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Chromosome-Level Genome Assembly of the Bioluminescent Cardinalfish Siphamia tubifer: An Emerging Model for Symbiosis Research.
Gould AL
,
Henderson JB
,
Lam AW
.
Abstract
The bioluminescent symbiosis involving the sea urchin cardinalfish Siphamia tubifer and the luminous bacterium Photobacterium mandapamensis is an emerging vertebrate model for the study of microbial symbiosis. However, little genetic data are available for the host, limiting the scope of research that can be implemented with this association. We present a chromosome-level genome assembly for S. tubifer using a combination of PacBio HiFi sequencing and Hi-C technologies. The final assembly was 1.2 Gb distributed on 23 chromosomes and contained 32,365 protein coding genes with a BUSCO score of 99%. A comparison of the S. tubifer genome to that of another nonluminous species of cardinalfish revealed a high degree of synteny, whereas a comparison to a more distant relative in the sister order Gobiiformes revealed the fusion of two chromosomes in the cardinalfish genomes. The complete mitogenome of S. tubifer was also assembled, and an inversion in the vertebrate WANCY tRNA genes as well as heteroplasmy in the length of the control region were discovered. A phylogenetic analysis based on whole the mitochondrial genome indicated that S. tubifer is divergent from the rest of the cardinalfish family, highlighting the potential role of the bioluminescent symbiosis in the initial divergence of Siphamia. This high-quality reference genome will provide novel opportunities for the bioluminescent S. tubifer-P. mandapamensis association to be used as a model for symbiosis research.
Fig. 1. (a) Hi–C contact heatmap for Siphamia tubifer. Black lines indicate chromosome boundaries. (b) Gene density distribution across the 23 chromosomes of the S. tubifer genome. (c) Circos plots depicting synteny between the genomes of S. tubifer and the orbiculate cardinalfish, Sphaeramia orbicularis (1.3 Gb) and (d) the mudskipper Periophthalmus magnuspinnatus (702 Mb). Each chromosome in the S. tubifer genome is represented by a distinct color, whereas the Sp. orbicularis and P. magnuspinnatus chromosomes are shown in dark and light gray, respectively. Links between the genomes represent single copy orthologs from the BUSCO Actinopterygii gene set.
Fig. 2. (a) Gene map of the complete mitogenome of Siphamia tubifer. All genes are labeled including the tRNA WANCY region as well as the control region and the approximate location of the goose hairpin (gh) within the control region. (b) Histogram depicting heteroplasmy in the length of the control region observed for the HiFi sequence reads spanning the entire region. (c) Maximum likelihood tree depicting the phylogenetic relationships of several cardinalfish species for which there is whole mitochondrial genome data available, including S. tubifer from this study, in relation to another member of the Apogonoidei clade, Kurtus gulliveri, and several species of gobies in the sister clade Gobioidei. Two Syngnathiformes species are included as an outgroup. The relationships are based on whole mitochondrial DNA sequences excluding the control region using the GTR + F+I + G4 model of substitution. Bootstrap support values (500 replicates) are listed at the nodes. The scale bar indicates nucleotide substitutions per site. Associated GenBank accession numbers for each species are listed in table S3, Supplementary Material online.
Altschul,
Basic local alignment search tool.
1990, Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Belcaid,
Symbiotic organs shaped by distinct modes of genome evolution in cephalopods.
2019,
Pubmed
Belton,
Hi-C: a comprehensive technique to capture the conformation of genomes.
2012,
Pubmed
Benson,
Tandem repeats finder: a program to analyze DNA sequences.
1999,
Pubmed
Bernt,
MITOS: improved de novo metazoan mitochondrial genome annotation.
2013,
Pubmed
Brucker,
Speciation by symbiosis.
2012,
Pubmed
Brůna,
BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database.
2021,
Pubmed
Brůna,
GeneMark-EP+: eukaryotic gene prediction with self-training in the space of genes and proteins.
2020,
Pubmed
Chakraborty,
Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage.
2016,
Pubmed
Chan,
tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes.
2021,
Pubmed
Cheng,
Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm.
2021,
Pubmed
Dudchenko,
De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds.
2017,
Pubmed
Dunlap,
Symbiosis initiation in the bacterially luminous sea urchin cardinalfish Siphamia versicolor.
2012,
Pubmed
,
Echinobase
Dunlap,
Functional morphology of the luminescence system of Siphamia versicolor (Perciformes: Apogonidae), a bacterially luminous coral reef fish.
2011,
Pubmed
,
Echinobase
Durand,
Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom.
2016,
Pubmed
Durand,
Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments.
2016,
Pubmed
Faber,
Tandemly repeated sequences in the mitochondrial DNA control region and phylogeography of the Pike-Perches Stizostedion.
1998,
Pubmed
Farrer,
Synima: a Synteny imaging tool for annotated genome assemblies.
2017,
Pubmed
Flynn,
RepeatModeler2 for automated genomic discovery of transposable element families.
2020,
Pubmed
Formenti,
Complete vertebrate mitogenomes reveal widespread repeats and gene duplications.
2021,
Pubmed
Gould,
Life history of the symbiotically luminous cardinalfish Siphamia tubifer (Perciformes: Apogonidae).
2016,
Pubmed
,
Echinobase
Gould,
Genomic analysis of a cardinalfish with larval homing potential reveals genetic admixture in the Okinawa Islands.
2017,
Pubmed
Gould,
Shedding Light on Specificity: Population Genomic Structure of a Symbiosis Between a Coral Reef Fish and Luminous Bacterium.
2019,
Pubmed
Gould,
Museum Genomics Illuminate the High Specificity of a Bioluminescent Symbiosis for a Genus of Reef Fish.
2021,
Pubmed
Guan,
Identifying and removing haplotypic duplication in primary genome assemblies.
2020,
Pubmed
Haas,
DAGchainer: a tool for mining segmental genome duplications and synteny.
2004,
Pubmed
Hoarau,
Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus.
2002,
Pubmed
Inoue,
Evolution of the deep-sea gulper eel mitochondrial genomes: large-scale gene rearrangements originated within the eels.
2003,
Pubmed
Jones,
InterProScan 5: genome-scale protein function classification.
2014,
Pubmed
Jühling,
Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements.
2012,
Pubmed
Kaeding,
Phylogenetic diversity and cosymbiosis in the bioluminescent symbioses of "Photobacterium mandapamensis".
2007,
Pubmed
Katoh,
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.
2002,
Pubmed
Keller,
A novel hybrid gene prediction method employing protein multiple sequence alignments.
2011,
Pubmed
Kozlov,
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference.
2019,
Pubmed
Kriventseva,
OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs.
2019,
Pubmed
Krzywinski,
Circos: an information aesthetic for comparative genomics.
2009,
Pubmed
Levy Karin,
MetaEuk-sensitive, high-throughput gene discovery, and annotation for large-scale eukaryotic metagenomics.
2020,
Pubmed
Li,
Minimap2: pairwise alignment for nucleotide sequences.
2018,
Pubmed
Li,
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph.
2015,
Pubmed
Lieberman-Aiden,
Comprehensive mapping of long-range interactions reveals folding principles of the human genome.
2009,
Pubmed
Ludwig,
Heteroplasmy in the mtDNA control region of sturgeon (Acipenser, Huso and Scaphirhynchus).
2000,
Pubmed
Nguyen,
IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.
2015,
Pubmed
Poulsen,
Mitogenomic sequences and evidence from unique gene rearrangements corroborate evolutionary relationships of myctophiformes (Neoteleostei).
2013,
Pubmed
Quinn,
Sequence evolution in and around the mitochondrial control region in birds.
1993,
Pubmed
Ranallo-Benavidez,
GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes.
2020,
Pubmed
Rao,
A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping.
2014,
Pubmed
Samonte,
Molecular phylogeny of Philippine freshwater sardines based on mitochondrial DNA analysis.
2000,
Pubmed
Simão,
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs.
2015,
Pubmed
Turanov,
Structure, evolution and phylogenetic informativeness of eelpouts (Cottoidei: Zoarcales) mitochondrial control region sequences.
2019,
Pubmed
Urbanczyk,
Genome sequence of Photobacterium mandapamensis strain svers.1.1, the bioluminescent symbiont of the cardinal fish Siphamia versicolor.
2011,
Pubmed
Wada,
LuxA gene of light organ symbionts of the bioluminescent fish Acropoma japonicum (Acropomatidae) and Siphamia versicolor (Apogonidae) forms a lineage closely related to that of Photobacterium leiognathi ssp. mandapamensis.
2006,
Pubmed
Xu,
OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species.
2019,
Pubmed
van Berkum,
Hi-C: a method to study the three-dimensional architecture of genomes.
2010,
Pubmed