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 The hidden pangenome: comparative genomics reveals pervasive diversity in symbiotic and free-living sulfur-oxidizing bacteria

2020 ◽  
Author(s):  
Rebecca Ansorge ◽  
Stefano Romano ◽  
Lizbeth Sayavedra ◽  
Maxim Rubin-Blum ◽  
Harald Gruber-Vodicka ◽  
...  
Keyword(s):  
Defense Mechanisms ◽  
Hydrothermal Vents ◽  
Driving Forces ◽  
Genetic Material ◽  
Genomic Analysis ◽  
Comparative Genomic ◽  
Free Living ◽  
Bacterial Populations ◽  
Genomic Studies ◽  
Sulfur Oxidizing

AbstractSulfur-oxidizing Thioglobaceae, often referred to as SUP05 and Arctic96BD clades, are widespread and common to hydrothermal vents and oxygen minimum zones. They impact global biogeochemical cycles and exhibit a variety of host-associated and free-living lifestyles. The evolutionary driving forces that led to the versatility, adoption of multiple lifestyles and global success of this family are largely unknown. Here, we perform an in-depth comparative genomic analysis using all available and newly generated Thioglobaceae genomes. Gene content variation was common, throughout taxonomic ranks and lifestyles. We uncovered a pool of variable genes within most Thioglobaceae populations in single environmental samples and we referred to this as the ‘hidden pangenome’. The ‘hidden pangenome’ is often overlooked in comparative genomic studies and our results indicate a much higher intra-specific diversity within environmental bacterial populations than previously thought. Our results show that core-community functions are different from species core genomes suggesting that core functions across populations are divided among the intra-specific members within a population. Defense mechanisms against foreign DNA and phages were enriched in symbiotic lineages, indicating an increased exchange of genetic material in symbioses. Our study suggests that genomic plasticity and frequent exchange of genetic material drives the global success of this family by increasing its evolvability in a heterogeneous environment.

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 Abundance of Reverse Tricarboxylic Acid Cycle Genes in Free-Living Microorganisms at Deep-Sea Hydrothermal Vents

2004 ◽  
Vol 70 (10) ◽  
pp. 6282-6289 ◽  
Author(s):  
Barbara J. Campbell ◽  
S. Craig Cary
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vents ◽  
Tricarboxylic Acid Cycle ◽  
Calvin Cycle ◽  
Tricarboxylic Acid ◽  
16S Rrna Genes ◽  
Rrna Genes ◽  
Free Living ◽  
Bisphosphate Carboxylase ◽  
Acid Cycle

ABSTRACT Since the discovery of hydrothermal vents more than 25 years ago, the Calvin-Bassham-Benson (Calvin) cycle has been considered the principal carbon fixation pathway in this microbe-based ecosystem. However, on the basis of recent molecular data of cultured free-living and noncultured episymbiotic members of the epsilon subdivision of Proteobacteria and earlier carbon isotope data of primary consumers, an alternative autotrophic pathway may predominate. Here, genetic and culture-based approaches demonstrated the abundance of reverse tricarboxylic acid cycle genes compared to the abundance of Calvin cycle genes in microbial communities from two geographically distinct deep-sea hydrothermal vents. PCR with degenerate primers for three key genes in the reverse tricarboxylic acid cycle and form I and form II of ribulose 1,5-bisphosphate carboxylase/oxygenase (Calvin cycle marker gene) were utilized to demonstrate the abundance of the reverse tricarboxylic acid cycle genes in diverse vent samples. These genes were also expressed in at least one chimney sample. Diversity, similarity matrix, and phylogenetic analyses of cloned samples and amplified gene products from autotrophic enrichment cultures suggest that the majority of autotrophs that utilize the reverse tricarboxylic acid cycle are members of the epsilon subdivision of Proteobacteria. These results parallel the results of previously published molecular surveys of 16S rRNA genes, demonstrating the dominance of members of the epsilon subdivision of Proteobacteria in free-living hydrothermal vent communities. Members of the epsilon subdivision of Proteobacteria are also ubiquitous in many other microaerophilic to anaerobic sulfidic environments, such as the deep subsurface. Therefore, the reverse tricarboxylic acid cycle may be a major autotrophic pathway in these environments and significantly contribute to global autotrophic processes.

scholarly journals Deep-sea mussels from a hybrid zone on the Mid-Atlantic Ridge host genetically indistinguishable symbionts

2021 ◽  
Author(s):  
Merle Ücker ◽  
Rebecca Ansorge ◽  
Yui Sato ◽  
Lizbeth Sayavedra ◽  
Corinna Breusing ◽  
...  
Keyword(s):  
Hybrid Zone ◽  
Deep Sea ◽  
Hydrothermal Vents ◽  
Geographic Location ◽  
Hybrid Zones ◽  
Natural Experiments ◽  
Orthologous Genes ◽  
Free Living ◽  
Single Nucleotide ◽  
Mid Atlantic Ridge

AbstractThe composition and diversity of animal microbiomes is shaped by a variety of factors, many of them interacting, such as host traits, the environment, and biogeography. Hybrid zones, in which the ranges of two host species meet and hybrids are found, provide natural experiments for determining the drivers of microbiome communities, but have not been well studied in marine environments. Here, we analysed the composition of the symbiont community in two deep-sea, Bathymodiolus mussel species along their known distribution range at hydrothermal vents on the Mid-Atlantic Ridge, with a focus on the hybrid zone where they interbreed. In-depth metagenomic analyses of the sulphur-oxidising symbionts of 30 mussels from the hybrid zone, at a resolution of single nucleotide polymorphism analyses of ~2500 orthologous genes, revealed that parental and hybrid mussels (F2–F4 generation) have genetically indistinguishable symbionts. While host genetics does not appear to affect symbiont composition in these mussels, redundancy analyses showed that geographic location of the mussels on the Mid-Atlantic Ridge explained most of the symbiont genetic variability compared to the other factors. We hypothesise that geographic structuring of the free-living symbiont population plays a major role in driving the composition of the microbiome in these deep-sea mussels.

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 Deep-sea mussels from a hybrid zone on the Mid-Atlantic Ridge host genetically indistinguishable symbionts

2020 ◽  
Author(s):  
Merle Ücker ◽  
Rebecca Ansorge ◽  
Yui Sato ◽  
Lizbeth Sayavedra ◽  
Corinna Breusing ◽  
...  
Keyword(s):  
Hybrid Zone ◽  
Deep Sea ◽  
Hydrothermal Vents ◽  
Geographic Location ◽  
Hybrid Zones ◽  
Natural Experiments ◽  
Orthologous Genes ◽  
Free Living ◽  
Single Nucleotide ◽  
Mid Atlantic Ridge

AbstractThe composition and diversity of animal microbiomes is shaped by a variety of factors, many of them interacting, such as host traits, the environment, and biogeography. Hybrid zones, in which the ranges of two host species meet and hybrids are found, provide natural experiments for determining the drivers of microbiome communities, but have not been well studied in marine environments. Here, we analysed the composition of the symbiont community in two deep-sea, Bathymodiolus mussel species along their known distribution range at hydrothermal vents on the Mid-Atlantic Ridge, with a focus on the hybrid zone where they interbreed. In-depth metagenomic analyses of the sulphur-oxidising symbionts of 30 mussels from the hybrid zone, at a resolution of single nucleotide polymorphism analyses of ∼2500 orthologous genes, revealed that parental and hybrid mussels have genetically indistinguishable symbionts. While host genetics does not appear to affect symbiont composition in these mussels, geographic location of the mussels on the Mid-Atlantic Ridge explained 45 % of symbiont genetic variability based on redundancy analyses. We hypothesize that geographic structuring of the free-living symbiont population plays a major role in driving the composition of the microbiome in these deep-sea mussels.

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