scholarly journals Discovery of chemoautotrophic symbiosis in the giant shipwormKuphus polythalamia(Bivalvia: Teredinidae) extends wooden-steps theory

2017 ◽  
Vol 114 (18) ◽  
pp. E3652-E3658 ◽  
Author(s):  
Daniel L. Distel ◽  
Marvin A. Altamia ◽  
Zhenjian Lin ◽  
J. Reuben Shipway ◽  
Andrew Han ◽  
...  
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vents ◽  
Digestive System ◽  
Phylogenetic Position ◽  
Sulfur Oxidizing ◽  
Chemoautotrophic Symbiosis ◽  
Decaying Wood ◽  
Organic Deposits ◽  
Wood Boring ◽  
Wood Digestion

The “wooden-steps” hypothesis [Distel DL, et al. (2000)Nature403:725–726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalveKuphus polythalamia. This rare and enigmatic species, which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show thatK. polythalamiaharbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate thatK. polythalamiais a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example in which a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.

scholarly journals Potential Interactions between Clade SUP05 Sulfur-Oxidizing Bacteria and Phages in Hydrothermal Vent Sponges

2019 ◽  
Vol 85 (22) ◽  
Author(s):  
Kun Zhou ◽  
Rui Zhang ◽  
Jin Sun ◽  
Weipeng Zhang ◽  
Ren-Mao Tian ◽  
...  
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Okinawa Trough ◽  
Sulfur Metabolism ◽  
Extreme Environments ◽  
Metagenomic Sequence ◽  
Sulfur Oxidizing ◽  
Biological Entities ◽  
Sulfur Oxidizing Bacteria

ABSTRACT In deep-sea hydrothermal vent environments, sulfur-oxidizing bacteria belonging to the clade SUP05 are crucial symbionts of invertebrate animals. Marine viruses, as the most abundant biological entities in the ocean, play essential roles in regulating the sulfur metabolism of the SUP05 bacteria. To date, vent sponge-associated SUP05 and their phages have not been well documented. The current study analyzed microbiomes of Haplosclerida sponges from hydrothermal vents in the Okinawa Trough and recovered the dominant SUP05 genome, designated VS-SUP05. Phylogenetic analysis showed that VS-SUP05 was closely related to endosymbiotic SUP05 strains from mussels living in deep-sea hydrothermal vent fields. Homology and metabolic pathway comparisons against free-living and symbiotic SUP05 strains revealed that the VS-SUP05 genome shared many features with the deep-sea mussel symbionts. Supporting a potentially symbiotic lifestyle, the VS-SUP05 genome contained genes involved in the synthesis of essential amino acids and cofactors that are desired by the host. Analysis of sponge-associated viral sequences revealed putative VS-SUP05 phages, all of which were double-stranded viruses belonging to the families Myoviridae, Siphoviridae, Podoviridae, and Microviridae. Among the phage sequences, one contig contained metabolic genes (iscR, iscS, and iscU) involved in iron-sulfur cluster formation. Interestingly, genome sequence comparison revealed horizontal transfer of the iscS gene among phages, VS-SUP05, and other symbiotic SUP05 strains, indicating an interaction between marine phages and SUP05 symbionts. Overall, our findings confirm the presence of SUP05 bacteria and their phages in sponges from deep-sea vents and imply a beneficial interaction that allows adaptation of the host sponge to the hydrothermal vent environment. IMPORTANCE Chemosynthetic SUP05 bacteria dominate the microbial communities of deep-sea hydrothermal vents around the world, SUP05 bacteria utilize reduced chemical compounds in vent fluids and commonly form symbioses with invertebrate organisms. This symbiotic relationship could be key to adapting to such unique and extreme environments. Viruses are the most abundant biological entities on the planet and have been identified in hydrothermal vent environments. However, their interactions with the symbiotic microbes of the SUP05 clade, along with their role in the symbiotic system, remain unclear. Here, using metagenomic sequence-based analyses, we determined that bacteriophages may support metabolism in SUP05 bacteria and play a role in the sponge-associated symbiosis system in hydrothermal vent environments.

Numerical taxonomy of heterotrophic sulfur-oxidizing bacteria isolated from southwestern Pacific hydrothermal vents

1994 ◽  
Vol 40 (8) ◽  
pp. 690-697 ◽  
Author(s):  
Pascale Durand ◽  
Afeda Benyagoub ◽  
Daniel Prieur
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vents ◽  
Numerical Taxonomy ◽  
Lau Basin ◽  
The North ◽  
Nitrate Reducers ◽  
Sulfur Oxidizing ◽  
North Fiji Basin ◽  
Back Arc ◽  
Sulfur Oxidizing Bacteria

Sulfur-oxidizing bacteria (n = 161) were enriched and isolated from samples of vent water, invertebrates, and chimney rocks collected at two deep-sea hydrothermal vents (2000 m) in back-arc basins from the southwestern Pacific: the North Fiji Basin and the Lau Basin. Several types of heterotrophic sulfur-oxidizing bacteria were repeatedly isolated. They oxidized thiosulfate either to sulfate (acid producing) or to polythionate (base producing). In most of the acid-producing cultures, thiosulfate was transitorily oxidized to polythionate. All of the bacteria were Gram negative, 37% were fermentative, and 88% were denitrifiers or nitrate reducers. Numerical taxonomy and analysis of the G+C content showed that they belong to several genera including Pseudomonas, Acinetobacter, and Vibrio.Key words: hydrothermal vent, culturable thiosulfate-oxidizing bacteria, numerical taxonomy.

scholarly journals Novel Forms of Structural Integration between Microbes and a Hydrothermal Vent Gastropod from the Indian Ocean

2004 ◽  
Vol 70 (5) ◽  
pp. 3082-3090 ◽  
Author(s):  
Shana K. Goffredi ◽  
Anders Warén ◽  
Victoria J. Orphan ◽  
Cindy L. Van Dover ◽  
Robert C. Vrijenhoek
Keyword(s):  
Indian Ocean ◽  
Deep Sea ◽  
Hydrothermal Vents ◽  
Iron Sulfides ◽  
Dense Population ◽  
Isotopic Signatures ◽  
Structural Integration ◽  
Esophageal Gland ◽  
The Indian Ocean ◽  
Sulfur Oxidizing

ABSTRACT Here we describe novel forms of structural integration between endo- and episymbiotic microbes and an unusual new species of snail from hydrothermal vents in the Indian Ocean. The snail houses a dense population of γ-proteobacteria within the cells of its greatly enlarged esophageal gland. This tissue setting differs from that of all other vent mollusks, which harbor sulfur-oxidizing endosymbionts in their gills. The significantly reduced digestive tract, the isotopic signatures of the snail tissues, and the presence of internal bacteria suggest a dependence on chemoautotrophy for nutrition. Most notably, this snail is unique in having a dense coat of mineralized scales covering the sides of its foot, a feature seen in no other living metazoan. The scales are coated with iron sulfides (pyrite and greigite) and heavily colonized by ε- and δ-proteobacteria, likely participating in mineralization of the sclerites. This novel metazoan-microbial collaboration illustrates the great potential of organismal adaptation in chemically and physically challenging deep-sea environments.

scholarly journals Diversity matters: Deep-sea mussels harbor multiple symbiont strains

2019 ◽  
Author(s):  
Rebecca Ansorge ◽  
Stefano Romano ◽  
Lizbeth Sayavedra ◽  
Anne Kupczok ◽  
Halina E. Tegetmeyer ◽  
...  
Keyword(s):  
Deep Sea ◽  
Defense Mechanisms ◽  
Hydrothermal Vents ◽  
Low Cost ◽  
Intracellular Bacteria ◽  
Adaptive Potential ◽  
Free Living ◽  
Nutrient Sources ◽  
Metabolic Functions ◽  
Sulfur Oxidizing

AbstractGenetic diversity of closely-related free-living microbes is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Indeed, symbiont strain diversity has long assumed to be restricted in intracellular bacteria associated with animals. Here, we sequenced the metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key metabolic functions, such as the use of energy and nutrient sources, electron acceptors and viral defense mechanisms. Most strain-specific genes were expressed, highlighting their adaptive potential. We show that fine-scale diversity is pervasive in Bathymodiolus symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, not the host, feeds the symbionts.

scholarly journals De Novo Genome Assembly of Limpet Bathyacmaea lactea (Gastropoda: Pectinodontidae): The First Reference Genome of a Deep-Sea Gastropod Endemic to Cold Seeps

2020 ◽  
Vol 12 (6) ◽  
pp. 905-910 ◽  
Author(s):  
Ruoyu Liu ◽  
Kun Wang ◽  
Jun Liu ◽  
Wenjie Xu ◽  
Yang Zhou ◽  
...  
Keyword(s):  
Deep Sea ◽  
Metal Ion ◽  
De Novo ◽  
Demographic History ◽  
Gene Families ◽  
Phylogenetic Position ◽  
Cold Seeps ◽  
Nitrogen And Phosphorus ◽  
De Novo Genome Assembly ◽  
A Genome

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.

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