Shallow-water Hydrothermal Vent Research Articles

Microbiome flexibility enhances the resilience of the potentially invasive coral Tubastraea aurea to abrupt environmental changes: Insights from a shallow water hydrothermal vent transplantation study

To comprehend the effects of potentially invasive coral Tubastraea aurea on marine ecosystems, it is crucial to understand their adaptive strategies to survive environmental changes and perturbations. Therefore, a cross-transplantation study was conducted to assess the microbiome's role in the resilience of T. aurea to sudden environmental changes.Hydrographic analyses revealed distinct ecological conditions at two sites: a hydrothermal vent (HV) site, characterized by harsh environmental conditions serving as a natural laboratory for future oceanic changes, and a regular coastal site Fulong (FU). Both sites showed significant differences in pH, temperature, and dissolved oxygen. Using Oxford Nanopore Technologies, we examined bacterial dynamics in coral tissue, mucus and ambient sediment samples following cross-transplantation experiments. We observed a rapid shift in dominant bacterial groups post-transplantation with transplanted corals acquiring microbiomes similar to native corals from their respective sites within 16 days. The bacteria Endozoicomonas euniceicola and Ruegeria profundi were dominant in both native and transplanted corals, suggesting their critical role in coral resilience. Furthermore, the enrichment of certain bacterial taxa post-transplantation suggests that opportunistic species also contribute to host acclimatization. Functional profiling data indicated that there was site-specific adaptation because corals had acquired beneficial bacterial assemblages to assist them cope with environmental stressors. More specifically, there was a switch towards sulfur and nitrogen metabolism in corals that moved to high sulfidic environments, while corals transplanted into normal coastal environments showed enriched photoautotrophic processes due to their symbionts. Our study underscored the highly flexible microbiome of T. aurea and its pivotal role in facilitating host resilience to environmental perturbations, particularly in the context of its potential invasiveness. Hence, these findings contribute to the understanding of coral-microbiome dynamics and emphasize the necessity of considering microbially-mediated resilience in managing potentially invasive coral species in marine ecosystems around the world, especially as ocean conditions continue to change.

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.

Mimicking Marine Conditions to Improve Prodigiosin Yields in Bioreactor

Prodigiosin is a red bacterial pigment with great potential as a natural dye and drug precursor, while presenting several pharmacological properties, including antimicrobial and anticancer activities. Its commercialization for biomedical applications, however, remains scarce. The major limitations are related to the lack of efficient bioprocesses and scaling up from laboratory to production. In the present work, the upstream process for prodigiosin production was developed using a marine Serratia rubidaea isolated from a sample collected near a shallow-water hydrothermal vent. The yield of product per biomass was found to be influenced by the cell concentration in the inoculum. The system was scaled up to 2 L stirred tank reactors with two different vessel geometries. It was shown that the vessel geometry and a cascade control mode for regulating the dissolved oxygen concentration influenced the volumetric oxygen mass transfer coefficient (kLa) and thus prodigiosin production. To improve product yields, strategies to mimic the aeration conditions found at the sampling site were tested. When the inoculum was grown for 5 h at 200 rpm and for 19 h at 25 rpm, which significantly decreased the oxygen available, the cells produced 588.2 mgproduct/gbiomass, corresponding to a production of 1066.2 mg of prodigiosin in 24 h and a productivity of 36.1 mgproduct/(L.h). This is a 3.7-fold increase in prodigiosin yield and a 4.5-fold increase in productivity in relation to when no particular strategy was promoted. Additionally, it was shown that lipid analysis and flow cytometry may be used as reliable at-line analytical tools, allowing the monitoring of cell condition and prodigiosin production during fermentation.

Improving Bioprocess Conditions for the Production of Prodigiosin Using a Marine Serratia rubidaea Strain.

The enormous potential attributed to prodigiosin regarding its applicability as a natural pigment and pharmaceutical agent justifies the development of sound bioprocesses for its production. Using a Serratia rubidaea strain isolated from a shallow-water hydrothermal vent, optimization of the growth medium composition was carried out. After medium development, the bacterium temperature, light and oxygen needs were studied, as was growth inhibition by product concentration. The implemented changes led to a 13-fold increase in prodigiosin production in a shake flask, reaching 19.7 mg/L. The conditions allowing the highest bacterial cell growth and prodigiosin production were also tested with another marine strain: S. marcescens isolated from a tide rock pool was able to produce 15.8 mg/L of prodigiosin. The bioprocess with S. rubidaea was scaled up from 0.1 L shake flasks to 2 L bioreactors using the maintenance of the oxygen mass transfer coefficient (kLa) as the scale-up criterion. The implemented parameters in the bioreactor led to an 8-fold increase in product per biomass yield and to a final concentration of 293.1 mg/L of prodigiosin in 24 h.

Non-rhythmic activity of shallow water hydrothermal vent crab Xenograpsus testudinatus affected by interactions of tides, water temperature and light intensity

Non-rhythmic activity of shallow water hydrothermal vent crab Xenograpsus testudinatus affected by interactions of tides, water temperature and light intensity

Isolation and Characterization of a Serratia rubidaea from a Shallow Water Hydrothermal Vent.

Microbial life present in the marine environment has to be able to adapt to rapidly changing and often extreme conditions. This makes these organisms a putative source of commercially interesting compounds since adaptation provides different biochemical routes from those found in their terrestrial counterparts. In this work, the goal was the identification of a marine bacterium isolated from a sample taken at a shallow water hydrothermal vent and of its red product. Genomic, lipidomic, and biochemical approaches were used simultaneously, and the bacterium was identified as Serratia rubidaea. A high-throughput screening strategy was used to assess the best physico-chemical conditions permitting both cell growth and production of the red product. The fatty acid composition of the microbial cells was studied to assess adaptation at the lipid level under stressful conditions, whilst several state-of-the-art techniques, such as DSC, FTIR, NMR, and Ultra-High Resolution Qq-Time-of-Flight mass spectrometry, were used to characterize the structure of the pigment. We hypothesize that the pigment, which could be produced by the cells up to 62 °C, is prodigiosin linked to an aliphatic compound that acts as an anchor to keep it close to the cells in the marine environment.

Novel Insights on the Bacterial and Archaeal Diversity of the Panarea Shallow-Water Hydrothermal Vent Field.

Current knowledge of the microbial diversity of shallow-water hydrothermal vents is still limited. Recent evidence suggests that these peculiar and heterogeneous systems might host highly diversified microbial assemblages with novel or poorly characterized lineages. In the present work, we used 16S rRNA gene metabarcoding to provide novel insights into the diversity of the bacterial and archaeal assemblages in seawater and sediments of three shallow-water hydrothermal systems of Panarea Island (Tyrrhenian Sea). The three areas were characterized by hot, cold, or intermediate temperatures and related venting activities. Microbial biodiversity in seawater largely differed from the benthic one, both in α-diversity (i.e., richness of amplicon sequence variants-ASVs) and in prokaryotic assemblage composition. Furthermore, at the class level, the pelagic prokaryotic assemblages were very similar among sites, whereas the benthic microbial assemblages differed markedly, reflecting the distinct features of the hydrothermal activities at the three sites we investigated. Our results show that ongoing high-temperature emissions can influence prokaryotic α-diversity at the seafloor, increasing turnover (β-)diversity, and that the intermediate-temperature-venting spot that experienced a violent gas explosion 20 years ago now displays the highest benthic prokaryotic diversity. Overall, our results suggest that hydrothermal vent dynamics around Panarea Island can contribute to an increase in the local heterogeneity of physical-chemical conditions, especially at the seafloor, in turn boosting the overall microbial (γ-)diversity of this peculiar hydrothermal system.

Mapping the microbial diversity associated with different geochemical regimes in the shallow-water hydrothermal vents of the Aeolian archipelago, Italy.

Shallow-water hydrothermal vents are unique marine environments ubiquitous along the coast of volcanically active regions of the planet. In contrast to their deep-sea counterparts, primary production at shallow-water vents relies on both photoautotrophy and chemoautotrophy. Such processes are supported by a range of geochemical regimes driven by different geological settings. The Aeolian archipelago, located in the southern Tyrrhenian sea, is characterized by intense hydrothermal activity and harbors some of the best sampled shallow-water vents of the Mediterranean Sea. Despite this, the correlation between microbial diversity, geochemical regimes and geological settings of the different volcanic islands of the archipelago is largely unknown. Here, we report the microbial diversity associated with six distinct shallow-water hydrothermal vents of the Aeolian Islands using a combination of 16S rRNA amplicon sequencing along with physicochemical and geochemical measurements. Samples were collected from biofilms, fluids and sediments from shallow vents on the islands of Lipari, Panarea, Salina, and Vulcano. Two new shallow vent locations are described here for the first time. Our results show the presence of diverse microbial communities consistent in their composition with the local geochemical regimes. The shallow water vents of the Aeolian Islands harbor highly diverse microbial community and should be included in future conservation efforts.

Differential feeding habits of the shallow-water hydrothermal vent crab Xenograpsus testudinatus correlate with their resident vent types at a scale of meters

Abstract. The shallow-water hydrothermal vents (SVs) located off Kueishan (KS) Island, Taiwan, are one of the world's most intensively studied vent systems. It has long been known that white vents (WVs) and yellow vents (YVs) differ in the color and composition of the vent plumes. The endemic vent crabs (Xenograpsus testudinatus) are abundant in both vent types, and ovigerous females migrate to the vent periphery with a distance of 100–200 m to release their offspring. However, most research on the vent crabs was associated with WV or unspecified vent areas. To increase our knowledge of the crabs dwelling in other vent types, we compared the feeding habits of the vent crabs living in WV and YV with 2 sampling months. Specifically, we examined the benthic community of WV and YV, the isotopic niche width, and protein expression patterns of the crabs from the two vents at a distance of 100 m and sampled in July and August 2010. The coverage of sessile organisms and low-mobility fauna in WV was more abundant than in YV, based on the survey in August 2010. The δ13C and δ15N values of crabs differed spatially and temporally (multivariate analysis of variance test; p&lt;0.05). The niche width of the vent crabs from YV-August (0.88 ‰2) narrowed substantially compared to the rest, i.e., YV-July (2.94 ‰2), WV-July (2.88 ‰2), and WV-August (3.62 ‰2; p&lt;0.05), respectively. Based on the protein expression patterns, the vent crabs exhibited three groups, i.e., WV-July and YV-July, WV-August, and YV-August, respectively. Our results indicated that the dwelling crabs were associated with their living vent, and within-vent variability was more noticeable in YV compared to WV. We suggested that vent crabs inhabit their resident vent. Even at a scale of meters, trans-vent movement is probably rare as an adaptation to minimize predation risk.

Microbial dynamics in shallow CO2 seeps system off Panarea Island (Italy)

Shallow-water hydrothermal vents are extreme environments characterized by high temperatures, low pH, and high CO2 concentrations; therefore, they are considered as suitable laboratories for studying the effect of global changes on marine microbes. We hypothesized a direct effect of vents on prokaryotic community structure and functioning in the Panarea Island’s hydrothermal system. Sampling was conducted along a 9-station transect characterized by three active emission points. The water column was stratified with a thermocline at 25 m depth and a deep chlorophyll maximum between 50 and 100 m. Prokaryotic abundance ranged from 0.2 to 1.5 × 109 cells L−1, prokaryotic carbon production from 2.4 to 75.4 ng C L−1 h−1, and exoenzymatic activities degrading proteins, phosphorylated compounds, and polysaccharides were on the order of 4–28, 2–31 and 0.2–4.16 nM h−1, respectively. While microbial abundance and production were shaped by the water column's physical structure, alkaline phosphatase and beta-glucosidase activities seemed to be enhanced by hydrothermal fluids. The 16S rRNA gene amplicon sequencing analysis identified a surface, a deep, and a vent-influenced microbial community. In terms of relative abundance members of the SAR11 group dominated the water column, alongside Synechococcus and Prochlorococcus in surface and bottom samples, respectively. Vent-influenced stations were characterized by the presence of Thiomicrorhabdus, a sulfur-oxidizer chemolithoautotroph. Overall, this study provides insights on the coupling between microbial community structure and the biogeochemical cycling of nutrients in low-pH conditions (CO2 and H2S-based), thus addressing some of the opened questions about the response of microbes to acidification.

Cellular mechanisms underlying extraordinary sulfide tolerance in a crustacean holobiont from hydrothermal vents.

The shallow-water hydrothermal vent system of Kueishan Island has been described as one of the world's most acidic and sulfide-rich marine habitats. The only recorded metazoan species living in the direct vicinity of the vents is Xenograpsus testudinatus, a brachyuran crab endemic to marine sulfide-rich vent systems. Despite the toxicity of hydrogen sulfide, X. testudinatus occupies an ecological niche in a sulfide-rich habitat, with the underlying detoxification mechanism remaining unknown. Using laboratory and field-based experiments, we characterized the gills of X. testudinatus that are the major site of sulfide detoxification. Here sulfide is oxidized to thiosulfate or bound to hypotaurine to generate the less toxic thiotaurine. Biochemical and molecular analyses demonstrated that the accumulation of thiosulfate and hypotaurine is mediated by the sodium-independent sulfate anion transporter (SLC26A11) and taurine transporter (Taut), which are expressed in gill epithelia. Histological and metagenomic analyses of gill tissues demonstrated a distinct bacterial signature dominated by Epsilonproteobacteria. Our results suggest that thiotaurine synthesized in gills is used by sulfide-oxidizing endo-symbiotic bacteria, creating an effective sulfide-buffering system. This work identified physiological mechanisms involving host-microbe interactions that support life of a metazoan in one of the most extreme environments on our planet.

Metagenomic insights into the functions of microbial communities in sulfur-rich sediment of a shallow-water hydrothermal vent off Kueishan Island.

Hydrothermal vent (HTV) systems are important habitats for understanding the biological processes of extremophiles on Earth and their relative contributions to material and energy cycles in the ocean. Current understanding on hydrothermal systems have been primarily focused on deep-sea HTVs, and little is known about the functions and metabolisms of microorganisms in shallow-water HTVs (SW-HTVs), which are distinguished from deep-sea HTVs by a depth limit of 200 m. In this study, we analyzed metagenomes of sulfur-rich sediment samples collected from a SW-HTV of Kueishan Island, located in a marginal sea of the western Pacific Ocean. Comparing with a previously published report of pelagic samples from the nearby sampling site, microbial communities in the SW-HTV sediments enriching with genes of both aerobic and anaerobic respiration inferred variable environments in the tested sediments. Abundant genes of energy metabolism encoding sulfur oxidation, H2 oxidation, and carbon fixation were detected from the sediment samples. Sixty-eight metagenome-assembled-genomes (MAGs) were reconstructed to further understand the metabolism and potential interactions between different microbial taxa in the SW-HTVs sediment. MAGs with the highest abundant were chemolithotrophic sulfur-oxidization bacteria, including Sulfurovum represented Campylobacteria involved sox multienzyme, sulfide oxidation genes and rTCA cycle, and Gammaproteobacteria involved dsr gene and CBB cycle. In addition, Desulfobacterota with the potential to participate in sulfur-disproportionating processes also had higher abundance than the sample's overall mean value. The interaction of these bacterial groups allows the microbial communities to efficiently metabolize a large variety of sulfur compounds. In addition, the potential to use simple organic carbon, such as acetate, was found in chemolithotrophic Campylobacterial MAGs. Collectively, our results revealed the complexity of environmental conditions of the vent sediment and highlight the interactive relationships of the dominant microbial populations in driving sulfur cycles in the SW-HTV sediments off Kueishan Island.

Shallow-water hydrothermal vent system as an extreme proxy for discovery of microbiome significance in a crustacean holobiont

The shallow-water hydrothermal vent (HV) system off Kueishan Island lies at the end of the Okinawa Trough to the northeast of Taiwan. Near its submarine vent openings, aperiodic vent discharges generate a dynamic acidic (pH 5.5-8.1) and sulfidic (9-3000 μM) ecosystem. The dominant metazoan in this unique environment is the brachyuran vent crab, Xenograpsus testudinatus, which has developed robust metabolic strategies and highly adaptive acid-base regulatory mechanisms to maintain its physiological homeostasis. X. testudinatus is considered a holobiont, but the symbiotic mechanisms underlying acid and sulfur tolerance in the host-microbe system remain largely unclear. In this study, we used LoopSeq long-read sequencing of the full-length 16S rRNA gene to identify the bacterial communities present in the gills and carapace surface of X. testudinatus. The alpha diversity analysis, Venn diagram, and principal coordinate analysis (PCoA) indicated that the gills and carapace surface exhibit different bacterial constituents. Further measurements of relative abundance, coupled with functional predictions and fluorescence in situ hybridization (FISH), revealed a predominance of Sulfurovum sp. NBC37-1, a key bacterium that can perform sulfur and hydrogen oxidation to support denitrification processes. Consequently, our findings suggest that the symbiotic bacteria may play a critical role in conferring the extraordinary acid and sulfur tolerances of X. testudinatus, allowing the crustacean holobiont to thrive in its ecological niche within one of the most extreme marine habitats on Earth.

Fluid flow stimulates chemoautotrophy in hydrothermally influenced coastal sediments

Hydrothermalism in coastal sediments strongly impacts biogeochemical processes and supports chemoautotrophy. Yet, the effect of fluid flow on microbial community composition and rates of chemoautotrophic production is unknown because rate measurements under natural conditions are difficult, impeding an assessment of the importance of these systems. Here, in situ incubations controlling fluid flow along a transect of three geochemically distinct locations at a shallow-water hydrothermal system off Milos (Greece) show that Campylobacteria dominated chemoautotrophy in the presence of fluid flow. Based on injected 13C-labelled dissolved inorganic carbon and its incorporation into fatty acids, we constrained carbon fixation to be as high as 12 µmol C cm−3 d−1, corresponding to areal rates up to 10-times higher than previously reported for coastal sediments, and showed the importance of fluid flow for supplying the necessary substrates to support chemoautotrophy. Without flow, rates were substantially lower and microbial community composition markedly shifted. Our results highlight the importance of fluid flow in shaping the composition and activity of microbial communities of shallow-water hydrothermal vents, identifying them as hotspots of microbial productivity.

Autochthony and isotopic niches of benthic fauna at shallow-water hydrothermal vents

The food webs of shallow-water hydrothermal vents are supported by chemosynthetic and photosynthetic autotrophs. However, the relative importance of these two basal resources for benthic consumers and its changes along the physicochemical gradient caused by vent plumes are unknown. We used stable carbon and nitrogen isotopes (i.e., δ13C and δ15N) and Bayesian mixing models to quantify the dietary contribution of basal resources to the benthic fauna at the shallow-water vents around Kueishan Island, Taiwan. Our results indicated that the food chains and consumer production at the shallow-water vents were mainly driven by photoautotrophs (total algal contribution: 26–54%) and zooplankton (19–34%) rather than by chemosynthetic production (total contribution: 14–26%). Intraspecific differences in the trophic support and isotopic niche of the benthic consumers along the physicochemical gradient were also evident. For instance, sea anemone Anthopleura sp. exhibited the greatest reliance on chemosynthetic bacteria (26%) and photoautotrophs (66%) near the vent openings, but zooplankton was its main diet in regions 150–300 m (32–49%) and 300–700 m (32–78%) away from the vent mouths. The vent-induced physicochemical gradient structures not only the community but also the trophic support and isotopic niche of vent consumers.

Does the Kuroshio Current transport planktonic larvae of the hydrothermal-vent crabXenograpsusTakeda &amp; Kurata, 1977 (Decapoda: Brachyura: Grapsoidea)?

AbstractThe grapsoid crab XenograpsusTakeda &amp; Kurata, 1977 inhabiting shallow-water hydrothermal vents shows a limited distribution in the western Pacific, thus providing a good opportunity to observe how a species expands its distribution and establishes and maintains a metapopulation. We analyzed four Japanese populations of Xenograpsus (Kueishan-dao, Showa Iwo-jima, Shikine-jima, and Omuro-dashi) distributed along the Kuroshio Current to assess whether population connectivity is affected by the current. The reconstructed phylogenetic tree indicated that the specimens analyzed belong to a single clade, including X. testudinatusNg, Huang &amp; Ho, 2000 in Kueishan-dao. We could not include genetic data of X. novaeinsularisTakeda &amp; Kurata, 1977 and tentatively refer to the specimens analyzed as X. testudinatus. All four populations shared the two major haplotypes. Statistically significant population differentiation was nevertheless recognized between Showa Iwo-jima and Omuro-dashi, about 1,000 km apart. The number of individuals analyzed in Shikine-jima (N = 11) and Kueishan-dao (N = 5) might not be enough to detect differences. The relative age of population expansion seemed to correlate with the direction of the Kuroshio Countercurrent. Together with knowledge on the distribution of the planktonic larvae, larvae of X. testudinatus stay and mostly contribute to its source population. The Kuroshio Current system occasionally transports the larvae and juveniles, or even adult individuals on floating pumice and other materials, to eventually settle into newly formed habitats after volcanic eruptions, thus expanding the distributional range of the species.

Microbial Biofilms Along a Geochemical Gradient at the Shallow-Water Hydrothermal System of Vulcano Island, Mediterranean Sea.

Shallow water hydrothermal vents represent highly dynamic environments where strong geochemical gradients can shape microbial communities. Recently, these systems are being widely used for investigating the effects of ocean acidification on biota as vent emissions can release high CO2 concentrations causing local pH reduction. However, other gas species, as well as trace elements and metals, are often released in association with CO2 and can potentially act as confounding factors. In this study, we evaluated the composition, diversity and inferred functional profiles of microbial biofilms in Levante Bay (Vulcano Island, Italy, Mediterranean Sea), a well-studied shallow-water hydrothermal vent system. We analyzed 16S rRNA transcripts from biofilms exposed to different intensity of hydrothermal activity, following a redox and pH gradient across the bay. We found that elevated CO2 concentrations causing low pH can affect the response of bacterial groups and taxa by either increasing or decreasing their relative abundance. H2S proved to be a highly selective factor shaping the composition and affecting the diversity of the community by selecting for sulfide-dependent, chemolithoautotrophic bacteria. The analysis of the 16S rRNA transcripts, along with the inferred functional profile of the communities, revealed a strong influence of H2S in the southern portion of the study area, and temporal succession affected the inferred abundance of genes for key metabolic pathways. Our results revealed that the composition of the microbial assemblages vary at very small spatial scales, mirroring the highly variable geochemical signature of vent emissions and cautioning for the use of these environments as models to investigate the effects of ocean acidification on microbial diversity.

Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas.

Environmental contamination by heavy metals (HMs) poses several indirect risks to human health, including the co-spreading of genetic traits conferring resistance to both HMs and antibiotics among micro-organisms. Microbial antibiotic resistance (AR) acquisition is enhanced at sites anthropogenically polluted by HMs, as well as in remote systems naturally enriched in HMs, such as hydrothermal vents in the deep sea. However, to date, the possible role of hydrothermal vents at shallower water depths as hot spots of microbial AR gain and spreading has not been tested, despite the higher potential risks associated with the closer vicinity of such ecosystems to coasts and human activities. In this work, we collected waters and sediments at the Panarea shallow-water hydrothermal vents, testing the presence of culturable marine bacteria and their sensitivity to antibiotics and HMs. All of the bacterial isolates showed resistance to at least one antibiotic and one HM and, most notably, 80% of them displayed multi-AR on average to 12 (min 8, max 15) different antibiotics, as well as multi-HM tolerance. We show that our isolates displayed high similarity (≥99%) to common marine bacteria, affiliating with Actinobacteria, Gammaproteobacteria, Alphaproteobacteria and Firmicutes, and all displayed wide growth ranges for temperature and salinity during in vitro physiological tests. Notably, the analysis of the genomes available in public databases for their closest relatives highlighted the lack of genes for AR, posing new questions on the origin of multi-AR acquisition in this peculiar HM-rich environment. Overall, our results point out that shallow-water hydrothermal vents may contribute to enhance AR acquisition and spreading among common marine bacteria in coastal areas, highlighting this as a focus for future research.

Transformation, Fluxes and Impacts of Dissolved Metals from Shallow Water Hydrothermal Vents on Nearby Ecosystem Offshore of Kueishantao (NE Taiwan)

Hydrothermal vents are one of the important sources of major or trace elements in the ocean. The elemental fluxes, however, may be dynamic due to coastal processes and hydrothermal plumes, especially in shallow-water hydrothermal vents. We collected water samples by using the trace-metal clean technique inside and outside two shallow-water hydrothermal vents (white vent: low temperature, high pH; and yellow vent: high temperature, low pH) off Kueishantao Islet, Taiwan, China via SCUBA divers. We analyzed these samples for their hydro-chemical parameters and dissolved elements (Fe, Mn, Mg, V, Cu, and Mo) thereafter. Our results show that dissolved metals’ concentrations were significantly different between the two vents, with higher Mn and Fe in the White Vent than in the Yellow Vent, likely due to the decreased affinity of the dissolved metals for particles in the white vent. We estimated the plume fluxes of dissolved metals from the hydrothermal mouth by multiplying in situ hydrothermal discharge flowrates with metals’ concentrations inside the vents, which were: 1.09~7.02 × 104 kg Mg, 0.10~1.23 kg Fe, 0.08~28 kg Mn, 33.4~306 g V, 2.89~77.7 g Cu, and 54.3~664 g Mo, annually. The results further indicate that such plumes probably have impacted nearby seawater due to coastal currents and particle desorption during transport. Furthermore, the concentrations of biogenic elements could be further modified in seawater, and potentially impact nearby ecosystems on a larger scale. Our study provides information with which to further understand metal redeployment in submarine shallow nearby ecosystems.

Microbiome of a Reef-Building Coral Displays Signs of Acclimation to a Stressful Shallow Hydrothermal Vent Habitat

Most tropical reef corals live at temperatures near 27°C and pH values near 8. Conditions outside of these can stress corals and lead to bleaching, disease, and death. However, some corals can survive in marginal or extreme habitats outside of these ranges. To date there is a paucity of knowledge about the role that associated microbes may play in the acclimation of corals to such extreme habitats. Here, we explore differences in the compositional and functional profile of the microbiomes of the scleractinian coral Porites panamensis living both on and off potentially stressful shallow-water hydrothermal vents. The environment near the vents is extreme, with temperatures exceeding 80°C and pH values below 6. Coral microbiomes under stress often exhibit increased diversity, increased abundance of pathogenic bacteria, and functional profiles that shift toward pathways associated with pathogenic taxa. Samples from along a transect that crossed an arc of hydrothermal vents were sequenced for the 16S rRNA gene (V4 region). On-vent coral microbiomes were distinct from those of off-vent corals, but did not have increased alpha or beta diversity. On-vent samples had a higher relative abundance of the beneficial endosymbiont, Endozoicomonas. On- and off-vent microbiomes did not differ in overall abundance of the endolithic green alga Ostreobium, however, a single ASV, close to O. quekettii was more abundant in on-vent corals. Ostreobium can provide many of the same benefits to corals as zooxanthellae and their symbiosis is better maintained under thermal stress. Surprisingly, on-vent coral microbiomes had fewer microbial taxa that are known to be pathogenic or associated with stress than did off-vent corals. The predicted functional profiles of on-vent microbiomes revealed enrichment of pathways related to aerobic respiration, fermentation and amino acid biosynthesis, but not of virulence-related pathways. Our results suggest that P. panamensis microbiomes have acclimated to the extreme environment of the hydrothermal vent habitat rather than showing signs of stress. These results exemplify the need to focus efforts on examining the mechanisms of resilience, including symbioses with microbiota, in corals living in extreme environments in an effort to design better management strategies for reef-building corals under thermal and pH stress.