Scallop-bacteria symbiosis from the deep sea reveals strong genomic coupling in the absence of cellular integration.

Previous studies have revealed tight metabolic complementarity between bivalves and their endosymbiotic chemosynthetic bacteria, but little is known about their interactions with ectosymbionts. Our analysis of the ectosymbiosis between a deep-sea scallop (Catillopecten margaritatus) and a gammaproteobacterium showed that bivalves could be highly interdependent with their ectosymbionts as well. Our microscopic observation revealed abundant sulfur-oxidizing bacteria (SOB) on the surfaces of the gill epithelial cells. Microbial 16S rRNA gene amplicon sequencing of the gill tissues showed the dominance of the SOB. An analysis of the SOB genome showed that it is substantially smaller than its free-living relatives and has lost cellular components required for free-living. Genomic and transcriptomic analyses showed that this ectosymbiont relies on rhodanese-like proteins and SOX multienzyme complex for energy generation, mainly on the Calvin-Benson-Bassham (CBB) cycle and peripherally on a phosphoenolpyruvate carboxylase for carbon assimilation. Besides, the symbiont encodes an incomplete tricarboxylic acid (TCA) cycle. Observation of the scallop's digestive gland and its nitrogen metabolism pathways indicates it does not fully rely on the ectosymbiont for nutrition. Analysis of the host's gene expression provided evidence that it could offer intermediates for the ectosymbiont to complete its TCA cycle and some amino acid synthesis pathways using exosomes, and its phagosomes, endosomes, and lysosomes might be involved in harvesting nutrients from the symbionts. Overall, our study prompts us to rethink the intimacy between the hosts and ectosymbionts in Bivalvia and the evolution of chemosymbiosis in general.

The Impact of Different Regions of Interest on Shear Wave Elastography Assessment of the Meniscus in the Knee Joint.

RATIONALE AND OBJECTIVES: To investigate the impact of different regions of interest (ROI) on the assessment of shear wave elastography (SWE) in evaluating the meniscus of the knee joint. MATERIALS AND METHODS: After ethical approval, a total of 141 participants were enrolled in this prospective study from February to October 2023. SWE was utilized to evaluate the anterior horn of the lateral meniscus (LM) and medial meniscus (MM), using two different ROIs (ROI-Small and ROI-Trace) to measure the elastic mean value (Emean) and elastic maximum value (Emax). The differences in elasticity values between the normal menisci and torn menisci were compared, and the impact of different ROI selection methods on the diagnostic performance of elastic parameters in the torn menisci was assessed using receiver operating characteristic (ROC) curves. RESULTS: In Emean comparison, only MM in the tear group showed higher ROI-S than ROI-T. When comparing Emax, all ROI-T values were higher than the ROI-S values, and this difference was statistically significant. Different sizes of ROI did not significantly impact the diagnostic performance of Emean in LM and MM, nor the diagnostic effectiveness of Emax in LM. However, only the area under the curve (AUC) of MM for Emax in both ROI-S and ROI-T showed a statistically significant difference. CONCLUSION: The shear wave elasticity values and diagnostic performance may vary depending on the ROI settings. Therefore, it is recommended to use a 2 mm diameter ROI placed at the central position of the meniscus, with Emean as the elasticity index.

Dynamic changes in bacterial communities in three species of corals during the 2017 bleaching event in subtropical Hong Kong waters.

Bacteria play important roles in coral health, yet little is known about the dynamics of coral-associated bacterial communities during coral bleaching. Here, we reported the dynamic changes of bacterial communities in three scleractinian corals (Montipora peltiformis, Pavona decussata and Platygyra carnosa) during and after bleaching through amplicon sequencing. Our results revealed that the bacterial composition and dominant bacteria varied among the three coral species. The higher susceptibility of M. peltiformis to bleaching corresponded to a lower bacterial community diversity, and the dominant Synechococcus shifted in abundance during the bleaching and coral recovery phases. The resilient P. decussata and P. carnosa had higher bacterial diversity and a more similar bacterial composition between the healthy and bleached conditions. Overall, our study reveals the dynamic changes in coral-associated microbial diversity under different conditions, contributing to explaining the differential susceptibility of corals to extreme climate conditions.

Phylogenomic analyses reveal a single deep-water colonisation in Patellogastropoda.

Patellogastropoda, the true limpets, is a major group of gastropods widely distributed in marine habitats from the intertidal to deep sea. Though important for understanding their evolutionary radiation, the phylogenetic relationships among the patellogastropod families have always been challenging to reconstruct, with contradictory results likely due to insufficient sampling. Here, we obtained mitogenomic and phylogenomic data (transcriptomic or genomic) from six species representing the three predominantly deep-water patellogastropod families: Lepetidae, Neolepetopsidae, and Pectinodontidae. By using various phylogenetic methods, we show that mitogenome phylogeny recovers monophyly of eight families in most of the trees, though the relationships among families remain contentious. Meanwhile, a more robust family-level topology consistent with morphology was achieved by phylogenomics. This also reveals that these mainly deep-water families are monophyletic, suggesting a single colonisation of the deep water around the Jurassic. We also found a lack of significant correlation between genome size and habitat depth, despite some deep-water species exhibiting larger genome sizes. Our phylogenomic tree provides a stable phylogenetic backbone for Patellogastropoda that includes seven of the nine recognized families and paves the way for future evolutionary analyses in this major group of molluscs.

Genetic divergence and migration patterns of a galatheoid squat lobster highlight the need for deep-sea conservation.

Information on genetic divergence and migration patterns of vent- and seep-endemic macrobenthos can help delimit biogeographical provinces and provide scientific guidelines for deep-sea conservation under the growing threats of anthropogenic disturbances. Nevertheless, related studies are still scarce, impeding the informed conservation of these hotspots of deep-sea biodiversity. To bridge this knowledge gap, we conducted a population connectivity study on the galatheoid squat lobster Shinkaia crosnieri - a deep-sea foundation species widely distributed in vent and seep ecosystems in the Northwest Pacific. With the application of an interdisciplinary methodology involving population genomics and oceanographic approaches, we unveiled two semi-isolated lineages of S. crosnieri with limited and asymmetrical gene flow potentially shaped by the geographic settings, habitat types, and ocean currents - one comprising vent populations in the Okinawa Trough, with those inhabiting the southern trough area likely serving as the source; the other being the Jiaolong (JR) seep population in the South China Sea. The latter might have recently experienced a pronounced demographic contraction and exhibited genetic introgression from the Okinawa Trough lineage, potentially mediated by the intrusion of the North Pacific Intermediate Water. We then compared the biogeographic patterns between S. crosnieri and two other representative and co-occurring vent- and seep-endemic species using published data. Based on their biogeographical subdivisions and source-sink dynamics, we highlighted the southern Okinawa Trough vents and the JR seep warrant imperative conservation efforts to sustain the deep-sea biodiversity in the Northwest Pacific.

Podarkeopsischinensis sp. nov. (Annelida, Hesionidae) from southeastern China.

Podarkeopsischinensissp. nov. (Annelida, Hesionidae) is described based on specimens collected from the coast of southeast China. It is the first Podarkeopsis species described from the Indo-Pacific, although there are already nine valid Podarkeopsis species known from other parts of the world. This new species can be distinguished from the other Podarkeopsis species in having a palpostyle as long as the palpophore and double aciculae in both notopodia and neuropodia, and in bearing bifid furcate chaetae which have a smooth base on the shorter tine. A phylogenetic analysis based on the concatenated sequences of five gene fragments (COI, 16S rRNA, 18S rRNA, 28S rRNA, and histone H3) from 18 specimens of P.chinensissp. nov. showed that they formed a monophyletic clade that is sister to P.levifuscina. K2P genetic distances indicated that the four gene fragments (COI, 16S rRNA, 18S rRNA, and 28S rRNA) of P.chinensissp. nov. diverged from the corresponding sequences of the closest related species of Podarkeopsis in GenBank and BOLD Systems by 21.1-27.5%, 20.3-23.1%, 0.1-0.2%, and 2.1-3.2%. An identification key is provided for species in the genus Podarkeopsis.

A New Paralepetopsis Limpet from a South China Sea Seep Hints at a Paraphyletic Neolepetopsidae.

Neolepetopsidae is a little-studied true limpet family only known from deep-sea chemosynthetic ecosystems, containing just over a dozen species in three genera: Neolepetopsis, Paralepetopsis, and Eulepetopsis. Although considered monophyletic by a recent phylogenetic analysis, a lack of Paralepetopsis sequence linked to morphology casts some uncertainty. Here, we discovered a new species of Paralepetopsis from the Haima methane seep in the South China Sea, described as Paralepetopsis polita sp. nov. The new species is distinct from all other described Paralepetopsis by its smooth and semi-transparent shell, combined with a radula exhibiting pluricuspid teeth with two cusps. We tested its relationship with other neolepetopsids using a molecular phylogeny reconstructed from the mitochondrial COI gene, revealing a surprising position nested within Lepetidae, a family with a very different radula morphology. The clade containing lepetids and our new species was recovered sister to other neolepetopsids with sequence data available. This hints at a paraphyletic Neolepetopsidae, and suggests the neolepetopsid-type radula might not be exclusive to one monophyletic group of limpets.

Cold-water coral diversity along the continental shelf margin of northwestern South China Sea.

Scleractinian cold-water corals (CWCs) are one of the most important habitat engineers of the deep sea. Although the South China Sea (SCS) abuts the biodiversity center of scleractinian CWCs in the western Pacific, only a few sporadic records are available. We discovered new CWC sites by means of trawl sampling and video observation along the continental shelf of the northwestern SCS. All trawled scleractinian CWC specimens were identified to species level according to skeleton morphology and structure. The living CWCs and associated fauna recorded in the video were -identified to a higher level of classification. Scleractinian corals were identified to genus level, while non-scleractinian CWCs were identified to family level and given general names such as gorgonian corals, bamboo corals and black corals. Associated benthic dwellers were divided into major categories. A total of 28 scleractinian CWC species were identified to 7 families, 15 genera, and 1 additional subgenus. Among them, 13 species were colonial, including important habitat-forming species in the genera Eguchipsammia, Dendrophyllia and Cladopsammia. Non-scleractinian CWCs were identified to 7 families, including 4 families gorgonian corals, 1 family bamboo corals, and 2 families black corals. Gorgonian corals were the most abundant non-scleractinian CWCs in this region. Meanwhile, starfish, sea anemones, fish, gastropods, echinoderms, and other associated benthic fauna were recorded in the CWC habitats, with starfish belonging to the order Brisingida being most common. New scleractinian CWC assemblages were discovered along the continental seabed mounds in the northwestern SCS. This study highlights the remarkable diversity of cold-water scleractinian corals in the whole SCS, and shows the potential widespread distribution and conservation prospect of CWC habitats in this region.

Genomic Analysis of a Scale Worm Provides Insights into Its Adaptation to Deep-Sea Hydrothermal Vents.

Deep-sea polynoid scale worms endemic to hydrothermal vents have evolved an adaptive strategy to the chronically hypoxic environment, but its underlying molecular mechanisms remain elusive. Here, we assembled a chromosome-scale genome of the vent-endemic scale worm Branchipolynoe longqiensis (the first annotated genome in the subclass Errantia) and annotated two shallow-water polynoid genomes, aiming to elucidate the adaptive mechanisms. We present a genome-wide molecular phylogeny of Annelida which calls for extensive taxonomy revision by including more genomes from key lineages. The B. longqiensis genome with a genome size of 1.86 Gb and 18 pseudochromosomes is larger than the genomes of two shallow-water polynoids, possibly due to the expansion of various transposable elements (TEs) and transposons. We revealed two interchromosomal rearrangements in B. longqiensis when compared with the two shallow-water polynoid genomes. The intron elongation and interchromosomal rearrangement can influence a number of biological processes, such as vesicle transport, microtubules, and transcription factors. Furthermore, the expansion of cytoskeleton-related gene families may favor the cell structure maintenance of B. longqiensis in the deep ocean. The expansion of synaptic vesicle exocytosis genes has possibly contributed to the unique complex structure of the nerve system in B. longqiensis. Finally, we uncovered an expansion of single-domain hemoglobin and a unique formation of tetra-domain hemoglobin via tandem duplications, which may be related to the adaptation to a hypoxic environment.

Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment.

Previous studies have deciphered the genomic basis of host-symbiont metabolic complementarity in vestimentiferans, bathymodioline mussels, vesicomyid clams and Alviniconcha snails, yet little is known about the chemosynthetic symbiosis in Thyasiridae-a family of Bivalvia regarded as an excellent model in chemosymbiosis research due to their wide distribution in both deep-sea and shallow-water habitats. We report the first circular thyasirid symbiont genome, named Candidatus Ruthturnera sp. Tsphm01, with a size of 1.53 Mb, 1521 coding genes and 100% completeness. Compared to its free-living relatives, Ca. Ruthturnera sp. Tsphm01 genome is reduced, lacking components for chemotaxis, citric acid cycle and de novo biosynthesis of small molecules (e.g. amino acids and cofactors), indicating it is likely an obligate intracellular symbiont. Nevertheless, the symbiont retains complete genomic components of sulphur oxidation and assimilation of inorganic carbon, and these systems were highly and actively expressed. Moreover, the symbiont appears well-adapted to anoxic environment, including capable of anaerobic respiration (i.e. reductions of DMSO and nitrate) and possession of a low oxygen-adapted type of cytochrome c oxidase. Analysis of the host transcriptome revealed its metabolic complementarity to the incomplete metabolic pathways of the symbiont and the acquisition of nutrients from the symbiont via phagocytosis and exosome. By providing the first complete genome of reduced size in a thyasirid symbiont, this study enhances our understanding of the diversity of symbiosis that has enabled bivalves to thrive in chemosynthetic habitats. The resources will be widely used in phylogenetic, geographic and evolutionary studies of chemosynthetic bacteria and bivalves.

A draft genome assembly of reef-building octocoral Heliopora coerulea.

Coral reefs are under existential threat from climate change and anthropogenic impacts. Genomic studies have enhanced our knowledge of resilience and responses of some coral species to environmental stress, but reference genomes are lacking for many coral species. The blue coral Heliopora is the only reef-building octocoral genus and exhibits optimal growth at a temperature close to the bleaching threshold of scleractinian corals. Local and high-latitude expansions of Heliopora coerulea were reported in the last decade, but little is known about the molecular mechanisms underlying its thermal resistance. We generated a draft genome of H. coerulea with an assembled size of 429.9 Mb, scaffold N50 of 1.42 Mb and BUSCO completeness of 94.9%. The genome contains 239.1 Mb repetitive sequences, 27,108 protein coding genes, 6,225 lncRNAs, and 79 miRNAs. This reference genome provides a valuable resource for in-depth studies on the adaptive mechanisms of corals under climate change and the evolution of skeleton in cnidarian.

The 2022 summer marine heatwaves and coral bleaching in China's Greater Bay Area.

From July to August 2022, scleractinian coral communities in China's Greater Bay Area (GBA) in the northern South China Sea (nSCS) experienced an unprecedented bleaching event, despite the fact that coral communities in this area are often considered coral thermal refugia due to their high latitude distribution. Field surveys of six sites covering three main coral distribution areas of the GBA revealed that coral bleaching occurred at all sites. Bleaching was more severe in shallow water (1-3 m) than in deep water (4-6 m), as indicated by both percent bleached cover (51.80 ± 10.04% vs. 7.09 ± 7.37%) and bleached colonies (45.86 ± 11.22% vs. 6.58 ± 6.53%). Coral genera Acropora, Favites, Montipora, Platygyra, Pocillopora, and Porites showed high susceptibility to bleaching, and Acropora and Pocillopora suffered high post-bleaching mortality. In the three areas surveyed, analysis of oceanographic data detected marine heatwaves (MHWs) during the summer, with mean intensities between 1.62 and 1.97 °C and durations between 5 and 22 days. These MHWs were primarily driven by increased shortwave radiation due to strong western Pacific Subtropical High (WPSH), combined with reduced mixing between the surface and deep upwelling waters due to reduced wind speed. Comparing with histological oceanographic data showed that the 2022 MHWs were unprecedented, and there was a significant increase in the frequency, intensity, and total days of MHWs during 1982-2022. Furthermore, the heterogeneous distribution of summer MHW characteristics indicates that the coastal upwelling may modulate the spatial distribution of summer MHWs in nSCS through its cooling effect. Overall, our study indicates that MHWs may have affected the structure of the subtropical coral communities in the nSCS, and impaired their potential as thermal refugia.

Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm.

Endosymbiosis with chemosynthetic Gammaproteobacteria is widely recognized as an adaptive mechanism of siboglinid tubeworms, yet evolution of these endosymbionts and their driving forces remain elusive. Here, we report a finished endosymbiont genome (HMS1) of the cold-seep tubeworm Sclerolinum annulatum. The HMS1 genome is small in size, with abundant prophages and transposable elements but lacking gene sets coding for denitrification, hydrogen oxidization, oxidative phosphorylation, vitamin biosynthesis, cell pH and/or sodium homeostasis, environmental sensing, and motility, indicative of early genome erosion and adaptive evolution toward obligate endosymbiosis. Unexpectedly, a prophage embedded in the HMS1 genome undergoes lytic cycle. Highly expressed ROS scavenger and LexA repressor genes indicate that the tubeworm host likely activates the lysogenic phage into lytic cycle through the SOS response to regulate endosymbiont population and harvest nutrients. Our findings indicate progressive evolution of Sclerolinum endosymbionts toward obligate endosymbiosis and expand the knowledge about phage-symbiont-host interaction in deep-sea tubeworms.

A New Species of Box Jellyfish (Cnidaria: Tripedaliidae: Tripedalia) from Hong Kong, China.

We describe a box jellyfish, Tripedalia maipoensis sp. nov., based on samples collected from a shrimp pond in Hong Kong. This new species is morphologically distinct from other species of the family Tripedaliidae by the following combination of characters: (1) three pedalia at each bell corner; (2) each pedalium with one tentacle; and (3) velarium with forked canals. Phylogenetic analyses based on a concatenated dataset of the 16S, 18S and 28S rRNA genes show that T. maipoensis sp. nov. is sister to the morphologically similar species T. cystophora, but the two species exhibit 17.4% divergence in the 16S rRNA gene, supporting T. maipoensis sp. nov. as a distinct species. This new species represents the fourth described species of Tripedaliidae, and the first record of the family in Chinese coastal waters.

Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms.

Bacterial symbioses allow annelids to colonise extreme ecological niches, such as hydrothermal vents and whale falls. Yet, the genetic principles sustaining these symbioses remain unclear. Here, we show that different genomic adaptations underpin the symbioses of phylogenetically related annelids with distinct nutritional strategies. Genome compaction and extensive gene losses distinguish the heterotrophic symbiosis of the bone-eating worm Osedax frankpressi from the chemoautotrophic symbiosis of deep-sea Vestimentifera. Osedax's endosymbionts complement many of the host's metabolic deficiencies, including the loss of pathways to recycle nitrogen and synthesise some amino acids. Osedax's endosymbionts possess the glyoxylate cycle, which could allow more efficient catabolism of bone-derived nutrients and the production of carbohydrates from fatty acids. Unlike in most Vestimentifera, innate immunity genes are reduced in O. frankpressi, which, however, has an expansion of matrix metalloproteases to digest collagen. Our study supports that distinct nutritional interactions influence host genome evolution differently in highly specialised symbioses.

Micropodarke fujianensis n. sp. (Annelida: Hesionidae) from Fujian, China.

We describe M. fujianensis n. sp. (Annelida: Hesionidae), collected from the coast of Fujian Province, China, based on morphological and molecular analyses. Micropodarke fujianensis n. sp. is characterized by having two pairs of minute eyes, and neurochaetae of middle segments without basal long teeth. The K2P distances of COI, 16S rRNA, 18S rRNA, 28S rRNA, and histone H3 fragments diverged from the corresponding sequences of the closest related species of Micropodarke in GenBank and BOLD Systems by 22.3%, 10.7%, 0, 1.15%, and 1.1%, respectively. Among the Micropodarke species with such DNA sequences for comparison, M. fujianensis n. sp. is most closely related to M. cf. dubia-a species collected from Daya Bay, China. An updated key to Micropodarke species is provided.

Mitochondrial genome of Leocrates chinensis Kinberg, 1866 (Annelida: Hesionidae).

We report the complete mitochondrial genome of Leocrates chinensis Kinberg, 1866 - the type species of the genus. It is 15061 bp long, and contains 13 protein-coding genes (PCGs), 22 tRNA genes (tRNAs), and 2 rRNA genes (rRNAs), and 1 putative control region. Phylogenetic analysis indicated that L. chinensis was placed as sister to Sirsoe methanicola (BS = 100) of the same family Hesionidae.

Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis.

Endosymbiosis with Gammaproteobacteria is fundamental for the success of bathymodioline mussels in deep-sea chemosynthesis-based ecosystems. However, the recent discovery of Campylobacteria on the gill surfaces of these mussels suggests that these host-bacterial relationships may be more complex than previously thought. Using the cold-seep mussel ( Gigantidas haimaensis) as a model, we explored this host-bacterial system by assembling the host transcriptome and genomes of its epibiotic Campylobacteria and endosymbiotic Gammaproteobacteria and quantifying their gene and protein expression levels. We found that the epibiont applies a sulfur oxidizing (SOX) multienzyme complex with the acquisition of soxB from Gammaproteobacteria for energy production and switched from a reductive tricarboxylic acid (rTCA) cycle to a Calvin-Benson-Bassham (CBB) cycle for carbon assimilation. The host provides metabolic intermediates, inorganic carbon, and thiosulfate to satisfy the materials and energy requirements of the epibiont, but whether the epibiont benefits the host is unclear. The endosymbiont adopts methane oxidation and the ribulose monophosphate pathway (RuMP) for energy production, providing the major source of energy for itself and the host. The host obtains most of its nutrients, such as lysine, glutamine, valine, isoleucine, leucine, histidine, and folate, from the endosymbiont. In addition, host pattern recognition receptors, including toll-like receptors, peptidoglycan recognition proteins, and C-type lectins, may participate in bacterial infection, maintenance, and population regulation. Overall, this study provides insights into the complex host-bacterial relationships that have enabled mussels and bacteria to thrive in deep-sea chemosynthetic ecosystems.