The deep sea, as the largest and maybe most hostile environment on Earth, is still underexplored, especially regarding its genetic repertoire. Yet, previous work has revealed significant habitat-specific deep-sea biodiversity. Here, we present an integrated deep-sea microbial genetic dataset comprising 502 million nonredundant genes from 2,138 samples and 2.4 million predicted structures and use it to link specific protein structures with genetic variants associated with life in the deep sea and to assess their biotechnology potential. Combining global sequence analysis with biophysical and biochemical measurements revealed unprecedented sequence diversity and substantial structural conservation of proteins. Especially, proteins involved in replication, recombination, and repair were identified as being under rapid evolution and with specialized properties. Among these, a structurally divergent helicase exhibited advantages in controlling nanopore sequencing speed. Thus, our work positions the deep sea as an evolutionary engine that generates and hosts genetic diversity and bridges genetic knowledge with biotechnology.

Solemyidae, an ancient lineage of protobranch bivalves, are characterized by unique morphology and obligate symbiosis with sulfur-oxidizing bacteria, enabling survival in sulfide-rich sediments. However, limited genomic resources have hindered understanding of their evolutionary history, symbiotic interactions, and environmental adaptation. Here, we report a chromosome-level reference genome of Acharax haimaensis, assembled using PacBio, Illumina, and Hi-C sequencing. The 4.27 Gb genome, with a scaffold N50 of 195.52 Mb, was anchored to 22 chromosomes and achieved high completeness (98.2%) based on BUSCO. Transposable elements occupy 50.17% of the assembly, dominated by long interspersed nuclear elements (14.20%). We predicted 38,343 protein-coding genes, of which 87.25% were functionally annotated. Macrosynteny analysis revealed each chromosome comprises two to four segments of ancestral linkage groups, indicating extensive chromosomal breakage and fusion in early bivalve evolution. Phylogenetic inference suggested A. haimaensis diverged from the common ancestor of Autobranchia ~550 Mya. This first deep-sea protobranch genome provides an essential resource for exploring bivalve evolution and the genetic basis of symbiosis and adaptation to extreme environments.

The effects of dietary rumen-protected glucose (RPG) supplementation on Dumengsa sheep growth performance, meat quality, and transcriptomic and metabolomic profiling are reported. Twelve sheep were randomly assigned to a control (basal diet, n = 6) or RPG (basal diet +1.0% RPG, n = 6) group for 100 d. RPG increased serum malondialdehyde (P = 0.015) and cholesterol (P = 0.046) concentrations, enhanced intramuscular fat content (P = 0.016), and tended to produce lower meat lightness (P = 0.072), redness (P = 0.053), and hue angle (P = 0.072) values. In total, 319 differentially expressed genes and 30 differentially abundant metabolites were identified. Transcriptomic analysis revealed RPG to alter the expression of genes related to oxidative phosphorylation, β-oxidation, and fat deposition. Metabolomic analysis revealed that RPG supplementation primarily increases the abundance of short-chain fatty acids. Integrated analysis using a Data Integration Analysis for Biomarker discovery using Latent Components (DIABLO) model revealed a strong and significant correlation (r = 0.93) between omics profiles. We report dietary supplementation with 1% RPG to modulate muscle lipid metabolism and potentially stimulate intramuscular fat deposition, but also to possibly induce a state of potential oxidative stress.

ABSTRACT Extreme environments, though hostile to most life forms, host specialized extremophile communities that have redefined biological cognition and emerged as vital biotechnological resources, with their unique adaptive traits and bioactive molecules driving advances in multiple scientific and industrial fields. However, research on extremophiles is hindered by limitations in culture-based methods, fragmented multi-omics data with non-uniform annotation standards across repositories, the lack of cross-extreme comparative research in existing resources, and the singularity of data dimensionality that neglects key structural information, all of which restrict the functional interpretation of extremophile microbes and the exploitation of their bioprospecting potential. To tackle these challenges, we developed ExMODE ( https://db.genomics.cn/exmode/ ), a comprehensive multi-omics database platform dedicated to extremophiles. It centrally integrates multi-omics data from diverse extreme habitats with a standardized annotation framework, resolving data fragmentation and enabling systematic cross-environment comparative analyses to elucidate extremophile adaptive mechanisms. Moreover, ExMODE aggregates multi-dimensional datasets including genes, genomes, secondary metabolite sequences and protein structures, overcoming the constraints of single-dimensional data and significantly improving the efficiency of biotechnological resource discovery from extreme microorganisms.

Deep-sea chemosynthetic ecosystems, critical for global methane and sulphur cycling, require accurate connectivity data for effective conservation planning amid increasing anthropogenic threats. Because hosts and their environmentally acquired symbionts operate at fundamentally different spatial and temporal scales, we analysed each at the scale appropriate to its biology: host Gigantidas platifrons population structure was assessed both regionally (across 11 Northwest Pacific chemosynthetic sites) and within a single cold seep (Site F, South China Sea) across six shell-length cohorts spanning < 1 year to > 100 years, while the methanotrophic endosymbiont Methyloprofundus sp. was profiled across the same cohorts at Site F to test whether its genetic composition tracks host age or is environmentally homogenized. We found that although the overall host population at Site F is panmictic (ADMIXTURE K = 1; max FST near zero), it exhibits significant fine-scale kinship structure within size cohorts. Kinship decreases sharply with geographic distance (p < 0.001), indicating distance-limited larval replenishment via localized burst recruitment events. In contrast, the methanotrophic symbiont Methyloprofundus sp. is genetically homogeneous across all six host shell-length cohorts at Site F (LD R2 = 0.18879-0.34945; D' = 0.86803-0.91859; max FST = 0.0352; π < 0.0022; overall Tajima's D = -0.5088), consistent with continuous environmental acquisition from a stable, well-mixed local reservoir, thereby buffering the holobiont's core function. Our findings highlight that the host's strong reliance on highly localized recruitment makes population persistence vulnerable to local disturbance. These findings directly challenge conservation models that assume high connectivity and mandate site-specific, holobiont-focused management protecting local breeding stock and age structure.

Deep-sea polymetallic nodules harbor unique microbial communities adapted to the distinctly extreme conditions, yet their functional potential remains poorly understood due to scarce metagenomic data. Here, we generated and expanded metagenomic dataset comprising 46 samples (22 newly sequenced and 24 publicly available) derived from deep-sea polymetallic nodules and their associated sediments collected across multiple Pacific Ocean regions. Metagenomic assembly and gene prediction produced over 147 million protein-coding sequences, which were clustered into a non-redundant gene catalog of more than 65 million representative genes. Approximately 62.0% of genes receiving functional assignments with eggNOG, KEGG, and Pfam database. Genome binning and dereplication yielded 617 species-level metagenome-assembled genomes spanning 41 diverse bacterial and archaeal phyla. Together, the non-redundant gene catalog and metagenome-assembled genomes collection provide a reference resource for comparative genomics, functional annotation, and ecological analyses of microbial communities associated with deep-sea nodule-bearing environments, and support future studies on microbial diversity, metabolic potential, and environmental assessments in abyssal ecosystems.

Aurelia coerulea (moon jellyfish), a radially symmetrical metazoan in the phylum Cnidaria, possesses key features pertinent to understanding the evolutionary origins of nervous systems. Here, we employed a combination of long-read sequencing, short-read sequencing, and Hi-C chromatin conformation capture techniques to generate a chromosome-level assembly of the A. coerulea genome. The final assembly comprises approximately 554.10 Mb distributed across 21 chromosomes, achieving a scaffold N50 of 24.06 Mb and demonstrating high completeness (protein BUSCO score: 93.0%). Approximately 71.48% of the genome consists of transposable elements. We identified 26,777 protein-coding genes, of which approximately 72.28% have been functionally annotated. This chromosome-level genome provides an essential resource for elucidating early neural evolution and advancing our understanding of cnidarian biology.

The deep sea, as the largest and maybe most hostile environment on Earth, is still underexplored, especially regarding its genetic repertoire. Yet, previous work has revealed significant habitat-specific deep-sea biodiversity. Here, we present an integrated deep-sea microbial genetic dataset comprising 502 million nonredundant genes from 2,138 samples and 2.4 million predicted structures and use it to link specific protein structures with genetic variants associated with life in the deep sea and to assess their biotechnology potential. Combining global sequence analysis with biophysical and biochemical measurements revealed unprecedented sequence diversity and substantial structural conservation of proteins. Especially, proteins involved in replication, recombination, and repair were identified as being under rapid evolution and with specialized properties. Among these, a structurally divergent helicase exhibited advantages in controlling nanopore sequencing speed. Thus, our work positions the deep sea as an evolutionary engine that generates and hosts genetic diversity and bridges genetic knowledge with biotechnology.

Wood constitutes the largest reservoir of biogenic carbon on Earth, yet remarkably few animals can exploit it. While terrestrial wood-feeders like termites rely on highly diverse gut microbiomes, xylotrophic marine bivalves have evolved a fundamentally different approach: a spatially segregated system where intracellular gill symbionts produce enzymes that act remotely within a nearly sterile cecum. However, the genetic and evolutionary basis of this unique symbiosis remains largely elusive. Here, we integrate hologenomics, transcriptomics, and biochemistry of a shallow-water shipworm (Teredo navalis) and a deep-sea borer (Xyloredo sp.). We find that despite diverging approximately 147 million years ago and occupying drastically different habitats, these bivalves maintain a strictly conserved ancestral karyotype and a shared genomic architecture for wood digestion. Our models reveal a clear host-symbiont division of labor. The host genome is specialized for lignin modification and targeted enzyme transport, whereas a highly streamlined symbiont community is responsible for core polysaccharide degradation. Central to this minimalist strategy is a lineage-specific GH5-GH6 dual-catalytic enzyme. By sharing amino acids across proximal binding pockets, this fusion protein unites endo- and exo-cellulase activities, enabling highly synergistic cellulose cleavage without the need for complex microbial communities. Ultimately, our comparative analysis with terrestrial models demonstrates that these marine invertebrates achieve efficient biomass degradation not through microbial expansion, but through extreme functional streamlining and molecular innovation, offering a distinct evolutionary paradigm for marine carbon cycling.

Cold stress impacts lamb mortality, welfare, and productivity. Wool and skin insulate lambs, but the mechanisms underlying their response to colder environments remain unclear. Shorn lambs (n = 20) of similar age (8 months), of the Hulunbuir (n = 10; average 34.5 ± 0.70 kg) and Hu (n = 10; average 34.9 ± 0.79 kg) breeds, were raised at the Ecological and Agricultural Experimental Station, Gaolan, Gansu Province, People's Republic of China (36°13″ N, 103°47″ E), at an altitude of 1780 m above sea level. These lambs were divided into four equal groups: Hulunbuir at -20 °C (HB-20), Hulunbuir at 15 °C (HB+15), Hu at -20 °C (HU-20), and Hu at 15 °C (HU+15). The groups were maintained at these temperatures in temperature-controlled facilities for 38 days. Skin tissues were analyzed with transcriptome sequencing, and selected wool and physiological traits were assessed. The HB-20 lambs had greater wool length growth (1.8 ± 0.13 vs. 1.0 ± 0.46 cm, p < 0.001) and epidermis thickness (20.0 ± 1.20 vs. 14.6 ± 0.87 μm, p = 0.006) but lower hair follicle density (33.6 ± 2.11 vs. 42.7 ± 3.06 per mm2, p = 0.041), rectal temperature (38.1 ± 0.10 vs. 38.8 ± 0.04 °C, p < 0.001), and respiratory rate (15.5 ± 1.08 vs. 24.0 ± 1.89 breaths/min, p = 0.004), compared to the HB+15 lambs. Similar differences in these traits were observed with the Hu lambs at the two temperatures. Transcriptome analyses revealed the activation of pathways related to immune and endocrine systems, signal transduction, and development and regeneration, irrespective of breed at -20 °C. The TNF signaling pathway and osteoclast differentiation may play roles in cold adaptation, as they are associated with differentially expressed genes (DEGs) identified in the Hulunbuir lambs, as well as shared DEGs between both breeds. This study revealed physiological and molecular differences in lambs exposed to lower temperatures and suggests potential targets for improving cold tolerance, welfare, and productivity.

This study conducted a graded dose feeding trial evaluating Nitraria tangutorum fruit extract (NTFE) effects on ruminal volatile fatty acid (VFA) metabolism and microbial ecology in Hu sheep fed with high concentrate diet (65: 35, concentrate: forage). The trial included three groups: control (CON), low-dose NTFE (NT1; 10 g/kg diet), and high-dose NTFE (NT2; 20 g/kg diet). Compared to CON, NT2 significantly increased the ratio of acetate to propionate (A/P) while reducing propionate proportion (P < 0.05). Metagenomic revealed NTFE enhanced microbial alpha and beta diversity (P < 0.05). Notably, the NT2 elevated abundances of key fiber degrading microbes (Fibrobacter, Alistipes sp., Treponema bryantii, Aristaeella lactis) while reduced abundances of methanogenic archaea (LDA >2, P < 0.05). Microbial networks showed heightened modularity and stability through weakened interspecies competition. Functionally, NT2 amplified lysosome mediated substrate degradation and upregulated cellulase genes (GH5, GH5_37, GH43) (LDA >2, P < 0.05). Concurrently, NT2 stimulated biosynthesis of antimicrobial nonribosomal peptides while downregulating lipopolysaccharide pathways, suggesting anti-inflammatory benefits (LDA >2, P < 0.05). Correlation analyses and partial least squares path modeling (PLS-PM) demonstrated intricate relationships among fiber-degrading microbes, microbial functions, and VFA profiles. The extract directly modulated specific microbial taxa and functions via increased diversity, ultimately altering the acetate to propionate ratio in rumen fermentation (P < 0.05). In conclusion, NT2 optimally modulates rumen function by enriching fiber-degrading microbiota, enhancing carbohydrate-active enzymes, suppressing methanogens, and stabilizing microbial networks, ultimately improving fermentation efficiency while demonstrating anti-inflammatory potential.

During cold stress, gut microbes play crucial roles in orchestrating energy metabolism to enhance environmental adaptation. In sheep, hindgut microbes ferment carbohydrates to generate short-chain fatty acids (SCFAs) as an energy source. However, the mechanisms by which hindgut microbes and their metabolites interact with the host to facilitate adaptation to cold environments remain ambiguous. Herein, we simulated a winter environment (− 20 °C) and provided a rationed diet to compare the cold adaptation mechanisms between Hulunbuir and Hu sheep. Our findings show that cold exposure enhances SCFA metabolism in the sheep cecum. In Hu sheep, acetate, butyrate, and total SCFA concentrations increased, whereas in Hulunbuir sheep, propionate and butyrate concentrations increased, with a notable increase in total SCFAs. Notably, butyrate concentration was higher in Hulunbuir sheep than in Hu sheep under cold stress. Following cold exposure, the proinflammatory cytokine IL-1β levels increased in both breeds. In addition, Hu sheep showed increased IL-10, whereas Hulunbuir sheep exhibited elevated secretory IgA levels. The cecal microbiota responded differently, Hu sheep showed no notable changes in alpha and beta diversity, whereas Hulunbuir sheep exhibited considerable alterations. In Hu sheep, the abundance of fungi, specifically Blastocystis sp. subtype 4, decreased, and that of several Lachnospiraceae species (Roseburia hominis, Faecalicatena contorta, and Ruminococcus gnavus) involved in SCFA metabolism increased. Pathways related to carbohydrate metabolism, such as starch and sucrose metabolism, galactose metabolism, and pentose and glucuronate interconversions, were upregulated. In Hulunbuir sheep, the abundance of Treponema bryantii, Roseburia sp. 499, and Prevotella copri increased, with upregulation in pathways related to amino acid metabolism and energy metabolism. Cold exposure increased node connectivity within the symbiotic networks of both breeds, with increased network vulnerability in Hu sheep. Following cold exposure, the microbial community of Hulunbuir sheep showed a decrease in the influence of stochastic processes on community assembly, with a corresponding increase in the role of environmental selection. Conversely, no such shift was evident in Hu sheep. Further transcriptomic analysis revealed distinct regulatory mechanisms between breeds. In Hu sheep, protein synthesis, energy metabolism, and thermogenesis pathways were substantially upregulated. By contrast, Hulunbuir sheep showed considerable upregulation of immune pathways and energy conservation through reduced ribosome synthesis. Correlation analysis indicated that butyrate holds a central position in both networks, with Hulunbuir sheep exhibiting a more complex and tightly regulated network involving SCFAs, microbiota, microbial functions, and transcriptomes. Partial least squares path modeling revealed that cold exposure substantially altered the cecal microbiota and transcriptomes of Hulunbuir sheep, affecting SCFAs and cytokines. The findings of this study suggest that under cold exposure, Hu sheep enhance acetate fermentation and rely on tissue thermogenesis for adaptation. By contrast, Hulunbuir sheep exhibit changes in microbial diversity and function, leading to increased propionate and butyrate metabolism. This may promote physiological energy conservation and innate immune defense, balancing heat loss and enhancing cold adaptation.

An erratum of this article has been published full details can be found at 10.1099/ijsem.0.006854 A novel Gram-negative, oxidase- and catalase-positive, rod-shaped bacterium, designated strain KX21116 T , was isolated from the mussel Gigantidas platifrons collected from a cold seep field in the South China Sea. Strain KX21116 T grew optimally at 28 °C, pH 6.0 with 3% (w/v) NaCl, under aerobic and microaerobic conditions. Its genome size was 3.16 Mb, with a G+C content of 28.4 mol%. The 16S rRNA sequences revealed that strain KX21116 T was closely related to Arcobacter nitrofigilis DSM 7299 T (98.77% gene sequence similarity) and Arcobacter acticola AR-13 T (95.58%). Phylogenetic and phylogenomic analysis revealed that strain KX21116 T clustered with the type species of the genus Arcobacter , with A. nitrofigilis DSM 7299 T as its nearest neighbour. The genomic average nucleotide identity (orthoANI) values between strain KX21116 T and A. nitrofigilis DSM 7299 T were 92.74%, while the in silico DNA–DNA hybridization (GGDC) values of the two strains were 48.8%. The predominant fatty acids are C 16:0 , C 16:1 ω7 c/C1 6:1 ω6 c and C 18:1 ω7 c/C1 8:1 ω6 c. Based on a comparative analysis of phylogenetic, phylogenomic, phenotypic and chemotaxonomic characteristics, strain KX21116 T represents a novel species of the genus Arcobacter , for which the name Arcobacter iocasae sp. nov. is proposed. The type strain is KX21116 T (=MCCC 1K08505 T =KCTC 92900 T =JCM 35939 T ).

Lucinidae, renowned as the most diverse chemosymbiotic invertebrate group, functions as a sulfide cleaner in coastal ecosystems and is thus ecologically important. Despite their significance, genomic studies on these organisms have been limited. Here, we present the chromosome-level genome assembly of Indoaustriella scarlatoi, an intertidal lucinid clam. Employing both short and long reads, and Hi-C sequencing, we assembled a 1.58 Gb genome comprising 690 contigs with a contig N50 length of 9.00 Mb, which were anchored to 17 chromosomes. The genome exhibits a high completeness of 95.4%, as assessed by the BUSCO analysis. Transposable elements account for 56.02% of the genome, with long terminal repeat retrotransposons (LTR, 42.66%) being the most abundant. We identified 34,469 protein-coding genes, 74.43% of which were functionally annotated. This high-quality genome assembly serves as a valuable resource for further studies on the evolutionary and ecological aspects of chemosymbiotic bivalves.

Microbes in cold seep water columns are essential for methane sequestration and biogeochemical cycling, yet their structures and ecological functions, particularly at the bottom water interface (BWI), are poorly understood. Here, we performed metagenomic analyses to explore the microbial biodiversity and functions at the F-site cold seep in the South China Sea. Functional stratification revealed that photosynthetic autotrophs dominate surface zones, heterotrophs are prevalent in mesopelagic zones, and chemosynthetic bacteria are abundant at the BWI. We obtained 377 metagenome-assembled-genomes (MAGs) and constructed genome-scale metabolic models to unveil metabolic interactions facilitating the coupling of carbon, nitrogen, and sulfur among microbes, particularly at the BWI. Notably, methanotrophic bacteria with diverse metabolic capabilities distributed from the BWI zone to the deep mesopelagic regions, highlighting the broader influence of methane. In conclusion, our findings reveal a high degree of heterogeneity in the composition and function of microorganisms across the F-site cold seep water column. Our study also sheds light on the ecological interactions and environmental gradients that shape these microbial communities.

Wool has distinctive biological, physical, and chemical properties that contribute to its value both for the sheep and in global fibre and textile markets. Its fibres are primarily composed of proteins, principally keratin and keratin-associated proteins (KAPs). To better comprehend the genes that underpin key wool traits, this study examined the keratin-associated protein 36-1 gene (KRTAP36-1) in Chinese Tan lambs. We identified three previously reported alleles of the gene (named A, B and C) that were present in the lambs studied, with genotype frequencies as follows: 2.0% (n = 5; AA), 6.9% (n = 17; AB), 13.8% (n = 34; AC), 8.9% (n = 22; BB), 33.4% (n = 82; BC) and 35.0% (n = 86; CC). The frequencies of the individual alleles in the Chinese Tan lambs were 12.4%, 29.1% and 58.5% for alleles A, B and C, respectively. The three alleles were in Hardy–Weinberg Equilibrium. In an association analysis, it was revealed that allele C was associated with variation in the mean fibre curvature of the fine wool of the Chinese Tan lambs, but this association was not observed in their heterotypic hair fibres. This finding suggests that KRTAP36-1 might be differentially expressed in the wool follicles that produce the two fibre types, and that along with other KRTAP genes, it may be involved in determining fibre curvature and the distinctive curly coat of the lambs.

Cold-seep carbonates, formed through interactions among methane, fluid chemistry, and microbial chemosynthesis, represent biodiversity hotspots in the deep sea. Spatial heterogeneity within these carbonates arises from variations in methane flux, yet the microbial contributions to this heterogeneity remain underexplored. Here we combined remotely operated vehicle-based in situ measurements, X-ray imaging, metagenomics, qPCR, and 13C-CH4 stable-isotope labeling to investigate microbial communities across carbonate habitats in the South China Sea. We found that methane flux linked to carbonate structural properties, shapes microbial metabolic interactions, notably anaerobic methane oxidation coupled with aragonite and FeS precipitation. These processes may contribute to self-sealing carbonate features, potentially reducing methane permeability and influencing geochemical gradients and geomorphology. Our findings reveal that microbiomes and their feedbacks play a significant role in shaping habitat-scale spatial heterogeneity of cold-seep carbonates, improving our understanding of methane cycling and carbonate ecosystem dynamics.

Functional annotation of proteins from extreme environments represents a major bottleneck for bioresource discovery, as a vast reservoir of functional dark matter defies existing homology-based methods. We demonstrate that environmental pressures impart conserved physicochemical energy signatures that co-determine protein function with sequence and structure. Here we developed ACCESS, a multimodal graph neural network employing hierarchical contrastive learning with a tailored label-sample co-embedding to fuse energy, sequence, and structural information and overcome homology scarcity. ACCESS surpasses state-of-the-art methods including BLASTp and CLEAN in annotating low-identity enzymes. Applied to extreme environmental metagenomics, we constructed a function map of extremophile enzymes to expand the biocatalyst library, pinpointed functionally critical residues to guide rational design, and enabled large-scale, function-based macro-evolutionary analyses. This paradigm transcends the limitations of homology, illuminating protein dark matter and accelerating the exploration of the biosphere’s functional diversity for applications in biotechnology and therapeutic development. ### Competing Interest Statement The authors have declared no competing interest. National Key Research and Development Program of China, 2025YFC2817100

Arylsulfatase catalyzes the cleavage of sulfate ester bonds and plays a role in agar desulfation, thereby enhancing agar gel strength and quality. While studying the desulfurization pathway in Pseudoalteromonassp. SR43-6, a sequence encoding a potential arylsulfatase-Pseudoalteromonas Ars (Ps-Ars)-was found. The enzyme, with p-nitrophenyl sulfate as a substrate, exhibited optimal activity at 35 °C and pH 8.0. Its relative activity (206 U/mg) exceeded that of the recently identified arylsulfatases. Four hundred units of the enzyme removed 86.4% of sulfate groups from Gelidium amansii agar in 4 h, whereas 800 U of the enzyme removed 71.3% of sulfate groups from Gracilaria lemaneiformis agar in 8 h. After enzymatic treatment, G. amansii agar gel strength was enhanced by 32%, and a similar improvement was observed in G. lemaneiformis agar gel strength. Enzymatic agar desulfurization offers mild, quality-retaining, and environmentally friendly advantages, augmenting industrial application prospects.

Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings. We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism’s ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments. Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.