El tamaño del genoma haploide estimado utilizando una estrategia ‘k-mer’ fue de 615 a 697 Mbp, que está dentro del rango registrado para corales escleractinios. Las estimaciones del contenido genómico repetitivo utilizando diferentes tamaños de palabras (= k-mers) indicaron que entre el 53% y el 65% del genoma de M. myriaster comprendía elementos repetitivos. Un número relativamente grande de estos elementos repetitivos descubiertos no se anotaron. Teniendo en cuenta sólo los elementos repetivos anotados, los más comunes se clasificaron como ADN satelital, que fueron más abundantes que los elementos móviles Clase I-LINE, Clase I—Penélope y Clase II (transposones de ADN)—Subclase 2 Maverick. Las familias de elementos repetidos menos abundantes incluyeron retro-transposones Clase I-LTR Ty3, elementos móviles Clase IISubclase 2- Helitron, así como elementos móviles Clase I-LTR-Bel-Pao y Clase I-DIRS. El operón ribosómico nuclear de M. myriaster se ensambló en un único contig que contiene, en el siguiente orden: un 5 ETS [longitud = 1.200 pb (parcialmente ensamblado)], ssrDNA (1.800 pb), ITS1 (233 pb), 5,8 S rDNA (158 pb), ITS2 (204 pb), lsrDNA (3.616 pb) y 3' ETS [827 pb (secuencia parcial)]. El genoma mitocondrial de M. myriaster tiene 17.044 pb de largo y codifica 13 genes codificadores de proteínas, 2 ARN de transferencia y dos genes ribosomales. Basándose en los genes que codifican proteínas, se examinó la posición filogenética de M. myriaster. Estos nuevos recursos genómicos son de suma relevancia para mejorar la comprensión de la biología de M. myriaster y para el desarrollo de planes de conservación de este coral formador de arrecifes de aguas profundas.

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Data availability

The whole-genome sequencing data are available in the NCBI Sequence Read Archive (SRA) repository (Bioproject: PRJNA611988; BioSample: SAMN14355079; SRA accession number: SRX7895127). The mitochondrial genome and ribosomal operon assemblies are available in NCBI’s GenBank with accession numbers OQ331104 and OP673530, respectively.

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Acknowledgements

J.A.B thanks Vincent P. Richards for bioinformatics support. The Galaxy server that was used for some calculations is in part funded by Collaborative Research Centre 992 Medical Epigenetics (DFG grant SFB 992/1 2012) and German Federal Ministry of Education and Research (BMBF grants 031 A538A/A538C RBC, 031L0101B/031L0101C de.NBI-epi, 031L0106 de.STAIR (de.NBI)). The authors thank Diana C. Ballesteros for permission to use her photographs.

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JT and JAB analyzed the data. JT, LMB, and JAB drafted the manuscript. JAB provided supervision. All authors contributed to the article and approved the submitted version.

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Correspondence to J. Antonio Baeza.

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The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Tucker, J., Barrios, L.M., Preziosi, R. et al. A first genomic portrait of the deep-water azooxanthellate reef-building coral Madracis myriaster: genome size, repetitive elements, nuclear RNA gene operon, mitochondrial genome, and phylogenetic placement in the family Pocilloporidae. Coral Reefs 42, 1241–1256 (2023). https://doi.org/10.1007/s00338-023-02419-y

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