scholarly journals Genomic Insights Into Chemosynthetic Symbiosis in a Deep-Sea Hydrothermal Vent Mussel

Author(s):  
Kai Zhang ◽  
Yao Xiao ◽  
Jin Sun ◽  
Ting Xu ◽  
Kun Zhou ◽  
...  

Abstract Background Symbiosis with chemosynthetic bacteria has allowed many invertebrates to flourish in ‘extreme’ deep-sea chemosynthesis-based ecosystems, such as hydrothermal vents and cold seeps. Bathymodioline mussels are considered as models of deep-sea animal-bacteria symbiosis, but the diversity of molecular mechanisms governing host-symbiont interactions remains understudied owing to the lack of hologenomes. In this study, we adopted a total hologenome approach in sequencing the hydrothermal vent mussel Bathymodiolus marisindicus and the endosymbiont genomes combined with a transcriptomic and proteomic approach that explore the mechanisms of symbiosis. Results Here, we provide the first coupled mussel-endosymbiont genome assembly. Comparative genome analysis revealed that both Bathymodiolus marisindicus and its endosymbiont reshape their genomes through the expansion of gene families, likely due to chemosymbiotic adaptation. Functional differentiation of host immune-related genes and attributes of symbiont self-protection that likely facilitate the establishment of endosymbiosis. Hologenomic analyses offer new evidence that metabolic complementarity between the host and endosymbionts enables the host to compensate for its inability to synthesize some essential nutrients, and two pathways (digestion of symbionts and molecular leakage of symbionts) that can supply the host with symbiontderived nutrients. Results also showed that bacteriocin and abundant toxins of symbiont may contribute to the defense of the B. marisindicus holobiont. Moreover, an exceptionally large number of anti-virus systems were identified in the B. marisindicus symbiont, which likely work synergistically to efficiently protect their hosts from phage infection, indicating virus-bacteria interactions in intracellular environments of a deepsea vent mussel. Conclusions Our study provides novel insights into the mechanisms of symbiosis enabling deep-sea mussels to successfully colonize the special hydrothermal vent habitats.

2020 ◽  
Author(s):  
Hao Chen ◽  
Minxiao Wang ◽  
Huan Zhang ◽  
Hao Wang ◽  
Li Zhou ◽  
...  

Abstract Background:As the dominant species inhabiting both cold seeps and hydrothermal vents,Bathymodiolinae mussels are one of the most successful megafauna in the deep sea.They thrive in dark and food-insufficient environmentsby harboring sulfur-oxidizing bacteria (SOB)and/or methane-oxidizing bacteria (MOB)ingill bacteriocytesand obtain the majority of their nutrition from them.Many attempts have been made to decode the mechanisms underlying their symbiosis, which yetremained largely undisclosedfor years due to the lack of cultivable symbionts. In the present study,the globalexpression pattern of immune-related genes and miRNAswere surveyed inGigantidasplatifronsduring bacterial challengesusing enriched symbiontsor nonsymbioticVibrio in attempting to reveal the molecular mechanisms underlying chemosynthetic symbiosis. Results: Multiple PRRs such as TLRs, LRRs and C1q were found vigorously modulated during challenges whiledistinctly clusteredbetween symbiotic and nonsymbiotic bacteria stimulation. As downstream of the immune response,dozens of immune effectors including HSP70, P450, CD82 andvacuolar protein sorting-associated proteinwere modulated simultaneously, contributing to the fine tuning of cellular homeostasis, lysosome activity and bacteria engulfment in either symbiotic and nonsymbiotic bacteria challenge.A total of 459 miRNAs were identified in gill tissue of G. platifrons while dozens of themwere differentially expressedduring the challenge.Among these miRNAs, some were also found in differentexpression patternbetween symbiont or nonsymbiontchallenges and targeting apoptosis and phagosome maturation-related genes, including caspase8, inhibitor of apoptosis, cAMP-responsive element-binding protein,IκB, Rab and integrin. Conclusion:It was suggested that G. platifrons PRRs might function cooperativelyto facilitate the specialized immune recognition to MOBs or nonsymbioticbacteria. Meanwhile, a shared expression pattern of immune effectorswas observed between bacterial challenges, indicatingthe conservative response of Bathymodiolinae mussels in promoting the adhesion andengulfment of symbionts and nonsymbiont. Nevertheless, the differentially expressed miRNAs were yet suggested to facilitate specialized modulationinsymbiosis by repressing apoptosis- and phagosome maturation-related genes.With the orchestra of immune-related genes and miRNAs, G. platifronsmussels could therefore maintain arobust immune response against invading pathogens while establishing symbiosis with chemosynthetic bacteria.


Paleobiology ◽  
1995 ◽  
Vol 21 (4) ◽  
pp. 461-478 ◽  
Author(s):  
Kathleen A. Campbell ◽  
David J. Bottjer

Brachiopods generally have not been considered to be typical or significant faunal components of modern or ancient hydrothermal vent and cold-seep settings. The Early Cretaceous (Neocomian) rhynchonellide brachiopodPeregrinellahas long been viewed as a paleontological curiosity because of its distinctive morphology, status as the largest Mesozoic brachiopod, anomalous stratigraphic associations, and widespread, yet discontinuous paleogeographic distribution. Examination of all worldwidePeregrinellaoccurrences (14) indicates restriction of this brachiopod to ancient cold-seeps. It is probable thatPeregrinellagrew to large sizes in such great abundances at fossil cold-seep sites because of a richly organic food supply generated by localized fluid seepage and bacterial chemosynthetic activity. Living brachiopods are not known to harbor chemosymbiotic bacteria in their tissues; however, direct chemoautotrophic utilization of reduced fluids byPeregrinellacannot be rejected or demonstrated at present.Peregrinellaoccurs at widely separated cold-seeps of Neocomian age (e.g., California, Mexico, Tibet, Europe), yet its mode of dispersal and larval development is unknown. In modern hydrothermal vents of the deep-sea, organism dispersal occurs along oceanic ridges, where benthic faunas display both planktotrophic and nonplanktotrophic larval-mode types.Peregrinellamay represent a Mesozoic relic of a long-lived “lineage” of vent-seep associated rhynchonellides from the Paleozoic (e.g., ?Eoperegrinella, Dzieduszyckia), but major gaps in the stratigraphic record between these rhynchonellide occurrences, and the lack of rigorous phylogenetic analysis for these groups preclude a clear resolution of the origin(s) of vent-seep brachiopods at present.


Author(s):  
Jack Chi-Ho Ip ◽  
Ting Xu ◽  
Jin Sun ◽  
Runsheng Li ◽  
Chong Chen ◽  
...  

Abstract Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.


2005 ◽  
Vol 2 (2) ◽  
pp. 257-260 ◽  
Author(s):  
Gaku Tokuda ◽  
Akinori Yamada ◽  
Kazuma Nakano ◽  
Nao Arita ◽  
Hideo Yamasaki

Deep-sea hydrothermal vents and methane seeps are extreme environments that have a high concentration of hydrogen sulphide. However, abundant unique invertebrates including shrimps of the family Bresiliidae have been found in such environments. The bresiliid shrimps are believed to have radiated in the Miocene (less than 20 Myr); however, the period when and the mechanisms by which they dispersed across the hydrothermal vents and cold seeps in oceans worldwide have not been clarified. In the present study, we collected the deep-sea blind shrimp Alvinocaris longirostris from the hydrothermal vent site in the Okinawa Trough and carried out the first investigation of the 18S rRNA gene of a bresiliid shrimp. The phylogenetic analysis revealed that the bresiliid shrimp is situated at an intermediate lineage within the infraorder Caridea and shows monophyly with palaemonid shrimps, which live in shallow sea and freshwater. Furthermore, the mitochondrial cytochrome oxidase I ( COI ) gene sequences were analysed to determine the phylogenetic relationship with known bresiliid shrimps. A. longirostris of the Okinawa Trough had two haplotypes of the COI gene, one of which was identical to the Alvinocaris sp. of the cold seeps in Sagami Bay. These results indicate that a long-distance dispersal of A. longirostris occurred possibly within the last 100 000 years.


2020 ◽  
Vol 12 (6) ◽  
pp. 905-910 ◽  
Author(s):  
Ruoyu Liu ◽  
Kun Wang ◽  
Jun Liu ◽  
Wenjie Xu ◽  
Yang Zhou ◽  
...  

Abstract Cold seeps, characterized by the methane, hydrogen sulfide, and other hydrocarbon chemicals, foster one of the most widespread chemosynthetic ecosystems in deep sea that are densely populated by specialized benthos. However, scarce genomic resources severely limit our knowledge about the origin and adaptation of life in this unique ecosystem. Here, we present a genome of a deep-sea limpet Bathyacmaea lactea, a common species associated with the dominant mussel beds in cold seeps. We yielded 54.6 gigabases (Gb) of Nanopore reads and 77.9-Gb BGI-seq raw reads, respectively. Assembly harvested a 754.3-Mb genome for B. lactea, with 3,720 contigs and a contig N50 of 1.57 Mb, covering 94.3% of metazoan Benchmarking Universal Single-Copy Orthologs. In total, 23,574 protein-coding genes and 463.4 Mb of repetitive elements were identified. We analyzed the phylogenetic position, substitution rate, demographic history, and TE activity of B. lactea. We also identified 80 expanded gene families and 87 rapidly evolving Gene Ontology categories in the B. lactea genome. Many of these genes were associated with heterocyclic compound metabolism, membrane-bounded organelle, metal ion binding, and nitrogen and phosphorus metabolism. The high-quality assembly and in-depth characterization suggest the B. lactea genome will serve as an essential resource for understanding the origin and adaptation of life in the cold seeps.


2001 ◽  
Vol 67 (10) ◽  
pp. 4566-4572 ◽  
Author(s):  
Barbara J. Campbell ◽  
Christian Jeanthon ◽  
Joel E. Kostka ◽  
George W. Luther ◽  
S. Craig Cary

ABSTRACT Recent molecular characterizations of microbial communities from deep-sea hydrothermal sites indicate the predominance of bacteria belonging to the epsilon subdivision of Proteobacteria(epsilon Proteobacteria). Here, we report the first enrichments and characterizations of four epsilonProteobacteria that are directly associated withAlvinella pompejana, a deep sea hydrothermal vent polychete, or with hydrothermal vent chimney samples. These novel bacteria were moderately thermophilic sulfur-reducing heterotrophs growing on formate as the energy and carbon source. In addition, two of them (Am-H and Ex-18.2) could grow on sulfur lithoautrotrophically using hydrogen as the electron donor. Optimal growth temperatures of the bacteria ranged from 41 to 45°C. Phylogenetic analysis of the small-subunit ribosomal gene of the two heterotrophic bacteria demonstrated 95% similarity to Sulfurospirillum arcachonense, an epsilon Proteobacteria isolated from an oxidized marine surface sediment. The autotrophic bacteria grouped within a deeply branching clade of the epsilonProteobacteria, to date composed only of uncultured bacteria detected in a sample from a hydrothermal vent along the mid-Atlantic ridge. A molecular survey of various hydrothermal vent environments demonstrated the presence of two of these bacteria (Am-N and Am-H) in more than one geographic location and habitat. These results suggest that certain epsilonProteobacteria likely fill important niches in the environmental habitats of deep-sea hydrothermal vents, where they contribute to overall carbon and sulfur cycling at moderate thermophilic temperatures.


Author(s):  
Sabine Stöhr ◽  
Michel Segonzac

The animal communities associated with the deep-sea reducing environment have been studied for almost 30 years, but until now only a single species of ophiuroid, Ophioctenella acies, has been found at both hydrothermal vents and methane cold seeps. Since the faunal overlap between vent and seep communities is small and many endemic species have been found among other taxa (e.g. Mollusca, Crustacea), additional species of ophiuroids were expected at previously unstudied sites. Chemical compositions at reducing sites differ greatly from the nearby bathyal environment. Generally, species adapted to chemosynthetic environments are not found in non-chemosynthetic habitats, but occasional visitors of other bathyal species to vent and seep sites have been recorded among many taxa except ophiuroids. This paper presents an analysis of the ophiuroid fauna found at hydrothermal vents and non-reducing nearby sites on the Mid-Atlantic Ridge and on methane cold seeps in the Gulf of Mexico, at Blake Ridge off South Carolina and south of Barbados. In addition to O. acies, four species were found at vents, Ophiactis tyleri sp. nov., Ophiocten centobi, Ophiomitra spinea and Ophiotreta valenciennesi rufescens. While Ophioctenella acies appears to be restricted to chemosynthetic areas, the other four species were also found in other bathyal habitats. They also occur in low numbers (mostly single individuals), whereas species adapted to hydrothermal areas typically occur in large numbers. Ophioscolex tripapillatus sp. nov. and Ophiophyllum atlanticum sp. nov. are described from nearby non-chemosynthetic sites. In a cold seep south of Barbados, three species of ophiuroids were found, including Ophioctenella acies, Amphiura sp., Ophiacantha longispina sp. nov. and Ophioplinthaca chelys. From the cold seeps at Blake Ridge and the Gulf of Mexico, Ophienigma spinilimbatum gen. et sp. nov. is described, likely restricted to the reducing environment. Ophiotreta valenciennesi rufescens occurred abundantly among Lophelia corals in the Gulf of Mexico seeps, which is the first record of this species from the West Atlantic. Habitat descriptions complement the taxonomic considerations, and the distribution of the animals in reducing environments is discussed.


2020 ◽  
pp. 238-292 ◽  
Author(s):  
Richard J. Léveillé ◽  
S. Kim Juniper

2020 ◽  
Author(s):  
Yi Lan ◽  
Jin Sun ◽  
Chong Chen ◽  
Yanan Sun ◽  
Yadong Zhou ◽  
...  

AbstractAnimals endemic to deep-sea hydrothermal vents often form obligatory relationships with bacterial symbionts, maintained by intricate host-symbiont interactions. Endosymbiosis with more than one symbiont is uncommon, and most genomic studies focusing on such ‘dual symbiosis’ systems have not investigated the host and the symbionts to a similar depth simultaneously. Here, we report a novel dual symbiosis among the peltospirid snail Gigantopelta aegis and its two Gammaproteobacteria endosymbionts – one being a sulphur oxidiser and the other a methane oxidiser. We assembled high-quality genomes for all three parties of this holobiont, with a chromosome-level assembly for the snail host (1.15 Gb, N50 = 82 Mb, 15 pseudo-chromosomes). In-depth analyses of these genomes reveal an intimate mutualistic relationship with complementarity in nutrition and metabolic codependency, resulting in a system highly versatile in transportation and utilisation of chemical energy. Moreover, G. aegis has an enhanced immune capability that likely facilitates the possession of more than one type of symbiont. Comparisons with Chrysomallon squamiferum, another chemosymbiotic snail in the same family but only with one sulphur-oxidising endosymbiont, show that the two snails’ sulphur-oxidising endosymbionts are phylogenetically distant, agreeing with previous results that the two snails have evolved endosymbiosis independently and convergently. Notably, the same capabilities of biosynthesis of specific nutrition lacking in the host genome are shared by the two sulphur-oxidising endosymbionts of the two snail genera, which may be a key criterion in the selection of symbionts by the hosts.


2020 ◽  
Vol 96 (2) ◽  
pp. 699-714
Author(s):  
Jong Guk Kim ◽  
Jimin Lee

The genus Smacigastes Ivanenko & Defaye, 2004 (Harpacticoida, Copepoda) is the most primitive genus in the family Tegastidae Sars, 1904, occurring in deep-sea chemosynthetic environments, such as hydrothermal vents, cold seeps, whale falls and wood falls. Our exploration of the Onnuri Vent Field, the sixth active hydrothermal vent system in the Central Indian Ridge, resulted in the discovery of a new species in the genus Smacigastes. A detailed morphological analysis of S. pumilasp. nov. reveals that it most resembles S. barti Gollner, Ivanenko & Martínez Arbizu, 2008, described from a hydrothermal vent in the East Pacific Ridge; the new species can be distinguished from the existing species by the 8-segmented female antennule, the absence of an abexopodal seta on the antennary basis, the mandibular exopod represented by a single seta and the exopod of the first leg with five setae. This is the first record of Smacigastes in the Indian Ocean. A dichotomous key to species of the genus Smacigastes worldwide is provided.


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