Yue Song

Teleosts are the most prolific vertebrates, occupying the vast majority of aquatic environments, and their pectoral fins have undergone remarkable physiological transformations throughout their evolution. Studying early teleost fishes, such as those belonging to the Osteoglossiformes order, could offer crucial insights into the adaptive evolution of pectoral fins within this group. In this study, we have assembled a chromosomal-level genome for the Clown featherback (Chitala ornata), achieving the highest quality genome assembly for Osteoglossiformes to date, with a contig N50 of 32.78 Mb and a scaffold N50 of 40.73 Mb. By combining phylogenetic analysis, we determined that the Clown featherback diverged approximately 202 to 203 million years ago (Ma), aligning with continental separation events. Our analysis revealed the intriguing discovery that a unique deletion of regulatory elements is adjacent to the Gli3 gene, specifically in teleosts. This deletion might be tied to the specialized adaptation of their pectoral fins. Furthermore, our findings indicate that specific contractions and expansions of transposable elements (TEs) in teleosts, including the Clown featherback, could be connected to their adaptive evolution. In essence, this study not only provides a high-quality genomic resource for Osteoglossiformes but also sheds light on the evolutionary trajectory of early teleosts.

Aquatic vertebrates consist of jawed fish (cartilaginous fish and bony fish), aquatic mammals, reptiles and amphibians. Here, we present a comprehensive analysis of 630 aquatic vertebrate genomes to generate a standardized compendium of genomic data. We demonstrate its value by assessing their genome features as well as illuminating gene families related to the transition from water to land, such as Hox genes and olfactory receptor genes. We found that LINEs are the major transposable element (TE) type in cartilaginous fish and aquatic mammals, while DNA transposons are the dominate type in bony fish. To our surprise, TE types are not fixed in amphibians, the first group that transitioned to living on land. These results illustrate the value of a unified resource for comparative genomic analyses of aquatic vertebrates. Our data and strategy are likely to support all evolutionary and ecological research on vertebrates.

The scaly-foot snail (Chrysomallon squamiferum) is highly adapted to deep-sea hydrothermal vents and has drawn much interest since its discovery. However, the limited information on its genome has impeded further related research and understanding of its adaptation to deep-sea hydrothermal vents. Here, we report the whole-genome sequencing and assembly of the scaly-foot snail and another snail (Gigantopelta aegis), which inhabits similar environments. Using Oxford Nanopore Technology, 10X Genomics, and Hi-C technologies, we obtained a chromosome-level genome of C. squamiferum with an N50 size of 20.71 Mb. By constructing a phylogenetic tree, we found that these 2 deep-sea snails evolved independently of other snails. Their divergence from each other occurred ∼66.3 million years ago. Comparative genomic analysis showed that different snails have diverse genome sizes and repeat contents. Deep-sea snails have more DNA transposons and long terminal repeats but fewer long interspersed nuclear elements than other snails. Gene family analysis revealed that deep-sea snails experienced stronger selective pressures than freshwater snails, and gene families related to the nervous system, immune system, metabolism, DNA stability, antioxidation, and biomineralization were significantly expanded in scaly-foot snails. We also found 251 H-2 Class II histocompatibility antigen, A-U α chain-like (H2-Aal) genes, which exist uniquely in the Gigantopelta aegis genome. This finding is important for investigating the evolution of major histocompatibility complex (MHC) genes. Our study provides new insights into deep-sea snail genomes and valuable resources for further studies.

Background: With more than 30,000 species, fish—including bony, jawless, and cartilaginous fish—are the largest vertebrate group, and include some of the earliest vertebrates. Despite their critical roles in many ecosystems and human society, fish genomics lags behind work on birds and mammals. This severely limits our understanding of evolution and hinders progress on the conservation and sustainable utilization of fish. Results: Here, we announce the Fish10K project, a portion of the Earth BioGenome Project aiming to sequence 10,000 representative fish genomes in a systematic fashion within 10 years, and we officially welcome collaborators to join this effort. As a step towards this goal, we herein describe a feasible workflow for the procurement and storage of biospecimens, as well as sequencing and assembly strategies. Conclusions: To illustrate, we present the genomes of 10 fish species from a cohort of 93 species chosen for technology development.

Cataloging an accurate functional gene set for the Symbiodiniaceae species is crucial for addressing biological questions of dinoflagellate symbiosis with corals and other invertebrates. To improve the gene models of Fugacium kawagutii, we conducted high-throughput chromosome conformation capture (Hi-C) for the genome and Illumina combined with PacBio sequencing for the transcriptome to achieve a new genome assembly and gene prediction. A 0.937-Gbp assembly of F. kawagutii were obtained, with a N50 > 13 Mbp and the longest scaffold of 121 Mbp capped with telomere motif at both ends. Gene annotation produced 45,192 protein-coding genes, among which, 11,984 are new compared to previous versions of the genome. The newly identified genes are mainly enriched in 38 KEGG pathways including N-Glycan biosynthesis, mRNA surveillance pathway, cell cycle, autophagy, mitophagy, and fatty acid synthesis, which are important for symbiosis, nutrition, and reproduction. The newly identified genes also included those encoding O-methyltransferase (O-MT), 3-dehydroquinate synthase, homologous-pairing protein 2-like (HOP2) and meiosis protein 2 (MEI2), which function in mycosporine-like amino acids (MAAs) biosynthesis and sexual reproduction, respectively. The improved version of the gene set (Fugka_Geneset _V3) raised transcriptomic read mapping rate from 33% to 54% and BUSCO match from 29% to 55%. Further differential gene expression analysis yielded a set of stably expressed genes under variable trace metal conditions, of which 115 with annotated functions have recently been found to be stably expressed under three other conditions, thus further developing the “core gene set” of F. kawagutii. This improved genome will prove useful for future Symbiodiniaceae transcriptomic, gene structure, and gene expression studies, and the refined “core gene set” will be a valuable resource from which to develop reference genes for gene expression studies.

The African eggplant (Solanum aethiopicum) is a nutritious traditional vegetable used in many African countries, including Uganda and Nigeria. It is thought to have been domesticated in Africa from its wild relative, Solanum anguivi. S. aethiopicum has been routinely used as a source of disease resistance genes for several Solanaceae crops, including Solanum melongena. A lack of genomic resources has meant that breeding of S. aethiopicum has lagged behind other vegetable crops. We assembled a 1.02-Gb draft genome of S. aethiopicum, which contained predominantly repetitive sequences (78.9%). We annotated 37,681 gene models, including 34,906 protein-coding genes. Expansion of disease resistance genes was observed via 2 rounds of amplification of long terminal repeat retrotransposons, which may have occurred ∼1.25 and 3.5 million years ago, respectively. By resequencing 65 S. aethiopicum and S. anguivi genotypes, 18,614,838 single-nucleotide polymorphisms were identified, of which 34,171 were located within disease resistance genes. Analysis of domestication and demographic history revealed active selection for genes involved in drought tolerance in both “Gilo” and “Shum” groups. A pan-genome of S. aethiopicum was assembled, containing 51,351 protein-coding genes; 7,069 of these genes were missing from the reference genome. The genome sequence of S. aethiopicum enhances our understanding of its biotic and abiotic resistance. The single-nucleotide polymorphisms identified are immediately available for use by breeders. The information provided here will accelerate selection and breeding of the African eggplant, as well as other crops within the Solanaceae family.

With more than 30,000 species, fish are the largest and most ancient vertebrate group. Despite their critical roles in many ecosystems and human society, fish genomics lags behind work on birds and mammals. This severely limits our understanding of evolution and hinders progress on the conservation and sustainable utilization of fish. Here, we announce the Fish10K project, an international collaborative project or initiative? aiming to sequence 10,000 representative fish genomes under a systematic context within ten years, and officially welcome collaborators to join this effort. As a step towards this goal, we herein describe a feasible workflow for the procurement and storage of biospecimens, and sequencing and assembly strategies. To illustrate, we present the genomes of ten fish species from a cohort of 93 species chosen for technology development.

Trans-splicing mechanisms have been documented in many lineages that are widely distributed phylogenetically, including dinoflagellates. The spliced leader (SL) sequence itself is conserved in dinoflagellates, although its gene sequences and arrangements have diversified within or across different species. In this study, we present 18 Fugacium kawagutii SL genes identified from stranded RNA-seq reads. These genes typically have a single SL but can contain several partial SLs with lengths ranging from 103 to 292 bp. Unexpectedly, we find the SL gene transcripts contain sequences upstream of the canonical SL, suggesting that generation of mature transcripts will require additional modifications following trans-splicing. We have also identified 13 SL-like genes whose expression levels and length are comparable to Dino-SL genes. Lastly, introns in these genes were identified and a new site for Sm-protein binding was proposed. Overall, this study provides a strategy for fast identification of SL genes and identifies new sequences of F. kawagutii SL genes to supplement our understanding of trans-splicing.

Cartilaginous fishes have a very high phenotypical diversity, a phenomenon for which the mechanisms have been largely unexplored. Here, we report the genome of the white-spotted bamboo shark as the first chromosome-level genome assembly of cartilaginous fish. Using this genome, we illustrated a dynamic chromosome rearrangement process in the bamboo shark, which resulted in the formation of 13 chromosomes, all of which were sparsely distributed with conserved genes and fast-evolving. We found the fast-evolving chromosomes to be enriched in immune-related genes with two chromosomes harboring the major genes for developing the single-chain antibody. We also found chromosome rearrangements to have resulted in the loss of two genes ( p2rx3 and p2rx5 ) which we also showed were involved in cartilage development using a CRISPR/Cas9 approach in zebrafish. Our study highlighted the significance of chromosome rearrangements in the phenotypical evolution of cartilaginous fishes, providing clues to inform further studies on mechanisms for fish diversification.