Microbial eukaryotic predation pressure and biomass at deep-sea hydrothermal vents.

Deep-sea hydrothermal vent geochemistry shapes the foundation of the microbial food web by fueling chemolithoautotrophic microbial activity. Microbial eukaryotes (or protists) play a critical role in hydrothermal vent food webs as consumers and hosts of symbiotic bacteria, and as a nutritional source to higher trophic levels. We measured microbial eukaryotic cell abundance and predation pressure in low-temperature diffuse hydrothermal fluids at the Von Damm and Piccard vent fields along the Mid-Cayman Rise in the Western Caribbean Sea. We present findings from experiments performed under in situ pressure that show cell abundances and grazing rates higher than those done at 1 atmosphere (shipboard ambient pressure); this trend was attributed to the impact of depressurization on cell integrity. A relationship between the protistan grazing rate, prey cell abundance, and temperature of end-member hydrothermal vent fluid was observed at both vent fields, regardless of experimental approach. Our results show substantial protistan biomass at hydrothermally fueled microbial food webs, and when coupled with improved grazing estimates, suggest an important contribution of grazers to the local carbon export and supply of nutrient resources to the deep ocean.

Future of the Search for Life: Workshop Report.

The 2-week, virtual Future of the Search for Life science and engineering workshop brought together more than 100 scientists, engineers, and technologists in March and April 2022 to provide their expert opinion on the interconnections between life-detection science and technology. Participants identified the advances in measurement and sampling technologies they believed to be necessary to perform in situ searches for life elsewhere in our Solar System, 20 years or more in the future. Among suggested measurements for these searches, those pertaining to three potential indicators of life termed "dynamic disequilibrium," "catalysis," and "informational polymers" were identified as particularly promising avenues for further exploration. For these three indicators, small breakout groups of participants identified measurement needs and knowledge gaps, along with corresponding constraints on sample handling (acquisition and processing) approaches for a variety of environments on Enceladus, Europa, Mars, and Titan. Despite the diversity of these environments, sample processing approaches all tend to be more complex than those that have been implemented on missions or envisioned for mission concepts to date. The approaches considered by workshop breakout groups progress from nondestructive to destructive measurement techniques, and most involve the need for fluid (especially liquid) sample processing. Sample processing needs were identified as technology gaps. These gaps include technology and associated sampling strategies that allow the preservation of the thermal, mechanical, and chemical integrity of the samples upon acquisition; and to optimize the sample information obtained by operating suites of instruments on common samples. Crucially, the interplay between science-driven life-detection strategies and their technological implementation highlights the need for an unprecedented level of payload integration and extensive collaboration between scientists and engineers, starting from concept formulation through mission deployment of life-detection instruments and sample processing systems.

Phosphate availability and implications for life on ocean worlds.

Several moons in the outer solar system host liquid water oceans. A key next step in assessing the habitability of these ocean worlds is to determine whether life's elemental and energy requirements are also met. Phosphorus is required by all known life and is often limited to biological productivity in Earth's oceans. This raises the possibility that its availability may limit the abundance or productivity of Earth-like life on ocean worlds. To address this potential problem, here we calculate the equilibrium dissolved phosphate concentrations associated with the reaction of water and rocks-a key driver of ocean chemical evolution-across a broad range of compositional inputs and reaction conditions. Equilibrium dissolved phosphate concentrations range from 10-11 to 10-1 mol/kg across the full range of carbonaceous chondrite compositions and reaction conditions considered, but are generally > 10-5 mol/kg for most plausible scenarios. Relative to the phosphate requirements and uptake kinetics of microorganisms in Earth's oceans, such concentrations would be sufficient to support initially rapid cell growth and construction of global ocean cell populations larger than those observed in Earth's deep oceans.

Globally-distributed microbial eukaryotes exhibit endemism at deep-sea hydrothermal vents.

Single-celled microbial eukaryotes inhabit deep-sea hydrothermal vent environments and play critical ecological roles in the vent-associated microbial food web. 18S rRNA amplicon sequencing of diffuse venting fluids from four geographically- and geochemically-distinct hydrothermal vent fields was applied to investigate community diversity patterns among protistan assemblages. The four vent fields include Axial Seamount at the Juan de Fuca Ridge, Sea Cliff and Apollo at the Gorda Ridge, all in the NE Pacific Ocean, and Piccard and Von Damm at the Mid-Cayman Rise in the Caribbean Sea. We describe species diversity patterns with respect to hydrothermal vent field and sample type, identify putative vent endemic microbial eukaryotes, and test how vent fluid geochemistry may influence microbial community diversity. At a semi-global scale, microbial eukaryotic communities at deep-sea vents were composed of similar proportions of dinoflagellates, ciliates, Rhizaria, and stramenopiles. Individual vent fields supported distinct and highly diverse assemblages of protists that included potentially endemic or novel vent-associated strains. These findings represent a census of deep-sea hydrothermal vent protistan communities. Protistan diversity, which is shaped by the hydrothermal vent environment at a local scale, ultimately influences the vent-associated microbial food web and the broader deep-sea carbon cycle.

Volcanically hosted venting with indications of ultramafic influence at Aurora hydrothermal field on Gakkel Ridge.

The Aurora hydrothermal system, Arctic Ocean, hosts active submarine venting within an extensive field of relict mineral deposits. Here we show the site is associated with a neovolcanic mound located within the Gakkel Ridge rift-valley floor, but deep-tow camera and sidescan surveys reveal the site to be ≥100 m across-unusually large for a volcanically hosted vent on a slow-spreading ridge and more comparable to tectonically hosted systems that require large time-integrated heat-fluxes to form. The hydrothermal plume emanating from Aurora exhibits much higher dissolved CH4/Mn values than typical basalt-hosted hydrothermal systems and, instead, closely resembles those of high-temperature ultramafic-influenced vents at slow-spreading ridges. We hypothesize that deep-penetrating fluid circulation may have sustained the prolonged venting evident at the Aurora hydrothermal field with a hydrothermal convection cell that can access ultramafic lithologies underlying anomalously thin ocean crust at this ultraslow spreading ridge setting. Our findings have implications for ultra-slow ridge cooling, global marine mineral distributions, and the diversity of geologic settings that can host abiotic organic synthesis - pertinent to the search for life beyond Earth.

Science Objectives for Flagship-Class Mission Concepts for the Search for Evidence of Life at Enceladus.

Cassini revealed that Saturn's Moon Enceladus hosts a subsurface ocean that meets the accepted criteria for habitability with bio-essential elements and compounds, liquid water, and energy sources available in the environment. Whether these conditions are sufficiently abundant and collocated to support life remains unknown and cannot be determined from Cassini data. However, thanks to the plume of oceanic material emanating from Enceladus' south pole, a new mission to Enceladus could search for evidence of life without having to descend through kilometers of ice. In this article, we outline the science motivations for such a successor to Cassini, choosing the primary science goal to be determining whether Enceladus is inhabited and assuming a resource level equivalent to NASA's Flagship-class missions. We selected a set of potential biosignature measurements that are complementary and orthogonal to build a robust case for any life detection result. This result would be further informed by quantifications of the habitability of the environment through geochemical and geophysical investigations into the ocean and ice shell crust. This study demonstrates that Enceladus' plume offers an unparalleled opportunity for in situ exploration of an Ocean World and that the planetary science and astrobiology community is well equipped to take full advantage of it in the coming decades.

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents.

Microbial eukaryotes (or protists) in marine ecosystems are a link between primary producers and all higher trophic levels, and the rate at which heterotrophic protistan grazers consume microbial prey is a key mechanism for carbon transport and recycling in microbial food webs. At deep-sea hydrothermal vents, chemosynthetic bacteria and archaea form the base of a food web that functions in the absence of sunlight, but the role of protistan grazers in these highly productive ecosystems is largely unexplored. Here, we pair grazing experiments with a molecular survey to quantify protistan grazing and to characterize the composition of vent-associated protists in low-temperature diffuse venting fluids from Gorda Ridge in the northeast Pacific Ocean. Results reveal protists exert higher predation pressure at vents compared to the surrounding deep seawater environment and may account for consuming 28 to 62% of the daily stock of prokaryotic biomass within discharging hydrothermal vent fluids. The vent-associated protistan community was more species rich relative to the background deep sea, and patterns in the distribution and co-occurrence of vent microbes provide additional insights into potential predator-prey interactions. Ciliates, followed by dinoflagellates, Syndiniales, rhizaria, and stramenopiles, dominated the vent protistan community and included bacterivorous species, species known to host symbionts, and parasites. Our findings provide an estimate of protistan grazing pressure within hydrothermal vent food webs, highlighting the important role that diverse protistan communities play in deep-sea carbon cycling.

In situ observation of sponge trails suggests common sponge locomotion in the deep central Arctic.

In 2016, the research ice-breaker Polarstern surveyed the submerged peaks of the permanently ice-covered Langseth Ridge, a tectonic feature comprising the Karasik seamount and two deeper seamount peaks, abutting the Gakkel ultra-slow spreading ridge (87°N 62°E to 85.5°N 57.4°E)1. A towed marine camera sled and a hybrid remotely operated vehicle revealed these peaks to be covered by a dense demosponge community, at first glance reminiscent of North Atlantic Geodia grounds (sensu2). Sponges were observed on top of a thick layer of spicule mat (Figure 1 and Video S1), intermixed with underlying layers of empty siboglinid tubes and bivalve shells, a substrate covering almost the entire seafloor. We observed trails of densely interwoven spicules connected directly to the underside or lower flanks of sponge individuals (Figure 1), suggesting these trails are traces of motile sponges. This is the first time abundant sponge trails have been observed in situ and attributed to sponge mobility. Given the low primary production in this permanently ice-covered region, these trails may relate to feeding behavior and/or a strategy for dispersal of juveniles. Such trails may remain visible for long periods given the regionally low sedimentation rates.

Hydrothermal plume detection dataset from Chinese cruises to the equatorial East Pacific Rise.

In this data article, a dataset from hydrothermal plume investigations on East Pacific Rise collected during Chinese cruises from 2008 to 2011 is reported. The dataset is related to the research article entitled "Abundance of low-temperature axial venting at the equatorial East Pacific Rise" published in the journal Deep-Sea Research I by Chen et al. (2020). In the dataset, continuous strings of time-series sensor data were obtained by Miniature Autonomous Plume Recorders (MAPR) and an Oxidation-Reduction Potential (ORP) sensor, while the underwater position data was derived using Ultra Short Base Line (USBL) navigation. In this contribution, general characteristics of the data are summarized and showed here. All the data are stored in separate Microsoft Excel spreadsheets that are available for researchers and a link is provided to the full data at http://dx.doi.org/10.17632/jckyj5vyjx.1. The data will be of comparative value to those investigating hydrothermal activities along mid-ocean ridges, worldwide.

Abiotic redox reactions in hydrothermal mixing zones: Decreased energy availability for the subsurface biosphere.

Subseafloor mixing of high-temperature hot-spring fluids with cold seawater creates intermediate-temperature diffuse fluids that are replete with potential chemical energy. This energy can be harnessed by a chemosynthetic biosphere that permeates hydrothermal regions on Earth. Shifts in the abundance of redox-reactive species in diffuse fluids are often interpreted to reflect the direct influence of subseafloor microbial activity on fluid geochemical budgets. Here, we examine hydrothermal fluids venting at 44 to 149 °C at the Piccard hydrothermal field that span the canonical 122 °C limit to life, and thus provide a rare opportunity to study the transition between habitable and uninhabitable environments. In contrast with previous studies, we show that hydrocarbons are contributed by biomass pyrolysis, while abiotic sulfate (SO42-) reduction produces large depletions in H2 The latter process consumes energy that could otherwise support key metabolic strategies employed by the subseafloor biosphere. Available Gibbs free energy is reduced by 71 to 86% across the habitable temperature range for both hydrogenotrophic SO42- reduction to hydrogen sulfide (H2S) and carbon dioxide (CO2) reduction to methane (CH4). The abiotic H2 sink we identify has implications for the productivity of subseafloor microbial ecosystems and is an important process to consider within models of H2 production and consumption in young oceanic crust.

The NASA Roadmap to Ocean Worlds.

In this article, we summarize the work of the NASA Outer Planets Assessment Group (OPAG) Roadmaps to Ocean Worlds (ROW) group. The aim of this group is to assemble the scientific framework that will guide the exploration of ocean worlds, and to identify and prioritize science objectives for ocean worlds over the next several decades. The overarching goal of an Ocean Worlds exploration program as defined by ROW is to "identify ocean worlds, characterize their oceans, evaluate their habitability, search for life, and ultimately understand any life we find." The ROW team supports the creation of an exploration program that studies the full spectrum of ocean worlds, that is, not just the exploration of known ocean worlds such as Europa but candidate ocean worlds such as Triton as well. The ROW team finds that the confirmed ocean worlds Enceladus, Titan, and Europa are the highest priority bodies to target in the near term to address ROW goals. Triton is the highest priority candidate ocean world to target in the near term. A major finding of this study is that, to map out a coherent Ocean Worlds Program, significant input is required from studies here on Earth; rigorous Research and Analysis studies are called for to enable some future ocean worlds missions to be thoughtfully planned and undertaken. A second finding is that progress needs to be made in the area of collaborations between Earth ocean scientists and extraterrestrial ocean scientists.

Characterization and flux of marine oil snow settling toward the seafloor in the northern Gulf of Mexico during the Deepwater Horizon incident: Evidence for input from surface oil and impact on shallow shelf sediments.

Sediment trap samples from the shelf edge area (400-450m water depth), 58km northeast of the failed Macondo well, were collected before, during and after the Deepwater Horizon oil spill. Detailed chemical analyses of particulates revealed that fluxes of spill-derived TPH (2356µg/m2/day), total PAH (5.4µg/m2/day), and hopane (0.89µg/m2/day) settling to the seafloor directly beneath the surface-plume were 19- to 44-times higher during the active spill than pre- and post-spill background values. The oil was variably biodegraded, evaporated and photo-oxidized indicating that it derived from the sinking of surface oil. The hopane-based oil flux that we calculate (10bbl/km2) indicates that at least 76,000bbl of Macondo oil that reached the ocean surface subsequently sank over an area of approximately 7600km2. We explore how this flux of sunken surface oil contributed to the total volume of oil deposited on the seafloor following the Deepwater Horizon incident.

Deciphering the Complex Chemistry of Deep-Ocean Particles Using Complementary Synchrotron X-ray Microscope and Microprobe Instruments.

The reactivity and mobility of natural particles in aquatic systems have wide ranging implications for the functioning of Earth surface systems. Particles in the ocean are biologically and chemically reactive, mobile, and complex in composition. The chemical composition of marine particles is thought to be central to understanding processes that convert globally relevant elements, such as C and Fe, among forms with varying bioavailability and mobility in the ocean. The analytical tools needed to measure the complex chemistry of natural particles are the subject of this Account. We describe how a suite of complementary synchrotron radiation instruments with nano- and micrometer focusing, and X-ray absorption spectroscopy (XAS) and X-ray diffraction (XRD) capabilities are changing our understanding of deep-ocean chemistry and life. Submarine venting along mid-ocean ridges creates hydrothermal plumes where dynamic particle-forming reactions occur as vent fluids mix with deep-ocean waters. Whether plumes are net sources or sinks of elements in ocean budgets depends in large part on particle formation, reactivity, and transport properties. Hydrothermal plume particles have been shown to host microbial communities and exhibit complex size distributions, aggregation behavior, and composition. X-ray microscope and microprobe instruments can address particle size and aggregation, but their true strength is in measuring chemical composition. Plume particles comprise a stunning array of inorganic and organic phases, from single-crystal sulfides to poorly ordered nanophases and polymeric organic matrices to microbial cells. X-ray microscopes and X-ray microprobes with elemental imaging, XAS, and XRD capabilities are ideal for investigating these complex materials because they can (1) measure the chemistry of organic and inorganic constituents in complex matrices, usually within the same particle or aggregate, (2) provide strong signal-to-noise data with exceedingly small amounts of material, (3) simplify the chemical complexity of particles or sets of particles with a focused-beam, providing spatial resolution over 6 orders of magnitude (nanometer to millimeter), (4) provide elemental specificity for elements in the soft-, tender-, and hard-X-ray energies, (5) switch rapidly among elements of interest, and (6) function in the presence of water and gases. Synchrotron derived data sets are discussed in the context of important advances in deep-ocean technology, sample handling and preservation, molecular microbiology, and coupled physical-chemical-biological modeling. Particle chemistry, size, and morphology are all important in determining whether particles are reactive with dissolved constituents, provide substrates for microbial respiration and growth, and are delivered to marine sediments or dispersed by deep-ocean currents.

Subseafloor microbial communities in hydrogen-rich vent fluids from hydrothermal systems along the Mid-Cayman Rise.

Warm fluids emanating from hydrothermal vents can be used as windows into the rocky subseafloor habitat and its resident microbial community. Two new vent systems on the Mid-Cayman Rise each exhibits novel geologic settings and distinctively hydrogen-rich vent fluid compositions. We have determined and compared the chemistry, potential energy yielding reactions, abundance, community composition, diversity, and function of microbes in venting fluids from both sites: Piccard, the world's deepest vent site, hosted in mafic rocks; and Von Damm, an adjacent, ultramafic-influenced system. Von Damm hosted a wider diversity of lineages and metabolisms in comparison to Piccard, consistent with thermodynamic models that predict more numerous energy sources at ultramafic systems. There was little overlap in the phylotypes found at each site, although similar and dominant hydrogen-utilizing genera were present at both. Despite the differences in community structure, depth, geology, and fluid chemistry, energetic modelling and metagenomic analysis indicate near functional equivalence between Von Damm and Piccard, likely driven by the high hydrogen concentrations and elevated temperatures at both sites. Results are compared with hydrothermal sites worldwide to provide a global perspective on the distinctiveness of these newly discovered sites and the interplay among rocks, fluid composition and life in the subseafloor.

Basin-scale transport of hydrothermal dissolved metals across the South Pacific Ocean.

Hydrothermal venting along mid-ocean ridges exerts an important control on the chemical composition of sea water by serving as a major source or sink for a number of trace elements in the ocean. Of these, iron has received considerable attention because of its role as an essential and often limiting nutrient for primary production in regions of the ocean that are of critical importance for the global carbon cycle. It has been thought that most of the dissolved iron discharged by hydrothermal vents is lost from solution close to ridge-axis sources and is thus of limited importance for ocean biogeochemistry. This long-standing view is challenged by recent studies which suggest that stabilization of hydrothermal dissolved iron may facilitate its long-range oceanic transport. Such transport has been subsequently inferred from spatially limited oceanographic observations. Here we report data from the US GEOTRACES Eastern Pacific Zonal Transect (EPZT) that demonstrate lateral transport of hydrothermal dissolved iron, manganese, and aluminium from the southern East Pacific Rise (SEPR) several thousand kilometres westward across the South Pacific Ocean. Dissolved iron exhibits nearly conservative (that is, no loss from solution during transport and mixing) behaviour in this hydrothermal plume, implying a greater longevity in the deep ocean than previously assumed. Based on our observations, we estimate a global hydrothermal dissolved iron input of three to four gigamoles per year to the ocean interior, which is more than fourfold higher than previous estimates. Complementary simulations with a global-scale ocean biogeochemical model suggest that the observed transport of hydrothermal dissolved iron requires some means of physicochemical stabilization and indicate that hydrothermally derived iron sustains a large fraction of Southern Ocean export production.

Tracking the Fate of Particle Associated Fukushima Daiichi Cesium in the Ocean off Japan.

A three year time-series of particle fluxes is presented from sediment traps deployed at 500 and 1000 m at a site 115 km southeast of Fukushima Daiichi Nuclear Power Plant (FDNPP). Results show a high fraction of lithogenic material and mass flux peaks that do not align between the trap depths, suggesting a lateral source of sediments. Fukushima cesium-137 and cesium-134 were enhanced in flux peaks that, given variations in trap (137)Cs/(210)Pbex ratios, are characteristic of material derived from shelf and slope sediments found from <120 to >500 m. These lateral flux peaks are possibly triggered by passing typhoons. The Cs fluxes are an order of magnitude higher than were previously reported for the trap located 100 km due east of FDNPP. We attribute this large difference to the position of our trap under the southeasterly currents that carry contaminated waters and resuspended sediments away from FDNPP and into the Pacific. These higher Cs sedimentary fluxes offshore are still small relative to the inventory of Cs currently buried nearshore. Consequently, we do not expect them to effect any rapid decrease in Cs levels for the coastal sediments near FDNPP that have been linked to enhanced Cs in demersal fish.

Pathways for abiotic organic synthesis at submarine hydrothermal fields.

Arguments for an abiotic origin of low-molecular weight organic compounds in deep-sea hot springs are compelling owing to implications for the sustenance of deep biosphere microbial communities and their potential role in the origin of life. Theory predicts that warm H2-rich fluids, like those emanating from serpentinizing hydrothermal systems, create a favorable thermodynamic drive for the abiotic generation of organic compounds from inorganic precursors. Here, we constrain two distinct reaction pathways for abiotic organic synthesis in the natural environment at the Von Damm hydrothermal field and delineate spatially where inorganic carbon is converted into bioavailable reduced carbon. We reveal that carbon transformation reactions in a single system can progress over hours, days, and up to thousands of years. Previous studies have suggested that CH4 and higher hydrocarbons in ultramafic hydrothermal systems were dependent on H2 generation during active serpentinization. Rather, our results indicate that CH4 found in vent fluids is formed in H2-rich fluid inclusions, and higher n-alkanes may likely be derived from the same source. This finding implies that, in contrast with current paradigms, these compounds may form independently of actively circulating serpentinizing fluids in ultramafic-influenced systems. Conversely, widespread production of formate by ΣCO2 reduction at Von Damm occurs rapidly during shallow subsurface mixing of the same fluids, which may support anaerobic methanogenesis. Our finding of abiogenic formate in deep-sea hot springs has significant implications for microbial life strategies in the present-day deep biosphere as well as early life on Earth and beyond.

Influence of ice thickness and surface properties on light transmission through Arctic sea ice.

The observed changes in physical properties of sea ice such as decreased thickness and increased melt pond cover severely impact the energy budget of Arctic sea ice. Increased light transmission leads to increased deposition of solar energy in the upper ocean and thus plays a crucial role for amount and timing of sea-ice-melt and under-ice primary production. Recent developments in underwater technology provide new opportunities to study light transmission below the largely inaccessible underside of sea ice. We measured spectral under-ice radiance and irradiance using the new Nereid Under-Ice (NUI) underwater robotic vehicle, during a cruise of the R/V Polarstern to 83°N 6°W in the Arctic Ocean in July 2014. NUI is a next generation hybrid remotely operated vehicle (H-ROV) designed for both remotely piloted and autonomous surveys underneath land-fast and moving sea ice. Here we present results from one of the first comprehensive scientific dives of NUI employing its interdisciplinary sensor suite. We combine under-ice optical measurements with three dimensional under-ice topography (multibeam sonar) and aerial images of the surface conditions. We investigate the influence of spatially varying ice-thickness and surface properties on the spatial variability of light transmittance during summer. Our results show that surface properties such as melt ponds dominate the spatial distribution of the under-ice light field on small scales (<1000 m2), while sea ice-thickness is the most important predictor for light transmission on larger scales. In addition, we propose the use of an algorithm to obtain histograms of light transmission from distributions of sea ice thickness and surface albedo.

Eruption of a deep-sea mud volcano triggers rapid sediment movement.

Submarine mud volcanoes are important sources of methane to the water column. However, the temporal variability of their mud and methane emissions is unknown. Methane emissions were previously proposed to result from a dynamic equilibrium between upward migration and consumption at the seabed by methane-consuming microbes. Here we show non-steady-state situations of vigorous mud movement that are revealed through variations in fluid flow, seabed temperature and seafloor bathymetry. Time series data for pressure, temperature, pH and seafloor photography were collected over 431 days using a benthic observatory at the active Håkon Mosby Mud Volcano. We documented 25 pulses of hot subsurface fluids, accompanied by eruptions that changed the landscape of the mud volcano. Four major events triggered rapid sediment uplift of more than a metre in height, substantial lateral flow of muds at average velocities of 0.4 m per day, and significant emissions of methane and CO2 from the seafloor.