Genomic Signatures Supporting the Symbiosis and Formation of Chitinous Tube in the Deep-Sea Tubeworm Paraescarpia echinospica.

Vestimentiferan tubeworms are iconic animals that present as large habitat-forming chitinized tube bushes in deep-sea chemosynthetic ecosystems. They are gutless and depend entirely on their endosymbiotic sulfide-oxidizing chemoautotrophic bacteria for nutrition. Information on the genomes of several siboglinid endosymbionts has improved our understanding of their nutritional supplies. However, the interactions between tubeworms and their endosymbionts remain largely unclear due to a paucity of host genomes. Here, we report the chromosome-level genome of the vestimentiferan tubeworm Paraescarpia echinospica. We found that the genome has been remodeled to facilitate symbiosis through the expansion of gene families related to substrate transfer and innate immunity, suppression of apoptosis, regulation of lysosomal digestion, and protection against oxidative stress. Furthermore, the genome encodes a programmed cell death pathway that potentially controls the endosymbiont population. Our integrated genomic, transcriptomic, and proteomic analyses uncovered matrix proteins required for the formation of the chitinous tube and revealed gene family expansion and co-option as evolutionary mechanisms driving the acquisition of this unique supporting structure for deep-sea tubeworms. Overall, our study provides novel insights into the host's support system that has enabled tubeworms to establish symbiosis, thrive in deep-sea hot vents and cold seeps, and produce the unique chitinous tubes in the deep sea.

Comparative Proteomics on Deep-Sea Amphipods after in Situ Copper Exposure.

The interest in deep-sea mining increased along with the environmental concerns of these activities to the deep-sea fauna. The discovery of optimal biomarkers of deep-sea mining activities in deep-sea species is a crucial step toward the supply of important ecological information for environmental impact assessment. In this study, an in situ copper exposure experiment was performed on deep-sea scavenging amphipods. Abyssorchomene distinctus individuals were selected among all the exposed amphipods for molecular characterization. Copper concentration within the gut was assessed, followed by a tandem mass tag-based coupled with two-dimensional liquid chromatography-mass spectrometry/mass spectrometry (LC-MS/MS) applied to identify and quantify the protein expression changes after 48 h of exposure. 2937 proteins were identified and annotated, and 1918 proteins among all identified proteins were assigned by at least two nonambiguous peptides. The screening process was performed based on the differences in protein abundance and the specific correlation between the proteins and copper in previous studies. These differentially produced proteins include Na+/K+ ATPase, cuticle, chitinase, and proteins with unknown function. Their abundances showed correlation with copper and had high sensitivity to indicate the copper level, being here proposed as biomarker candidates for deep-sea mining activities in the future. This is a key step in the development of environmental impact assessment of deep-sea mining activities integrating ecotoxicological data.

Changes in community structures and functions of the gut microbiomes of deep-sea cold seep mussels during in situ transplantation experiment.

BACKGROUND: Many deep-sea invertebrates largely depend on chemoautotrophic symbionts for energy and nutrition, and some of them have reduced functional digestive tracts. By contrast, deep-sea mussels have a complete digestive system although symbionts in their gills play vital roles in nutrient supply. This digestive system remains functional and can utilise available resources, but the roles and associations among gut microbiomes in these mussels remain unknown. Specifically, how the gut microbiome reacts to environmental change is unclear. RESULTS: The meta-pathway analysis showed the nutritional and metabolic roles of the deep-sea mussel gut microbiome. Comparative analyses of the gut microbiomes of original and transplanted mussels subjected to environmental change revealed shifts in bacterial communities. Gammaproteobacteria were enriched, whereas Bacteroidetes were slightly depleted. The functional response for the shifted communities was attributed to the acquisition of carbon sources and adjusting the utilisation of ammonia and sulphide. Self-protection was observed after transplantation. CONCLUSION: This study provides the first metagenomic insights into the community structure and function of the gut microbiome in deep-sea chemosymbiotic mussels and their critical mechanisms for adapting to changing environments and meeting of essential nutrient demand.

Endosymbiont population genomics sheds light on transmission mode, partner specificity, and stability of the scaly-foot snail holobiont.

The scaly-foot snail (Chrysomallon squamiferum) inhabiting deep-sea hydrothermal vents in the Indian Ocean relies on its sulphur-oxidising gammaproteobacterial endosymbionts for nutrition and energy. In this study, we investigate the specificity, transmission mode, and stability of multiple scaly-foot snail populations dwelling in five vent fields with considerably disparate geological, physical and chemical environmental conditions. Results of population genomics analyses reveal an incongruent phylogeny between the endosymbiont and mitochondrial genomes of the scaly-foot snails in the five vent fields sampled, indicating that the hosts obtain endosymbionts via horizontal transmission in each generation. However, the genetic homogeneity of many symbiont populations implies that vertical transmission cannot be ruled out either. Fluorescence in situ hybridisation of ovarian tissue yields symbiont signals around the oocytes, suggesting that vertical transmission co-occurs with horizontal transmission. Results of in situ environmental measurements and gene expression analyses from in situ fixed samples show that the snail host buffers the differences in environmental conditions to provide the endosymbionts with a stable intracellular micro-environment, where the symbionts serve key metabolic functions and benefit from the host's cushion. The mixed transmission mode, symbiont specificity at the species level, and stable intracellular environment provided by the host support the evolutionary, ecological, and physiological success of scaly-foot snail holobionts in different vents with unique environmental parameters.

Hologenome analysis reveals dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis.

Animals endemic to deep-sea hydrothermal vents often form obligatory symbioses with bacteria, maintained by intricate host-symbiont interactions. Most genomic studies on holobionts have not investigated both sides to similar depths. Here, we report dual symbiosis in the peltospirid snail Gigantopelta aegis with two gammaproteobacterial endosymbionts: a sulfur oxidiser and a methane oxidiser. We assemble high-quality genomes for all three parties, including a chromosome-level host genome. Hologenomic analyses reveal mutualism with nutritional complementarity and metabolic co-dependency, highly versatile in transporting and using chemical energy. Gigantopelta aegis likely remodels its immune system to facilitate dual symbiosis. Comparisons with Chrysomallon squamiferum, a confamilial snail with a single sulfur-oxidising gammaproteobacterial endosymbiont, show that their sulfur-oxidising endosymbionts are phylogenetically distant. This is consistent with previous findings that they evolved endosymbiosis convergently. Notably, the two sulfur-oxidisers share the same capabilities in biosynthesising nutrients lacking in the host genomes, potentially a key criterion in symbiont selection.

Nearest vent, dearest friend: biodiversity of Tiancheng vent field reveals cross-ridge similarities in the Indian Ocean.

Biodiversity of hydrothermal vents in the Indian Ocean, particularly those on the Southwest Indian Ridge (SWIR), are still relatively poorly understood. The Tiancheng field on the SWIR was initially reported with only a low-temperature diffuse flow venting area, but here we report two new active areas, including a chimney emitting high-temperature vent fluids. Biological sampling in these new sites doubled the known megafauna and macrofauna richness reported from Tiancheng. Significantly, we found several iconic species, such as the scaly-foot snail and the first Alviniconcha population on the SWIR. Tiancheng shares a high proportion of taxa with vents on the Central Indian Ridge (CIR) and lacks a number of key taxa that characterize other vents investigated so far on the SWIR. Population genetics of the scaly-foot snail confirmed this, as the Tiancheng population was clustered with populations from the CIR, showing low connectivity with the Longqi field. Unlike the previously examined populations, scales of the Tiancheng scaly-foot snail were coated in zinc sulfide, although this results only from precipitation. The close connection between Tiancheng and CIR vents indicates that the dispersal barrier for vent endemic species is not the Rodriguez Triple Junction as previously suggested but the transformation faults between Tiancheng and Longqi, warranting further studies on deep currents in this area to resolve the key barrier, which has important implications for biological conservation.

Genomic, transcriptomic, and proteomic insights into the symbiosis of deep-sea tubeworm holobionts.

Deep-sea hydrothermal vents and methane seeps are often densely populated by animals that host chemosynthetic symbiotic bacteria, but the molecular mechanisms of such host-symbiont relationship remain largely unclear. We characterized the symbiont genome of the seep-living siboglinid Paraescarpia echinospica and compared seven siboglinid-symbiont genomes. Our comparative analyses indicate that seep-living siboglinid endosymbionts have more virulence traits for establishing infections and modulating host-bacterium interaction than the vent-dwelling species, and have a high potential to resist environmental hazards. Metatranscriptome and metaproteome analyses of the Paraescarpia holobiont reveal that the symbiont is highly versatile in its energy use and efficient in carbon fixation. There is close cooperation within the holobiont in production and supply of nutrients, and the symbiont may be able to obtain nutrients from host cells using virulence factors. Moreover, the symbiont is speculated to have evolved strategies to mediate host protective immunity, resulting in weak expression of host innate immunity genes in the trophosome. Overall, our results reveal the interdependence of the tubeworm holobiont through mutual nutrient supply, a pathogen-type regulatory mechanism, and host-symbiont cooperation in energy utilization and nutrient production, which is a key adaptation allowing the tubeworm to thrive in deep-sea chemosynthetic environments.