Metal Release from Manganese Nodules in Anoxic Seawater and Implications for Deep-Sea Mining Dewatering Operations.

The potential mining of deep-sea polymetallic nodules has been gaining increasing attention due to their enrichment in metals essential for a low-carbon future. To date, there have been few scientific studies concerning the geochemical consequences of dewatered mining waste discharge into the pelagic water column, which can inform best practices in future mining operations. Here, we report the results of laboratory incubation experiments that simulate mining discharge into anoxic waters such as those that overlie potential mining sites in the North Pacific Ocean. We find that manganese nodules are reductively dissolved, with an apparent activation energy of 42.8 kJ mol-1, leading to the release of associated metals in the order manganese > nickel > copper > cobalt > cadmium > lead. The composition of trace metals released during the incubation allows us to estimate a likely trace metal budget from the simulated dewatering waste plume. These estimates suggest that released cobalt and copper are the most enriched trace metals within the plume, up to ∼15 times more elevated than the background seawater. High copper concentrations can be toxic to marine organisms. Future work on metal toxicity to mesopelagic communities could help us better understand the ecological effects of these fluxes of trace metals.

Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites.

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated Vmax, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample's methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.

Interactions Between Iron Sulfide Minerals and Organic Carbon: Implications for Biosignature Preservation and Detection.

Microbe-mineral interactions can produce unique composite materials, which can preserve biosignatures. Geological evidence suggests that iron sulfide (Fe-S) minerals are abundant in the subsurface of Mars. On Earth, the formation of Fe-S minerals is driven by sulfate-reducing microorganisms (SRM) that produce reactive sulfide. Moreover, SRM metabolites, as well as intact cells, can influence the morphology, particle size, aggregation, and composition of biogenic Fe-S minerals. In this work, we evaluated how simple and complex organic molecules-hexoses and amino acid/peptide mixtures, respectively-influence the formation of Fe-S minerals (simulated prebiotic conditions), and whether the observed patterns mimic the biological influence of SRM. To this end, organo-mineral aggregates were characterized with X-ray diffraction, scanning electron microscopy, and scanning transmission X-ray microscopy coupled to near-edge X-ray absorption fine structure spectroscopy. Overall, Fe-S minerals were found to have a strong affinity for proteinaceous organic matter. Fe-S minerals precipitated at simulated prebiotic conditions yielded organic carbon distributions that were more homogeneous than treatments with whole SRM cells. In prebiotic experiments, spectroscopy detected potential organic transformations during Fe-S mineral formation, including conversion of hexoses to sugar acids and polymerization of amino acids/peptides into larger peptides/proteins. In addition, prebiotic mineral-carbon assemblages produced nanometer-scaled filamentous aggregated morphologies. On the contrary, in biotic treatments with cells, organic carbon in minerals displayed a more heterogeneous distribution. Notably, "hot spots" of organic carbon and oxygen-containing functional groups, with the size, shape, and composition of microbial cells, were preserved in mineral aggregates. We propose a list of characteristics that could be used to help distinguish biogenic from prebiotic/abiotic Fe-S minerals and help refine the search of extant or extinct microbial life in the martian subsurface.

Mapping metabolic activity at single cell resolution in intact volcanic fumarole sediment.

Interactions among microorganisms and their mineralogical substrates govern the structure, function and emergent properties of microbial communities. These interactions are predicated on spatial relationships, which dictate metabolite exchange and access to key substrates. To quantitatively assess links between spatial relationships and metabolic activity, this study presents a novel approach to map all organisms, the metabolically active subset and associated mineral grains, all while maintaining spatial integrity of an environmental microbiome. We applied this method at an outgassing fumarole of Vanuatu's Marum Crater, one of the largest point sources of several environmentally relevant gaseous compounds, including H2O, CO2 and SO2. With increasing distance from the sediment-air surface and from mineral grain outer boundaries, organism abundance decreased but the proportion of metabolically active organisms often increased. These protected niches may provide more stable conditions that promote consistent metabolic activity of a streamlined community. Conversely, exterior surfaces accumulate more organisms that may cover a wider range of preferred conditions, implying that only a subset of the community will be active under any particular environmental regime. More broadly, the approach presented here allows investigators to see microbial communities 'as they really are' and explore determinants of metabolic activity across a range of microbiomes.

Iron and sulfide nanoparticle formation and transport in nascent hydrothermal vent plumes.

Deep-sea hydrothermal vents are a significant source of dissolved metals to the global oceans, producing midwater plumes enriched in metals that are transported thousands of kilometers from the vent source. Particle precipitation upon emission of hydrothermal fluids controls metal speciation and the magnitude of metal export. Here, we document metal sulfide particles, including pyrite nanoparticles, within the first meter of buoyant plumes from three high-temperature vents at the East Pacific Rise. We observe a zone of particle settling 10-20 cm from the orifice, indicated by stable sulfur isotopes; however, we also demonstrate that nanoparticulate pyrite (FeS2) is not removed from the plume and can account for over half of the filtered Fe (≤0.2 µm) up to one meter from the vent orifice. The persistence of nanoparticulate pyrite demonstrates that it is an important mechanism for near-vent Fe stabilisation and highlights the potential role of nanoparticles in element transport.

The Fe(II)-oxidizing Zetaproteobacteria: historical, ecological and genomic perspectives.

The Zetaproteobacteria are a class of bacteria typically associated with marine Fe(II)-oxidizing environments. First discovered in the hydrothermal vents at Loihi Seamount, Hawaii, they have become model organisms for marine microbial Fe(II) oxidation. In addition to deep sea and shallow hydrothermal vents, Zetaproteobacteria are found in coastal sediments, other marine subsurface environments, steel corrosion biofilms and saline terrestrial springs. Isolates from a range of environments all grow by autotrophic Fe(II) oxidation. Their success lies partly in their microaerophily, which enables them to compete with abiotic Fe(II) oxidation at Fe(II)-rich oxic/anoxic transition zones. To determine the known diversity of the Zetaproteobacteria, we have used 16S rRNA gene sequences to define 59 operational taxonomic units (OTUs), at 97% similarity. While some Zetaproteobacteria taxa appear to be cosmopolitan, others are enriched by specific habitats. OTU networks show that certain Zetaproteobacteria co-exist, sharing compatible niches. These niches may correspond with adaptations to O2, H2 and nitrate availability, based on genomic analyses of metabolic potential. Also, a putative Fe(II) oxidation gene has been found in diverse Zetaproteobacteria taxa, suggesting that the Zetaproteobacteria evolved as Fe(II) oxidation specialists. In all, studies suggest that Zetaproteobacteria are widespread, and therefore may have a broad influence on marine and saline terrestrial Fe cycling.

Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses.

Deep-sea hydrothermal vents are populated by dense communities of animals that form symbiotic associations with chemolithoautotrophic bacteria. To date, our understanding of which factors govern the distribution of host/symbiont associations (or holobionts) in nature is limited, although host physiology often is invoked. In general, the role that symbionts play in habitat utilization by vent holobionts has not been thoroughly addressed. Here we present evidence for symbiont-influenced, regional-scale niche partitioning among symbiotic gastropods (genus Alviniconcha) in the Lau Basin. We extensively surveyed Alviniconcha holobionts from four vent fields using quantitative molecular approaches, coupled to characterization of high-temperature and diffuse vent-fluid composition using gastight samplers and in situ electrochemical analyses, respectively. Phylogenetic analyses exposed cryptic host and symbiont diversity, revealing three distinct host types and three different symbiont phylotypes (one ε-proteobacteria and two γ-proteobacteria) that formed specific associations with one another. Strikingly, we observed that holobionts with ε-proteobacterial symbionts were dominant at the northern fields, whereas holobionts with γ-proteobacterial symbionts were dominant in the southern fields. This pattern of distribution corresponds to differences in the vent geochemistry that result from deep subsurface geological and geothermal processes. We posit that the symbionts, likely through differences in chemolithoautotrophic metabolism, influence niche utilization among these holobionts. The data presented here represent evidence linking symbiont type to habitat partitioning among the chemosynthetic symbioses at hydrothermal vents and illustrate the coupling between subsurface geothermal processes and niche availability.