Host-symbiont population genomics provide insights into partner fidelity, transmission mode and habitat adaptation in deep-sea hydrothermal vent snails

Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species level associations that might influence genetic structuring, connectivity and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across a ~800 km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with local strains of their specific symbiont phylotypes, which confirms a model of horizontal transmission in both Ifremeria and Alviniconcha. Strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor wide-spread genetic connectivity and ecological resilience unless physical dispersal barriers are present.

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Growth and Phylogenetic Properties of Novel Bacteria Belonging to the Epsilon Subdivision of the Proteobacteria Enriched fromAlvinella pompejana and Deep-Sea Hydrothermal Vents

Applied and Environmental Microbiology ◽

10.1128/aem.67.10.4566-4572.2001 ◽

2001 ◽

Vol 67 (10) ◽

pp. 4566-4572 ◽

Cited By ~ 102

Author(s):

Barbara J. Campbell ◽

Christian Jeanthon ◽

Joel E. Kostka ◽

George W. Luther ◽

S. Craig Cary

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Heterotrophic Bacteria ◽

Geographic Location ◽

Optimal Growth ◽

Small Subunit ◽

Ribosomal Gene ◽

Moderately Thermophilic ◽

Novel Bacteria

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.

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Dual symbiosis in the deep-sea hydrothermal vent snail Gigantopelta aegis revealed by its hologenome

10.1101/2020.09.23.308304 ◽

2020 ◽

Author(s):

Yi Lan ◽

Jin Sun ◽

Chong Chen ◽

Yanan Sun ◽

Yadong Zhou ◽

...

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Snail Host ◽

Bacterial Symbionts ◽

Mutualistic Relationship ◽

Genomic Studies ◽

Similar Depth ◽

Selection Of ◽

Chromosome Level

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.

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262 Voyages Beneath the Sea: a global assessment of macro- and megafaunal biodiversity and research effort at deep-sea hydrothermal vents

PeerJ ◽

10.7717/peerj.7397 ◽

2019 ◽

Vol 7 ◽

pp. e7397 ◽

Cited By ~ 4

Author(s):

Andrew D. Thaler ◽

Diva Amon

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Research Effort ◽

Spreading Center ◽

Biological Research ◽

Northwest Pacific ◽

North East ◽

East Pacific ◽

Biogeographic Provinces

For over 40 years, hydrothermal vents and the communities that thrive on them have been a source of profound discovery for deep-sea ecologists. These ecosystems are found throughout the world on active plate margins as well as other geologically active features. In addition to their ecologic interest, hydrothermal vent fields are comprised of metallic ores, sparking a nascent industry that aims to mine these metal-rich deposits for their mineral wealth. Here, we provide the first systematic assessment of macrofaunal and megafaunal biodiversity at hydrothermal vents normalized against research effort. Cruise reports from scientific expeditions as well as other literature were used to characterize the extent of exploration, determine the relative biodiversity of different biogeographic provinces, identify knowledge gaps related to the distribution of research effort, and prioritize targets for additional sampling to establish biodiversity baselines ahead of potential commercial exploitation. The Northwest Pacific, Southwest Pacific, and Southern Ocean biogeographic provinces were identified as high biodiversity using rarefaction of family-level incidence data, whereas the North East Pacific Rise, Northern East Pacific, Mid-Atlantic Ridge, and Indian Ocean provinces had medium biodiversity, and the Mid-Cayman Spreading Center was identified as a province of relatively low biodiversity. A North/South divide in the extent of biological research and the targets of hydrothermal vent mining prospects was also identified. Finally, we provide an estimate of sampling completeness for each province to inform scientific and stewardship priorities.

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Simple harpacticoid composition observed at deep hydrothermal vent sites on sea knoll calderas in the North-west Pacific

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315421000874 ◽

2022 ◽

pp. 1-10

Author(s):

Futa Nakasugi ◽

Motohiro Shimanaga ◽

Hidetaka Nomaki ◽

Hiromi Kayama Watanabe ◽

Tomo Kitahashi ◽

...

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Environmental Parameters ◽

Sea Floor ◽

North West ◽

Isotopic Signatures ◽

Carbon Isotopic ◽

The North ◽

Spatial Differences

Abstract Dirivultid copepods (Siphonostomatoida), one of the most successful meiobenthic organisms found at deep-sea hydrothermal vents, have been the focus of most previous ecological studies among meiofauna in these habitats. The ecology of Harpacticoida, a major benthic copepod group in typical deep-sea floor, however, is not well understood in terms of variations in community structure and controlling factors at venting sites. The spatial heterogeneities in benthic harpacticoid composition and their association with environmental parameters were investigated at hydrothermal vent chimney structures in the calderas of three neighbouring sea knolls (Bayonnaise Knoll, Myojin Knoll and Myojin-sho Caldera) in the western North Pacific. While a previous study had reported the distribution of dirivultids was strongly associated with spatial differences in stable carbon isotopic signatures (δ13C) of organic matter in the detritus on active chimneys in the field, multivariate analyses detected no significant corelation between the parameter and harpacticoid composition in this study. Instead, high associations of the harpacticoid composition with differences in water depth and total organic carbon (TOC) concentration were detected. Ectinosomatidae dominated at vent sites with lower TOC values in the shallowest Bayonnaise Knoll, while they were less prevalent at deeper vent fields in the other knolls, where Miraciidae was the most abundant family. This study indicated the availability of vent chemoautotrophic carbon is not a primary factor controlling the composition of harpacticoids even in the habitats on the hydrothermal vents, but instead by the food amount, regardless of its resources (including marine snow from the sea surface), in the study area.

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A community-supported metaproteomic pipeline for improving peptide identifications in hydrothermal vent microbiota

Briefings in Bioinformatics ◽

10.1093/bib/bbab052 ◽

2021 ◽

Author(s):

Yafei Chang ◽

Qilian Fan ◽

Jialin Hou ◽

Yu Zhang ◽

Jing Li

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Extreme Environments ◽

Reference Database ◽

False Discovery Rate Method ◽

Analysis Strategy ◽

Gene Database ◽

And Function ◽

Functional Profiles

Abstract Microorganisms in deep-sea hydrothermal vents provide valuable insights into life under extreme conditions. Mass spectrometry-based proteomics has been widely used to identify protein expression and function. However, the metaproteomic studies in deep-sea microbiota have been constrained largely by the low identification rates of protein or peptide. To improve the efficiency of metaproteomics for hydrothermal vent microbiota, we firstly constructed a microbial gene database (HVentDB) based on 117 public metagenomic samples from hydrothermal vents and proposed a metaproteomic analysis strategy, which takes the advantages of not only the sample-matched metagenome, but also the metagenomic information released publicly in the community of hydrothermal vents. A two-stage false discovery rate method was followed up to control the risk of false positive. By applying our community-supported strategy to a hydrothermal vent sediment sample, about twice as many peptides were identified when compared with the ways against the sample-matched metagenome or the public reference database. In addition, more enriched and explainable taxonomic and functional profiles were detected by the HVentDB-based approach exclusively, as well as many important proteins involved in methane, amino acid, sugar, glycan metabolism and DNA repair, etc. The new metaproteomic analysis strategy will enhance our understanding of microbiota, including their lifestyles and metabolic capabilities in extreme environments. The database HVentDB is freely accessible from http://lilab.life.sjtu.edu.cn:8080/HventDB/main.html.

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A new squat lobster species of the genus Munida Leach, 1820 (Crustacea: Anomura: Galatheoidea: Munididae) from hydrothermal vents on the Eastern Pacific Rise

Zootaxa ◽

10.11646/zootaxa.4743.1.12 ◽

2020 ◽

Vol 4743 (1) ◽

pp. 131-136 ◽

Cited By ~ 1

Author(s):

XINMING LIU ◽

XINZHENG LI ◽

RONGCHENG LIN

Keyword(s):

New Species ◽

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Eastern Pacific ◽

Single Specimen ◽

Squat Lobster ◽

The Third ◽

A New Species

A new species of the genus Munida Leach, 1820, is described and illustrated based on a single specimen from the deep-sea hydrothermal vent on the Eastern Pacific Rise. Munida alba sp. nov. closely resembles M. ampliantennulata Komai, 2011, M. watatsumin Komai, 2014. and M. magniantennulata, but differences in the morphologies of the third maxilliped, pollex of the cheliped and the third segment of the antennal peduncle readily distinguish the new species from the three relatives. The new species is the fourth of the genus occurring at the hydrothermal vent areas.

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Cutting through the smoke: the diversity of microorganisms in deep-sea hydrothermal plumes

Royal Society Open Science ◽

10.1098/rsos.160829 ◽

2017 ◽

Vol 4 (4) ◽

pp. 160829 ◽

Cited By ~ 4

Author(s):

Anni Djurhuus ◽

Svein-Ole Mikalsen ◽

Helge-Ansgar Giebel ◽

Alex D. Rogers

Keyword(s):

Community Composition ◽

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Microbial Community Composition ◽

Illumina Miseq ◽

Black Smoker ◽

Microbial Composition ◽

Diffuse Flow ◽

Environmental Selection

There are still notable gaps regarding the detailed distribution of microorganisms between and within insular habitats such as deep-sea hydrothermal vents. This study investigates the community composition of black smoker vent microorganisms in the Southern Hemisphere, and changes thereof along a spatial and chemical gradient ranging from the vent plume to surrounding waters. We sampled two hydrothermal vent fields, one at the South West Indian Ridge (SWIR), the other at the East Scotia Ridge (ESR). Samples were collected across vent fields at varying vertical distances from the origin of the plumes. The microbial data were sequenced on an Illumina MiSeq platform for the 16SrRNA gene. A substantial amount of vent-specific putative chemosynthetic microorganisms were found, particularly in samples from focused hydrothermal venting. Common vent-specific organisms from both vent fields were the genera Arcobacter , Caminibacter and Sulfurimonas from the Epsilonproteobacteria and the SUP05 group from the Gammaproteobacteria. There were no major differences in microbial composition between SWIR and ESR for focused plume samples. However, within the ESR the diffuse flow and focused samples differed significantly in microbial community composition and relative abundance. For Epsilonproteobacteria, we found evidence of niche-specificity to hydrothermal vent environments. This taxon decreased in abundance by three orders of magnitude from the vent orifice to background water. Epsilonproteobacteria distribution followed a distance–decay relationship as vent-effluents mixed with the surrounding seawater. This study demonstrates strong habitat affinity of vent microorganisms on a metre scale with distinct environmental selection.

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Population connectivity of the crab Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) (Decapoda: Brachyura: Bythograeidae) from deep-sea hydrothermal vents in the northwestern Pacific

Journal of Crustacean Biology ◽

10.1093/jcbiol/ruaa045 ◽

2020 ◽

Vol 40 (5) ◽

pp. 556-562

Author(s):

Hiromi K Watanabe ◽

Chong Chen ◽

Shigeaki Kojima ◽

Shogo Kato ◽

Hiroyuki Yamamoto

Keyword(s):

Deep Sea ◽

Hydrothermal Vents ◽

Okinawa Trough ◽

Coi Gene ◽

Genetic Connectivity ◽

Reverse Direction ◽

Northwestern Pacific ◽

Brachyuran Crab ◽

The Okinawa Trough ◽

Mariana Arc

Abstract Genetic connectivity provides a basis for evaluating the resilience of animal communities by elucidating gene flow and serves as a proxy for realized dispersal through planktonic larval dispersal, settlement, and reproductive success. Gandalfus yunohana (Takeda, Hashimoto & Ohta, 2000) is a brachyuran crab endemic to deep-sea hydrothermal vents in the northwestern Pacific. Although an iconic and often dominant species, the connectivity among its populations is yet to be examined. We obtained barcoding sequences of the mitochondrial COI gene of G. yunohana from four vent fields including two on the Izu Arc, one on the northern Mariana Arc, and one in the Okinawa Trough. Genetic diversity of populations on the Izu and northern Mariana arcs were similar and shared the dominant haplotypes, showing no genetic subdivision regardless of the habitat depth. The Okinawa Trough population, for which only one specimen was available, was not genetically different from specimens from the Izu/Mariana arc populations. Estimation of the number of immigrants among populations suggests that the migration from north to south is higher than in the reverse direction. Our results resonate with previous laboratory-culture experiments, suggesting a high dispersal capability for G. yunohana. Visual observations and sampling, however, suggest that G. yunohana is exceedingly rare in the Okinawa Trough. This perhaps results from a lack of sufficient larval supply from the Izu-Bonin-Mariana Arc vents, and there may not be a reproductive population in the Okinawa Trough.

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Organic complexation of copper in deep-sea hydrothermal vent systems

Environmental Chemistry ◽

10.1071/en06086 ◽

2007 ◽

Vol 4 (2) ◽

pp. 81 ◽

Cited By ~ 46

Author(s):

Sylvia G. Sander ◽

Andrea Koschinsky ◽

Gary Massoth ◽

Matthew Stott ◽

Keith A. Hunter

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Natural Habitat ◽

Hydrothermal Systems ◽

Conditional Stability ◽

Copper Binding ◽

Medium Temperature ◽

Ambient Seawater ◽

Organic Complexation

Environmental context. Deep-sea hydrothermal vents represent a natural habitat for many extremophile organisms able to cope with extreme physical and chemical conditions, including high loads of heavy metals and reduced gases. To date, no information is available on the level and role of organic complexation of metals in these systems, which will have consequences on the bioavailability and precipitation or mineralisation of metals. In this work, we give evidence for the presence of organic molecules, including thiols, capable of forming complexes with copper strong enough to compete against sulfide present at high levels in hydrothermal systems. Abstract. Here we report, for the first time, that strong organic complexation plays an important role in the chemical speciation of copper in hydrothermal vent systems including medium temperature outlets, diffuse vents with an adjacent hydrothermal biocommunity, and local mixing zone with seawater. Samples from three deep-sea hydrothermal vent areas show a wide concentration range of organic copper-binding ligands, up to 4000 nM, with very high conditional stability constants (log K′Cu′L = 12.48 to 13.46). Measurements were usually made using voltammetric methods after removal of sulfide species under ambient seawater conditions (pH 7.8), but binding still occurs at pH 4.5 and 2.1. The voltammetric behaviour of our hydrothermal samples is compared with that of glutathione (GSH) a known strong Cu-binding ligand, as a representative of an organic thiol. Our results provide compelling evidence for the presence of organic ligands, including thiols, which form complexes strong enough to play an important role in controlling the bioavailability and geochemical behaviour of metal ions around hydrothermal vents.

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Draft Genome Sequence of Exiguobacterium sp. HVEsp1, a Thermophilic Bacterium Isolated from a Deep-Sea Hydrothermal Vent in the Okinawa Trough

Genome Announcements ◽

10.1128/genomea.00253-17 ◽

2017 ◽

Vol 5 (17) ◽

Cited By ~ 1

Author(s):

Chen Chen ◽

Li Sun

Keyword(s):

Genome Sequence ◽

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Sequence Data ◽

Okinawa Trough ◽

Draft Genome ◽

Thermophilic Bacterium ◽

Draft Genome Sequence ◽

The Okinawa Trough

ABSTRACT We report here the draft genome sequence of Exiguobacterium sp. HVEsp1, a thermophilic bacterium isolated from a deep-sea hydrothermal vent. The estimated genome size of this strain is 2,838,499 bp with a G+C content of 48.2%. The genome sequence data provide valuable information that will facilitate studies on the adaptation mechanisms of bacteria living in deep-sea hydrothermal vents.

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