Minxiao Wang

Deep-sea hydrothermal vents and methane seeps host unique animal communities sustained by chemosynthetic symbioses, yet how biological diversification proceeds across these geochemically distinct and geographically fragmented habitats remains poorly understood. Previous studies have largely focused on either host genomic adaptation or symbiont diversity as drivers of isolation, leaving unresolved how environmental geochemistry and host–microbe associations jointly shape evolutionary trajectories in chemosynthetic ecosystems. Here, we addressed this gap by combining chromosome-level host genomics, population resequencing, and episymbiont metagenomics in the deep-sea chemosynthetic lobster Shinkaia crosnieri, a dominant species inhabiting both hydrothermal vents and methane seeps. Genomic innovations—including sensory tradeoffs (vision loss versus chemosensory expansion), metabolic compensation for pigment loss, and positive selection on respiratory protein—underpin deep-sea colonization of S. crosnieri. Populations from the Okinawa Trough vent and the South China Sea seep exhibit pronounced genetic divergence, potentially driven by Pleistocene vicariance and reinforced by divergent selection across sulfur-enriched (vent) versus sulfur-depleted, methane-dominated (seep) environments. This selection targets host genes involved in chemoreception and immunity, with coordinated signatures in both sequence evolution and structural variation. Crucially, holobiont-level adaptation is amplified by habitat-specific recruitment of episymbionts: sulfur-oxidizing Campylobacterales/Thiotrichales dominate vent-associated lobsters, while methanotrophic Methylococcales prevail at seep counterparts. These symbionts partition energy niches metabolically, with seep-associated communities enhancing biosynthesis of key cofactors (e.g. coenzyme Q, tetrahydrofolate). Host transporters for these nutrients are concurrently upregulated, demonstrating functional synergy. Our findings establish that diversification in extreme environments operates holobiont-wide, where geochemical gradients synergistically shape host genomic plasticity and symbiont metabolic specialization to drive early-stage divergence.

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.

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 F _ST 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 R ² = 0.18879–0.34945; D ′ = 0.86803–0.91859; max F _ST = 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.

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.

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 hadal trench is the deepest part of the global ocean and harbors highly abundant microbial cells. However, the diversity and function of the majority of microbial communities in this part of the ocean are still unclear. Here, we collected 35 metagenomes from three push cores across different sites in both the northern and southern Yap trench to construct a comprehensive gene and genome dataset. A total of 32 million non-redundant genes were predicted from the whole metagenome datasets, with 63% assigned to known functional groups based on currently available databases. A total of 404 metagenome-assembled genomes (MAGs) with completeness >50% and contamination <10% were retrieved, and their taxonomy was highly diverse across 26 phyla. Alpha- and Gammaproteobacteria, Phycisphaerae, Nitrospiria, and Dehalococcoidia were dominant classes across all samples. The nonredundant gene and MAG datasets are valuable resources for advancing our understanding of the diversity, composition, and functions of microbiota in the sediment of the hadal trench.

Methane hydrates are a potential energy source, but their extraction may disrupt deep-sea ecosystems that rely on methane. Understanding biological responses to methane fluctuations in cold seep environments remains limited, primarily due to the inability to monitor subcellular metabolic dynamics in real time. This study applied confocal Raman microscopy combined with full-spectrum normalization to investigate subcellular metabolic adaptations in the gill tissues of the deep-sea mussel containing symbionts under methane deficiency. This label-free and nondestructive technique allows high-resolution quantitative analysis of biomolecules. Results demonstrate that methane deficiency induced metabolic reprogramming and structural reorganization, disrupting energy metabolism while enhancing proteolysis and lipolysis. Spatial heterogeneity is evident across cellular regions, with varying degrees of structural recovery and degradation highlighting differential resilience. These findings collectively underscore the indispensable role of methane in maintaining metabolic and structural homeostasis in deep-sea mussels, offering key insights into their adaptation strategies under methane deficiency and fundamental data for assessing the ecological impacts of methane extraction. The successful application of our methodology demonstrates broad potential for real-time metabolic monitoring in diverse organisms and for evaluating subcellular effects of environmental disturbances, establishing a new avenue for noninvasive, high-resolution quantitative metabolic tracking.