Genus-Specific Carbon Fixation Activity Measurements Reveal Distinct Responses to Oxygen Among Hydrothermal Vent Campylobacteria

2021 ◽  
Author(s):  
Jesse McNichol ◽  
Stefan Dyksma ◽  
Marc Mußmann ◽  
Jeffrey S. Seewald ◽  
Sean P. Sylva ◽  
...  
Keyword(s):  
Community Composition ◽  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Carbon Fixation ◽  
Sequence Variant ◽  
Experimental Conditions ◽  
Activity Measurements ◽  
Initial Starting

Molecular surveys of low temperature deep-sea hydrothermal vent fluids have shown that Campylobacteria (prev. Epsilonproteobacteria ) often dominate the microbial community and that three genera - Arcobacter , Sulfurimonas and Sulfurovum - frequently coexist. In this study, we used replicated radiocarbon incubations of deep-sea hydrothermal fluids to investigate activity of each genus under three experimental conditions. To quantify genus-specific radiocarbon incorporation, we used newly designed oligonucleotide probes for Arcobacter , Sulfurimonas , and Sulfurovum to quantify their activity using catalyzed-reporter deposition fluorescence in-situ hybridization (CARD-FISH) combined with fluorescence-activated cell sorting. All three genera actively fixed CO 2 in short-term (∼ 20 h) incubations, but responded differently to the additions of nitrate and oxygen. Oxygen additions had the largest effect on community composition, and caused a pronounced shift in community composition at the amplicon sequence variant (ASV) level after only 20 h of incubation. The effect of oxygen on carbon fixation rates appeared to depend on the initial starting community. The presented results support the hypothesis that these chemoautotrophic genera possess functionally redundant core metabolic capabilities, but also reveal finer-scale differences in growth likely reflecting adaptation of physiologically-distinct phylotypes to varying oxygen concentrations in situ . Overall, our study provides new insights into how oxygen controls community composition and total chemoautotrophic activity, and underscores how quickly deep-sea vent microbial communities respond to disturbances. Importance: Sulfidic environments worldwide are often dominated by sulfur-oxidizing, carbon-fixing Campylobacteria . Environmental factors associated with this group's dominance are now understood, but far less is known about the ecology and physiology of members of subgroups of chemoautotrophic Campylobacteria . In this study, we used a novel method to differentiate the genus-specific chemoautotrophic activity of three subtypes of Campylobacteria. In combination with evidence from microscopic counts, chemical consumption/production during incubations, and DNA-based measurements, our data show that oxygen concentration affects both community composition and chemoautotrophic function in situ . These results help us better understand factors controlling microbial diversity at deep-sea hydrothermal vents, and provide first-order insights into the ecophysiological differences between these distinct microbial taxa.

scholarly journals Group-Specific Carbon Fixation Activity Measurements Reveal Distinct Responses to Oxygen Among Hydrothermal vent Campylobacteria

2020 ◽  
Author(s):  
Jesse McNichol ◽  
Stefan Dyksma ◽  
Marc Mußmann ◽  
Jeffrey S. Seewald ◽  
Sean P. Sylva ◽  
...  
Keyword(s):  
Community Composition ◽  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Carbon Fixation ◽  
Genomic Diversity ◽  
Sequence Variant ◽  
Activity Measurements ◽  
Initial Starting

AbstractMolecular surveys of low temperature deep-sea hydrothermal vent fluids have shown that Campylobacteria (prev. Epsilonproteobacteria) often dominate the microbial community and that three subgroups - Arcobacter, Sulfurimonas and Sulfurovum - frequently coexist. In this study, we used replicated radiocarbon incubations of deep-sea hydrothermal fluids to investigate the activities of each group under three distinct incubation conditions. In order to quantify group-specific radiocarbon incorporation, we used newly designed oligonucleotide probes for Arcobacter, Sulfurimonas, and Sulfurovum to quantify their activity using catalyzed-reporter deposition fluorescence in-situ hybridization (CARD-FISH) combined with fluorescence-activated cell sorting. All three groups actively fixed CO2 in short-term (~ 20 h) incubations with either nitrate, oxygen, or no additions (control) at similar per-cell carbon fixation rates. Oxygen additions had the largest effect on community composition and overall cell numbers, and caused a pronounced shift in community composition at the amplicon sequence variant (ASV) level after only 20 h of incubation for all three groups. Interestingly, the effect of oxygen on carbon fixation rates appeared to depend on the initial starting community. Higher carbon fixation rates in oxygen-amended treatments were noted for all three taxa after an unintended disturbance to the sample site that may have selected for more oxygen-tolerant phylotypes. When viewed from a coarse taxonomic level, our data support assertions that these chemoautotrophic groups are functionally redundant in terms of their core metabolic capabilities since they were simultaneously active under all incubation conditions. In contrast, the higher resolution of amplicon sequencing allowed us to reveal finer-scale differences in growth that likely reflect adaptation of physiologically-distinct subtypes to varying oxygen concentrations in situ. Despite this progress, we still know remarkably little about the factors that maintain genomic diversity and allow for stable co-existence among these three campylobacterial groups. Moving forward, we suggest that more subtle biological factors such as enzyme substrate specificity, motility, cell morphology, and tolerance to environmental stress should be more thoroughly investigated to better understand ecological niche differentiation at deep-sea hydrothermal vents.

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

2017 ◽  
Vol 4 (4) ◽  
pp. 160829 ◽  
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.

scholarly journals LabHorta: a controlled aquarium system for monitoring physiological characteristics of the hydrothermal vent mussel Bathymodiolus azoricus

2010 ◽  
Vol 68 (2) ◽  
pp. 349-356 ◽  
Author(s):  
Ana Colaço ◽  
Raul Bettencourt ◽  
Valentina Costa ◽  
Silvia Lino ◽  
Humberto Lopes ◽  
...  
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Hydrothermal Vents ◽  
Experimental Studies ◽  
Environmental Parameters ◽  
Condition Index ◽  
Physiological Characteristics ◽  
Good Tool ◽  
Experimental Conditions ◽  
Menez Gwen

AbstractColaço, A., Bettencourt, R., Costa, V., Lino, S., Lopes, H., Martins, I., Pires, L., Prieto, C., and Serrão Santos, R. 2011. LabHorta: a controlled aquarium system for monitoring physiological characteristics of the hydrothermal vent mussel Bathymodiolus azoricus. – ICES Journal of Marine Science, 68: 349–356. LabHorta is a facility composed of laboratories and retrievable deep-sea cages created to support and expand the capabilities of research cruises. It also enhances the ability to conduct experimental studies with organisms from deep-sea hydrothermal vents and other deep-sea environments, while keeping them under controlled conditions of pressure and water chemistry. This paper presents a case study with the vent mussel Bathymodiolus azoricus (which harbours a dual symbiosis) collected at the Menez Gwen hydrothermal vent field at 840-m depth, transported to experimental aquaria at atmospheric pressure and maintained under four different controlled experimental conditions to study their comparative condition index (CI). Environmental parameters were monitored daily and efforts were made to keep these constant. During the first few months, there were differences between the CI scores of mussels kept under the various conditions. After 6 months, the differences are not so clear but mussels still had sulphur-oxidizing bacteria when fed with sulphide. The methane oxidizer bacteria disappear even in the presence of methane. A range of CI scores appeared as a function of the culture type. The LabHorta facility is a good tool for performing long-term physiological studies of deep-sea organisms, simulating possible changes in the natural environmental where they normally thrive.

scholarly journals Rapid Microbial Production of Filamentous Sulfur Mats at Hydrothermal Vents

1999 ◽  
Vol 65 (5) ◽  
pp. 2253-2255 ◽  
Author(s):  
Craig D. Taylor ◽  
Carl O. Wirsen ◽  
Françoise Gaill
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Continuous Flow ◽  
Hydrothermal Vents ◽  
Flow Reactors ◽  
Organic Matter Production ◽  
Matter Production ◽  
Metabolic Capability ◽  
Continuous Flow Reactors

ABSTRACT During recent oceanographic cruises to Pacific hydrothermal vent sites (9°N and the Guaymas Basin), the rapid microbial formation of filamentous sulfur mats by a new chemoautotrophic, hydrogen sulfide-oxidizing bacterium was documented in both in situ and shipboard experiments. Observations suggest that formation of these sulfur mats may be a factor in the initial colonization of hydrothermal surfaces by macrofaunal Alvinella worms. This novel metabolic capability, previously shown to be carried out by a coastal strain in H2S continuous-flow reactors, may be an important, heretofore unconsidered, source of microbial organic matter production at deep-sea hydrothermal vents.

scholarly journals Development of an Easy-to-Operate Underwater Raman System for Deep-Sea Cold Seep and Hydrothermal Vent In Situ Detection

Sensors ◽  
2021 ◽  
Vol 21 (15) ◽  
pp. 5090
Author(s):  
Qingsheng Liu ◽  
Jinjia Guo ◽  
Wangquan Ye ◽  
Kai Cheng ◽  
Fujun Qi ◽  
...  
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Methane Hydrate ◽  
Sulfur Cycle ◽  
Cold Seep ◽  
Remotely Operated Vehicle ◽  
Bacterial Mats ◽  
Optical Module ◽  
In Situ Detection

As a powerful in situ detection technique, Raman spectroscopy is becoming a popular underwater investigation method, especially in deep-sea research. In this paper, an easy-to-operate underwater Raman system with a compact design and competitive sensitivity is introduced. All the components, including the optical module and the electronic module, were packaged in an L362 × Φ172 mm titanium capsule with a weight of 20 kg in the air (about 12 kg in water). By optimising the laser coupling mode and focusing lens parameters, a competitive sensitivity was achieved with the detection limit of SO42− being 0.7 mmol/L. The first sea trial was carried out with the aid of a 3000 m grade remotely operated vehicle (ROV) “FCV3000” in October 2018. Over 20,000 spectra were captured from the targets interested, including methane hydrate, clamshell in the area of cold seep, and bacterial mats around a hydrothermal vent, with a maximum depth of 1038 m. A Raman peak at 2592 cm−1 was found in the methane hydrate spectra, which revealed the presence of hydrogen sulfide in the seeping gas. In addition, we also found sulfur in the bacterial mats, confirming the involvement of micro-organisms in the sulfur cycle in the hydrothermal field. It is expected that the system can be developed as a universal deep-sea survey and detection equipment in the near future.

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

2001 ◽  
Vol 67 (10) ◽  
pp. 4566-4572 ◽  
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.

Pressure and Temperature Adaptation of Cytosolic Malate Dehydrogenases of Shallowand Deep-Living Marine Invertebrates: Evidence for High Body Temperatures in Hydrothermal Vent Animals

1991 ◽  
Vol 159 (1) ◽  
pp. 473-487 ◽  
Author(s):  
ELIZABETH DAHLHOFF ◽  
GEORGE N. SOMERO
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vents ◽  
Elevated Temperatures ◽  
Marine Invertebrates ◽  
Distribution Patterns ◽  
Pressure Effects ◽  
Temperature Adaptation ◽  
Body Temperatures ◽  
Elevated Pressures

Effects of temperature and hydrostatic pressure were measured on cytosolic malate dehydrogenases (cMDHs) from muscle tissue of a variety of shallow- and deep-living benthic marine invertebrates, including seven species endemic to the deep-sea hydrothermal vents. The apparent Michaelis-Menten constant (Km) of coenzyme (nicotinamide adenine dinucleotide, NADH), used to index temperature and pressure effects, was conserved within a narrow range (approximately 15–25 μmoll−1) at physiological temperatures and pressures for all species. However, at elevated pressures, the Km of NADH rose sharply for cMDHs of shallow species (depths of occurrence >Approximately 500 m), but not for the cMDHs of deep-sea species. Cytosolic MDHs of invertebrates from the deep-sea hydrothermal vents generally were not perturbed by elevated temperatures (15–25°C) at in situ pressures, but cMDHs of cold-adapted deep-sea species were. At a single measurement temperature, the Km of NADH for cMDHs from invertebrates from habitats with well-characterized temperatures was inversely related to maximal sustained body temperature. This correlation was used to predict the maximal sustained body temperatures of vent invertebrates for which maximal habitat and body temperatures are difficult to estimate. Species occurring on the ‘smoker chimneys’, which emit waters with temperatures up to 380°C, are predicted to have sustained body temperatures that are approximately 20–25°C higher than vent species living in cooler vent microhabitats. We conclude that, just as adaptation of enzymes to elevated pressures is important in establishing species’ depth distribution patterns, adaptation of pressure-adapted enzymes to temperature is critical in enabling certain vent species to exploit warm-water microhabitats in the vent environment.

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

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.

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

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e7397 ◽  
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.

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

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.

Sign in / Sign up

Export Citation Format

Share Document