Vent Ecosystems Research Articles

Characteristics of Microbial Diversity and Metabolic Versatility in Dynamic Mid-Okinawa Trough Subsurface Sediments

Large-scale and multi-sample datasets have revealed that microbial diversity and geographic distribution patterns are distinct across various habitats, particularly between hydrothermal vent and cold seep ecosystems. To date, our understanding of the effects of spatial and geochemical gradients on marine microbial communities remains limited. Here, we report the microbial diversity and metabolic versatility of a remote seafloor sediment ecosystem at different sites (GC-2, -4, -5, -6, -8) in the Mid-Okinawa Trough (Mid-OT) using high-throughput metagenomic sequencing technology. Desulfobacteraceae (3.1%) were detected in a high abundance at GC-2 with intense methane concentrations (353 μL/L), which showed a clear correlation with cold seeping. Whereas Candidatus Brocadiaceae (1.7%), Rhodobacteraceae (0.9%), and Rhodospirillaceae (0.7%), which are commonly involved in denitrification and sulfur oxidation, were enriched at GC-8. Concurrently investigating the potential of deep-sea microbial metabolism, we gained insights into the adaptive capabilities and metabolic mechanisms of microorganisms within seafloor environments. Utilizing the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, the analysis of functional modules revealed a significant enrichment (71–74%) of genes associated with metabolic pathways. These results expand our knowledge of the relationship between microbial biodiversity and metabolic versatility in deep-sea extreme environments.

Novel isolates of hydrogen-oxidizing chemolithoautotrophic Sulfurospirillum provide insight to the functions and adaptation mechanisms of Campylobacteria in shallow-water hydrothermal vents.

Enhancing the availability of representative isolates from hydrothermal vents (HTVs) is imperative for comprehending the microbial processes that propel the vent ecosystem. In recent years, Campylobacteria have emerged as the predominant and ubiquitous taxon across both shallow and deep-sea vent systems. Nevertheless, only a few isolates have been cultured, primarily originating from deep-sea HTVs. Presently, no cultivable isolates of Campylobacteria are accessible in shallow water vent systems (<200 m), which exhibit markedly distinct environmental conditions from their deep-sea counterparts. In this study, we enriched a novel isolate (genus Sulfurospirillum, Campylobacteria) from shallow-water HTVs of Kueishan Island. Genomic and physiological analysis revealed that this novel Campylobacteria species grows on a variety of substrate and carbon/energy sources. The pan-genome and phenotypic comparisons with 12 previously isolated Sulfurospirillum species from different environments supported the identification of functional features in Sulfurospirillum genomes crucial for adaptation to vent environments, such as sulfur oxidation, carbon fixation, biofilm formation, and benzoate/toluene degradation, as well as diverse genes related with signal transportation. To conclude, the metabolic characteristics of this novel Campylobacteria augment our understanding of Campylobacteria spanning from deep-sea to shallow-water vent systems.IMPORTANCECampylobacteria emerge as the dominant and ubiquitous taxa within vent systems, playing important roles in the vent ecosystems. However, isolated representatives of Campylobacteria have been mainly from the deep-sea hydrothermal fields, leaving a significant knowledge gap regarding the functions, activities, and adaptation strategies of the vent microorganisms in shallow-water hydrothermal vents (HTVs). This study bridges this gap by providing insights into the phenomics and genomic diversity of genus Sulfurospirillum (order Campylobacterales, class Campylobacteria) based on data derived from a novel isolate obtained from shallow-water HTVs. Our mesophilic isolate of Sulfurospirillum not only augments the genus diversity of Campylobacteria pure cultures derived from vent systems but also serves as the inaugural reference isolate for Campylobacteria in shallow-water environments.

Significant correlations between heavy metals and prokaryotes in the Okinawa Trough hydrothermal sediments

Prokaryotes play crucial roles in hydrothermal vent ecosystems, yet their interactions with heavy metals are not well understood. This study explored the diversity of prokaryotic communities and their correlations with heavy metals and nutrient elements in hydrothermal sediments from Okinawa Trough. A total of 117 bacterial genera in 26 bacterial phyla and 10 archaeal classes in 3 archaeal phyla were identified, including dominant prokaryotic phyla Planctomycetes, Acidobacteria, Verrucomicrobia, and Euryarchaeota. Furthermore, Fe (39.61 mg/g), Mn (2.84 mg/g) and Ba (0.36 mg/g) were found to be the most abundant heavy metals in the Okinawa hydrothermal sediments. Notably, the concentrations of Zn, Ba, Mn, total organic carbon, and total nitrogen significantly increased, whereas the total sulfur concentration distinctively decreased at sampling sites farther from hydrothermal vents. These changes corresponded with reductions in prokaryotic abundance and diversity. Most heavy metals, including Mn, Fe, Co, Cu and As, presented significant positive correlations with a number of prokaryotic genera in the nearby sediment samples. In contrast, both positive and negative correlations with prokaryotes were observed in remote sediment. The keystone taxa include Magnetospirillum, GOUTA19, Lysobacter, Kaistobacter, Treponema, and Clostridium were detected through prokaryote interspecies interactions. The functional predictions revealed significant genes involved in carbon fixation, nitrogen/sulfur cycling, heat shock protein, and metal resistance pathways. Structural equation modeling confirmed that metal and nutrient elements directly influence the composition of prokaryotic communities, which in turn affects the relative abundance of functional genes.

Ocean circulation contributes to genetic connectivity of limpet populations at deep-sea hydrothermal vents in a back-arc basin.

For endemic benthos inhabiting hydrothermal vent fields, larval recruitment is critical for population maintenance and colonization via migration among separated sites. The vent-endemic limpet, Lepetodrilus nux, is abundant at deep-sea hydrothermal vents in the Okinawa Trough, a back-arc basin in the northwestern Pacific; nonetheless, it is endangered due to deep-sea mining. This species is associated with many other vent species and is an important successor in these vent ecosystems. However, limpet genetic diversity and connectivity among local populations have not yet been examined. We conducted a population genetics study of L. nux at five hydrothermal vent fields (maximum geographic distance, ~545 km; depths ~700 m to ~1650 m) using 14 polymorphic microsatellite loci previously developed. Genetic diversity has been maintained among these populations. Meanwhile, fine population genetic structure was detected between distant populations, even within this back-arc basin, reflecting geographic distances between vent fields. There was a significant, positive correlation between genetic differentiation and geographic distance, but no correlation with depth. Contrary to dispersal patterns predicted by an ocean circulation model, genetic migration is not necessarily unidirectional, based on relative migration rates. While ocean circulation contributes to dispersal of L. nux among vent fields in the Okinawa Trough, genetic connectivity may be maintained by complex, bidirectional dispersal processes over multiple generations.

Faunal colonists, including mussel settlers, respond to microbial biofilms at deep-sea hydrothermal vents

Colonization processes at dynamic deep-sea hydrothermal vent ecosystems ultimately determine ecosystem structure, function, resilience, and recovery. Microbial biofilms form rapidly on surfaces near hydrothermal vents and are continuously exposed to the highly variable abiotic environment. Thus, biofilm microbes may provide a temporally integrated signal that can indicate whether the habitat is suitable for faunal colonists. This study explored the role of microbial biofilms in controlling faunal colonization through in-situ colonization experiments at Tica Vent in the 9°50’ N region of the East Pacific Rise (EPR). Short-term experiments (∼2 weeks) were conducted by deploying colonization surfaces (“sandwiches”) either with an established biofilm (developed for >1 year) or a fresh biofilm (developed throughout experiment) in zones characterized by different faunal assemblages. Differences in associated larval settlers, faunal immigrants, and microbial communities according to biofilm age across multiple biogenic zones were investigated. Faunal and microbial community compositions significantly differed according to whether the sandwiches had established or fresh biofilms as well as the biogenic zone they were deployed in. Several faunal colonists, including settlers such as the foundational chemosymbiotic mussel Bathymodiolus thermophilus and the nectochaete Archinome sp., were found associated more with established biofilms than fresh biofilms. Microbial biofilm communities were dominated by putative chemoautotrophic members of the Campylobacterota phylum and Gammaproteobacteria class and several microbial taxa were found to covary with faunal colonists. Overall, these findings show that microbial community composition plays a role in larval settlement and animal migration in hydrothermal vent systems and the detection of microbial and faunal interactions provides a starting point for identifying key microbial characteristics influencing colonization processes at hydrothermal vents.

Diversities and interactions of phages and bacteria in deep-sea sediments as revealed by metagenomics.

Phages are found virtually everywhere, even in extreme environments, and are extremely diverse both in their virion structures and in their genomic content. They are thought to shape the taxonomic and functional composition of microbial communities as well as their stability. A number of studies on laboratory culture and viral metagenomic research provide deeper insights into the abundance, diversity, distribution, and interaction with hosts of phages across a wide range of ecosystems. Although most of these studies focus on easily accessible samples, such as soils, lakes, and shallow oceans, little is known about bathypelagic phages. In this study, through analyzing the 16S rRNA sequencing and viral metagenomic sequencing data of 25 samples collected from five different bathypelagic ecosystems, we detected a high diversity of bacteria and phages, particularly in the cold seep and hydrothermal vent ecosystems, which have stable chemical energy. The relative abundance of phages in these ecosystems was higher than in other three abyssal ecosystems. The low phage/host ratios obtained from host prediction were different from shallow ecosystems and indicated the prevalence of prophages, suggesting the complexity of phage-bacteria interactions in abyssal ecosystems. In the correlation analysis, we revealed several phages-bacteria interaction networks of potential ecological relevance. Our study contributes to a better understanding of the interactions between bathypelagic bacteria and their phages.

Trophic diversity of chemosymbiont hosts in deep-sea hydrothermal vents using amino acid nitrogen isotopes

Chemosymbiotic species inhabiting deep-sea hydrothermal vents are known to rely on microbial symbionts for nutrition. However, the relative contributions of heterotrophic energy sources to their diets remain poorly understood. In this study, we investigate the trophic positions (TP) of symbiont-bearing taxa, including vent mussels, snails, and shrimps, and examine the contribution of copepods and detrital organic matter (OM) to the food chain. Amino acid nitrogen isotopic compositions (δ15NAA) were used to investigate the TP of vent mussels (Bathymodiolus septemdierum and Gigantidas vrijenhoeki), snails (Alviniconcha spp.), and shrimps (Alvinocaris sp. and Rimicaris kairei) from two different vent environments. δ15NAA values in copepods and OM were also measured. Microbial resynthesis index (ΣV) was calculated to predict the contribution of reworked OM as an energy source to the hydrothermal vent ecosystem. Variations in TP were observed among vent mussels and snails from different vent environments, with higher TP in species from diffusing vents than in those from black smoker vents. Shrimps dwelling in a single diffusing vent exhibited distinct TP, suggesting that microhabitat and phylogeny may influence their energy acquisition. Notably, copepods occupied higher TPs than expected, possibly owing to the consumption of detrital OM. Our findings provide new insights into the trophic diversity of chemosymbiotic species in deep-sea hydrothermal vents and demonstrate the utility of δ15NAA analysis as a tool for unraveling food web dynamics and ecosystem functioning in these unique environments.

Hydrothermal vent fauna of the western Pacific Ocean: Distribution patterns and biogeographic networks

AbstractAimDeep‐sea hydrothermal vent habitats support a low‐diversity fauna in which most species are unique to the ecosystem. To inform conservation planning around this vulnerable marine ecosystem, we examine species distributions over a wide area to assess the underlying beta‐diversity components and to examine biogeographic patterns. We assess the concept of a highly connected fauna that would repopulate areas of local extinction from distal locations.LocationWestern Pacific Ocean from Japan to New Zealand.MethodsWe assemble a database of 295 confirmed species records for 11 western Pacific vent systems. The SET beta‐diversity framework supports query of the distribution of pairwise pattern components in comparisons among vent systems. We build a network based in graph theory to examine connectivity among vent systems based on shared species similarity. A bipartite network revealed the relative role of each species in linkages among vent system nodes. We assess the importance of sampling bias and distance between systems.ResultsOverall, two‐thirds of the taxa are restricted to a single basin or arc. The Mariana Trough system has the highest corrected weighted endemism for vent‐specific species, followed by that of the Okinawa Trough. Species replacement is the dominant feature of beta‐diversity. Eleven vent systems form seven network modules with stronger connectivity in the Southwest than Northwest Pacific. The Manus Basin vent system emerges as a network ‘hub’ reflecting its central geographic near the equator.Main ConclusionTwo western Pacific biogeographic provinces arise, north and south of the equator that few species transcend. Local and regional conservation plans should consider the low network connectivity and high system endemism in management of hydrothermal vent ecosystems in the event of seabed mining. Species recruitment is unlikely to transcend vent system boundaries. We identify Okinawa Trough, Mariana Trough, Manus Basin, Feni‐Tabar Arc and Kermadec Arc for development of conservation plans that initiate or expand protection.

Genetic divergence and migration patterns of a galatheoid squat lobster highlight the need for deep-sea conservation.

Information on genetic divergence and migration patterns of vent- and seep-endemic macrobenthos can help delimit biogeographical provinces and provide scientific guidelines for deep-sea conservation under the growing threats of anthropogenic disturbances. Nevertheless, related studies are still scarce, impeding the informed conservation of these hotspots of deep-sea biodiversity. To bridge this knowledge gap, we conducted a population connectivity study on the galatheoid squat lobster Shinkaia crosnieri - a deep-sea foundation species widely distributed in vent and seep ecosystems in the Northwest Pacific. With the application of an interdisciplinary methodology involving population genomics and oceanographic approaches, we unveiled two semi-isolated lineages of S. crosnieri with limited and asymmetrical gene flow potentially shaped by the geographic settings, habitat types, and ocean currents - one comprising vent populations in the Okinawa Trough, with those inhabiting the southern trough area likely serving as the source; the other being the Jiaolong (JR) seep population in the South China Sea. The latter might have recently experienced a pronounced demographic contraction and exhibited genetic introgression from the Okinawa Trough lineage, potentially mediated by the intrusion of the North Pacific Intermediate Water. We then compared the biogeographic patterns between S. crosnieri and two other representative and co-occurring vent- and seep-endemic species using published data. Based on their biogeographical subdivisions and source-sink dynamics, we highlighted the southern Okinawa Trough vents and the JR seep warrant imperative conservation efforts to sustain the deep-sea biodiversity in the Northwest Pacific.

Symbioses of alvinocaridid shrimps from the South West Pacific: No chemosymbiotic diets but conserved gut microbiomes.

Rimicaris exoculata shrimps from hydrothermal vent ecosystems are known to host dense epibiotic communities inside their enlarged heads and digestive systems. Conversely, other shrimps from the family, described as opportunistic feeders have received less attention. We examined the nutrition and bacterial communities colonising 'head' chambers and digestive systems of three other alvinocaridids-Rimicaris variabilis, Nautilocaris saintlaurentae and Manuscaris sp.-using a combination of electron microscopy, stable isotopes and sequencing approaches. Our observations inside 'head' cavities and on mouthparts showed only a really low coverage of bacterial epibionts. In addition, no clear correlation between isotopic ratios and relative abundance of epibionts on mouthparts could be established among shrimp individuals. Altogether, these results suggest that none of these alvinocaridids rely on chemosynthetic epibionts as their main source of nutrition. Our analyses also revealed a substantial presence of several Firmicutes and Deferribacterota lineages within the foreguts and midguts of these shrimps, which closest known lineages were systematically digestive symbionts associated with alvinocaridids, and more broadly for Firmicutes from digestive systems of other crustaceans from marine and terrestrial ecosystems. Overall, our study opens new perspectives not only about chemosynthetic symbioses of vent shrimps but more largely about digestive microbiomes with potential ancient and evolutionarily conserved bacterial partnerships among crustaceans.

Metagenome-based metabolic modelling predicts unique microbial interactions in deep-sea hydrothermal plume microbiomes

Deep-sea hydrothermal vents are abundant on the ocean floor and play important roles in ocean biogeochemistry. In vent ecosystems such as hydrothermal plumes, microorganisms rely on reduced chemicals and gases in hydrothermal fluids to fuel primary production and form diverse and complex microbial communities. However, microbial interactions that drive these complex microbiomes remain poorly understood. Here, we use microbiomes from the Guaymas Basin hydrothermal system in the Pacific Ocean to shed more light on the key species in these communities and their interactions. We built metabolic models from metagenomically assembled genomes (MAGs) and infer possible metabolic exchanges and horizontal gene transfer (HGT) events within the community. We highlight possible archaea–archaea and archaea–bacteria interactions and their contributions to the robustness of the community. Cellobiose, D-Mannose 1-phosphate, O2, CO2, and H2S were among the most exchanged metabolites. These interactions enhanced the metabolic capabilities of the community by exchange of metabolites that cannot be produced by any other community member. Archaea from the DPANN group stood out as key microbes, benefiting significantly as acceptors in the community. Overall, our study provides key insights into the microbial interactions that drive community structure and organisation in complex hydrothermal plume microbiomes.

Foraging under extreme events: Contrasting adaptations by benthic macrofauna to drastic biogeochemical disturbance

Abstract Hydrothermal vent systems are important biodiversity hotspots that host a vast array of unique species and provide information on life's evolutionary adaptations to extreme environments. However, these habitats are threatened by both human exploitation and extreme natural events, both of which can rapidly disrupt the delicate balance of the food webs found in these systems. This is particularly true for shallow vent endemic animals due to their limited dietary niche and specialized adaptations to specific biogeochemical conditions. In this study, we used the shallow hydrothermal vents of Kueishantao off the coast of Taiwan as a natural laboratory to examine the response of a benthic food web to a M5.8 earthquake and a C5 typhoon that led to a two‐year “near shutdown” of the vents. These perturbations drastically altered the local biogeochemical cycle and the dietary availability of chemosynthetic versus photosynthetic food resources. Our analysis of multiple stable isotopes, including those of sulphur, carbon, and nitrogen (δ34S, δ13C, and δ15N), from different benthic macrofauna reveals that endemic and non‐endemic consumers exhibited different responses to sudden disruption in habitat and biogeochemical cycling. The endemic vent crab, Xenograpsus testudinatus, continued to partially rely on chemosynthetic sulphur bacteria despite photosynthetic sources being the most dominant food source after the disruption. We posit that X. testudinatus has an obligate nutritional dependence on chemoautotrophic sources because the decrease in chemoautotrophic production was accompanied by a dramatic decrease in the abundance of X. testudinatus. The population decline rate was ~19 individuals per m2 per year before the perturbation, but the decline rate increased to 40 individuals per m2 per year after the perturbation. In contrast, the non‐endemic gastropods exhibited much greater dietary plasticity that tracked the overall abundance of photo‐ and chemo‐synthetic dietary sources. The catastrophic events in shallow hydrothermal vent ecosystem presented a novel opportunity to examine dietary adaptations among endemic and non‐endemic benthic macrofauna in response to altered biogeochemical cycling. Our findings highlight the vulnerability of benthic specialists to the growing environmental pressures exerted by human activities worldwide. Read the free Plain Language Summary for this article on the Journal blog.

Active hydrothermal vent ecosystems in the Indian Ocean are in need of protection

Deep-sea hydrothermal vent fields are among the most pristine and remarkable ecosystems on Earth. They are fueled by microbial chemosynthesis, harbor unique life and can be sources of precipitated mineral deposits. As the global demand for mineral resources rises, vent fields have been investigated for polymetallic sulfides (PMS) and biological resources. The International Seabed Authority (ISA) has issued 7 contracts for PMS exploration, including 4 licenses for vent fields in the Indian Ocean. Here, we provide a summary of the available ecological knowledge of Indian vent communities and we assess their vulnerability, sensitivity, ecological and biological significance. We combine and apply scientific criteria for Vulnerable Marine Ecosystems (VMEs) by FAO, Particular Sensitive Sea Areas (PSSAs) by IMO, and Ecologically or Biologically Significant Areas (EBSAs) by CBD. Our scientific assessment shows that all active vent fields in the Indian Ocean appear to meet all scientific criteria for protection, and both the high degree of uniqueness and fragility of these ecosystems stand out.

From basalt to biosphere: Early non-vent community succession on the erupting Vailulu’u deep seamount

Volcanic eruptions provide rare opportunities to witness the biological recolonization of areas covered by new lava flows by effectively resetting the ecological succession clock to zero. The role of submarine volcanic eruptions as disturbance events and the resulting patterns of ecological succession have mainly been studied in hydrothermal vent ecosystems. However, the effects of submarine volcanic eruptions as disturbance forces have rarely been studied in non-vent ecosystems, particularly on seamounts. Here, we document the early stages of ecological succession of non-vent benthic communities inhabiting the summit caldera of the active Vailulu’u submarine volcano in American Samoa. Sitting above the Samoan volcanic hotspot, Vailulu’u is the youngest volcano of the Samoan chain. Repeated mapping of Vailulu’u in 1999, 2005, 2006, 2012, and 2017 revealed the progressive growth of a new cone named Nafanua. In 18 years, the cone grew &amp;gt;300 meters in height from a starting depth of ~1000 meters below sea level (mbsl). The differential analyses of this time-series bathymetry dataset enabled the assignment of maximum age ranges to different portions of the new cone. High-definition ROV imagery collected in 2017 revealed patterns of community structuring consistent with ecological succession: newly erupted seafloor contained a subset of the benthic species found on older seafloor. Furthermore, individual animal sizes in the younger seafloor zones were smaller than in the older zones. This unusual interdisciplinary combination of geological and biological observations provides constraints on which deep-sea animals recolonize new seafloor after a major disturbance event and how quickly. This knowledge could be applied to identify signs and states of recovery from anthropogenic disturbances by a deep seamount ecosystem.

Hydrothermal vent chimney-base sediments as unique habitat for meiobenthos and nanobenthos: Observations on millimeter-scale distributions

Hydrothermal vents are critical to marine geochemical cycling and ecosystem functioning. Although hydrothermal vent-associated megafauna and chemoautotrophic prokaryotes have received extensive dedicated study, smaller hydrothermal vent-associated eukaryotes such as meiofauna and nanobiota have received much less attention. These communities comprise critical links in trophic flow and carbon cycling of other marine habitats, so study of their occurrence and role in hydrothermal vent ecosystems is warranted. Further, an understudied vent habitat is the thin sediment cover at the base of hydrothermal vent chimneys. An initial study revealed that sediments at the base of vent chimneys of the Izu-Ogawasara Arc system (western North Pacific) support metazoan meiofauna, but very little is known about the taxonomic composition and abundance of the meiobenthic protists and nanobiota, or their millimeter-scale distributions. Using the Fluorescently Labeled Embedded Coring method (FLEC), we describe results on meiofaunal and nanobiota higher-level identifications, life positions and relative abundances within sediments from three habitats (base of vent chimneys, inside caldera but away from chimneys, and outside caldera) of the Myojin-Knoll caldera and vicinity. Results suggest that the chimney-base community is unique and more abundant compared to non-chimney associated eukaryotic communities. Supporting evidence (molecular phylogeny, scanning and transmission electron microscopy imaging) documents first known hydrothermal-vent-associated occurrences for two protist taxa. Collectively, results provide valuable insights into a cryptic component of the hydrothermal vent ecosystem.

Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota.

The disproportionation of inorganic sulfur compounds could be widespread in natural habitats, and microorganisms could produce energy to support primary productivity through this catabolism. However, the microorganisms that carry this process out and the catabolic pathways at work remain relatively unstudied. Here, we investigated the bacterial diversity involved in sulfur disproportionation in hydrothermal plumes from Carlsberg Ridge in the northwestern Indian Ocean by enrichment cultures. A bacterial community analysis revealed that bacteria of the genera Sulfurimonas and Sulfurovum, belonging to the phylum Campylobacterota and previously having been characterized as chemolithoautotrophic sulfur oxidizers, were the most dominant members in six enrichment cultures. Subsequent bacterial isolation and physiological studies confirmed that five Sulfurimonas and Sulfurovum isolates could disproportionate thiosulfate and elemental sulfur. The ability to disproportionate sulfur was also demonstrated in several strains of Sulfurimonas and Sulfurovum that were isolated from hydrothermal vents or other natural environments. Dialysis membrane experiments showed that S0 disproportionation did not require the direct contact of cells with bulk sulfur. A comparative genomic analysis showed that Campylobacterota strains did not contain some genes of the Dsr and rDSR pathways (aprAB, dsrAB, dsrC, dsrMKJOP, and qmoABC) that are involved in sulfur disproportionation in some other taxa, suggesting the existence of an unrevealed catabolic pathway for sulfur disproportionation. These findings provide evidence for the catabolic versatility of these Campylobacterota genera, which are widely distributed in chemosynthetic environments, and expand our knowledge of the microbial taxa involved in this reaction of the biogeochemical sulfur cycle in hydrothermal vent environments. IMPORTANCE The phylum Campylobacterota, notably represented by the genera Sulfurimonas and Sulfurovum, is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats. Herein, we show that the mesophilic predominant chemolithoautotrophs of the genera Sulfurimonas and Sulfurovum could grow via sulfur disproportionation to gain energy. This is the first report of the chemolithoautotrophic disproportionation of thiosulfate and elemental sulfur within the genera Sulfurimonas and Sulfurovum, and this comes in addition to their already known role in the chemolithoautotrophic oxidation of sulfur compounds. Sulfur disproportionation via chemolithoautotrophic Campylobacterota may represent a previously unrecognized primary production process in hydrothermal vent ecosystems.

Methane seepage intensity distinguish microbial communities in sediments at the Mid-Okinawa Trough

Shallow methane/sulfate transition zones in cold seeps are hotspots to study microbially mediated geochemical cycles due to high methane fluxes. However, our knowledge about the microbial communities in remote seafloor cold seep ecosystems with different methane seepage intensity is still sparse due to the challenge for sampling and visual observations. In this work, three remotely operated vehicle (ROV) video-guided push sediment cores were sampled from cold seep fields with different methane seepage intensity (low-intensity seepage, R5-C1; moderate-intensity seepage, R6-C2; high-intensity seepage, R6-C3) at the western slope of Mid-Okinawa Trough (Mid-OT) and subjected to high throughput sequencing of 16S rRNA genes for bacteria and archaea. Vesicomyid clams and white microbial mats are visible by video at R6-C3 with methane bubbles. The high relative abundances of anaerobic methanotrophic archaea (ANME-1, -2, and -3), δ-Proteobacteriacea and Campylobacteria in R6-C3 indicated that the processes of anaerobic methane oxidation (AOM), sulfate reduction and sulfur oxidation might occur in this active seeping site. In contrast, Bathyarchaeia, Nitrosopumilales, Sphingomonadales, and Burkholderiales were enriched in bubble-free sites, which commonly involved in the degradation of organic compounds. Principal coordinate analysis showed that both bacterial and archaeal communities were clustered according to sampling sites, also indicating the impact of methane seepage intensity on microbial communities. The co-occurrence network analysis revealed that microbes at the site with high methane fluxes mainly cooperated with each other to sustain the ecosystems, whereas competition enhanced at sites with low methane fluxes. Detection of thermophiles Thermoanaerobaculia and Hydrothermarchaeota may indicate microbial transmission from nearby hydrothermal vents, suggesting potential interactions between cold seepage and hydrothermal vent ecosystems. These results expand our knowledge about the composition and distribution of bacteria and archaea with different methane seepage intensity in cold seep field at the Mid-OT, contributing to the ongoing efforts in understanding carbon cycling in the cold seep ecosystems.

Non-Vent Megafaunal Communities on the Endeavour and Middle Valley Segments of the Juan de Fuca Ridge, Northeast Pacific Ocean

There has been increasing interest in mining polymetallic sulfide deposits at deep-sea inactive hydrothermal vents, leading to the development of regulations to minimize risk to the marine environment. While an extensive body of literature exists on the ecological communities at active vents, fauna at inactive hydrothermal vents and the vent periphery are poorly described and their vulnerability to disturbance is unknown. We examined patterns in abundance of non-vent epibenthic megafauna on two segments of the Juan de Fuca Ridge, Northeast Pacific Ocean. Video footage was collected by the remotely operated vehicle ROPOS during four dives at the Endeavour Segment and two dives at Middle Valley in August 2016. At the Endeavour Segment, the substrate is characterized predominantly by basalt and edifices of hydrothermal sulfide that range in hydrothermal activity from inactive to vigorous, high-temperature venting. In contrast, Middle Valley is heavily sedimented and most hydrothermal activity is low-temperature diffuse flow. While inactive substrates at both sites harboured slow-growing sessile fauna, the dominant members of the community differed between sites. At Endeavour, the most abundant morphotaxa included rossellid vase sponges, alcyonacean corals, and crinoids. Estimated richness and total abundance of morphotaxa was higher on hard substrates than sedimented substrates and highest on inactive chimneys. At Middle Valley, the most abundant morphotaxa included antipatharian corals, anemones, and ascidians. Species richness was higher on inactive chimneys and mixed substrates than sediment. The abundance of some megafauna varied with proximity to active vents. At Endeavour, deep-water corals were nearly absent within 25 m of active chimneys and very few occurred between 26 and 50 m from active chimneys. Rossellid vase sponges were in low abundance within 25 m of active chimneys but were more abundant than corals at 26-50 m from active chimneys. This project contributes baseline data on megafaunal assemblages on inactive hydrothermal vents and can provide the basis for more focused research on the structure and function of inactive vent ecosystems.

Full-Length Transcriptome Comparison Provides Novel Insights into the Molecular Basis of Adaptation to Different Ecological Niches of the Deep-Sea Hydrothermal Vent in Alvinocaridid Shrimps

The deep-sea hydrothermal vent ecosystem is one of the extreme chemoautotrophic environments. Shinkaicaris leurokolos Kikuchi and Hashimoto, 2000, and Alvinocaris longirostris Kikuchi and Ohta, 1995, are typically co-distributed and closely related alvinocaridid shrimps in hydrothermal vent areas with different ecological niches, providing an excellent model for studying the adaptive evolution mechanism of animals in the extreme deep-sea hydrothermal vent environment. The shrimp S. leurokolos lives in close proximity to the chimney vent discharging high-temperature fluid, while A. longirostris inhabits the peripheral areas of hydrothermal vents. In this study, full-length transcriptomes of S. leurokolos and A. longirostris were generated using a combination of single-molecule real-time (SMRT) and Illumina RNA-seq technology. Expression analyses of the transcriptomes showed that among the top 30% of highly expressed genes of each species, more genes related to sulfide and heavy metal metabolism (sulfide: quinone oxidoreductase, SQR; persulfide dioxygenase, ETHE1; thiosulfate sulfurtransferase, TST, and ferritin, FRI) were specifically highly expressed in S. leurokolos, while genes involved in maintaining epibiotic bacteria or pathogen resistance (beta-1,3-glucan-binding protein, BGBP; endochitinase, CHIT; acidic mammalian chitinase, CHIA, and anti-lipopolysaccharide factors, ALPS) were highly expressed in A. longirostris. Gene family expansion analysis revealed that genes related to anti-oxidant metabolism (cytosolic manganese superoxide dismutase, SODM; glutathione S-transferase, GST, and glutathione peroxidase, GPX) and heat stress (heat shock cognate 70 kDa protein, HSP70 and heat shock 70 kDa protein cognate 4, HSP7D) underwent significant expansion in S. leurokolos, while CHIA and CHIT involved in pathogen resistance significantly expanded in A. longirostris. Finally, 66 positively selected genes (PSGs) were identified in the vent shrimp S. leurokolos. Most of the PSGs were involved in DNA repair, antioxidation, immune defense, and heat stress response, suggesting their function in the adaptive evolution of species inhabiting the extreme vent microhabitat. This study provides abundant genetic resources for deep-sea invertebrates, and is expected to lay the foundation for deep decipherment of the adaptive evolution mechanism of shrimps in a deep-sea chemosynthetic ecosystem based on further whole-genome comparison.

A Comprehensive Profile of Antibiotic Resistance Genes in the Water Column of a Shallow-Sea Hydrothermal Vent Ecosystem

Antibiotic resistance genes (ARGs) became an emerging contaminant, and were found to accumulate in natural and man-made environments. A comprehensive understanding of the diversity and abundance of ARGs in pristine environments is critical for defining the baseline levels of environmental ARGs. However, there is limited information available on the ARG profiles of pristine environments, especially for shallow-sea hydrothermal vents ecosystems. Here, we combined 16S rRNA gene full-length amplicon sequencing and high-throughput quantitative PCR (HT-qPCR) to study the bacterial communities, and ARG abundance and diversity in the shallow-sea hydrothermal vent ecosystem of the Kueishantao Islet. The results of the 16S rRNA gene amplicon sequencing showed that several sulfur-cycling related bacterial genera, including Thiomicrorhabdus, Thioreductor, Sulfurovum, Sulfurimonas and Lebetimonas, dominated in the water column of the shallow-sea system. Temperature was the significant factor shaping the bacterial communities. The results of HT-qPCR analysis showed that the Kueishantao shallow-sea system harbored the lowest diversity (average 10 ARG subtypes) and abundance (average 1.0 × 10−3 copy per bacterial cell) of ARGs compared with other pristine (i.e., Tibet lake sediments, marine water and sediments) and anthropogenic-disturbed (i.e., drinking water reservoirs, urban ponds and wastewater treatment plants) environments. Procrustes analysis demonstrated a concordant pattern between the compositions of bacterial communities and ARGs in the shallow-sea system, while variation partition analysis revealed that the shared effects of physicochemical and bacterial communities explained &gt;80% of the variation in the composition of ARGs. These results suggest that the vent bacterial communities and local environmental factors played an important role in shaping the distribution of the ARG profiles. Our study provides the first comprehensive overview of the background level of ARGs in a shallow-sea hydrothermal vent ecosystem.