Biogeochemical processes at hydrothermal vents : microbes and minerals, bioenergetics, and carbon fluxes

Author Posting. © The Oceanography Society, 2012. This article is posted here by permission of The Oceanography Society for personal use, not for redistribution. The definitive version was published in Oceanography 25, no. 1 (2012): 196–208, doi:10.5670/oceanog.2012.18.Hydrothermal vents are among the most biologically active regions of the deep ocean. However, our understanding of the limits of life in this extreme environment, the extent of biogeochemical transformation that occurs in the crust and overlying ocean, and the impact of vent life on regional and global ocean chemistry is in its infancy. Recently, scientific studies have expanded our view of how vent microbes gain metabolic energy at vents through their use of dissolved chemicals and minerals contained in ocean basalts, seafloor sulfide deposits, and hydrothermal plumes and, in turn, how they catalyze chemical and mineral transformations. The scale of vent environments and the difficulties inherent in the study of life above, on, and below the deep seafloor have led to the development of geochemical and bioenergetic models. These models predict habitability and biological activity based on the chemical composition of hydrothermal fluids, seawater, and the surrounding rock, balanced by the physiological energy demand of cells. This modeling, coupled with field sampling for ground truth and discovery, has led to a better understanding of how hydrothermal vents affect the ocean and global geochemical cycles, and how they influence our views of life on the early Earth and the search for life beyond our own planet.Research for this paper was supported by the National Science Foundation (NSF) Division of Ocean Sciences grants 0732611 for JFH, 0926805 and 1038055 for JAB, and 1038055 for BMT; and by the University of Missouri Research Board for KLR

A multi-modal approach to measuring particulate iron speciation in buoyant hydrothermal plumes

Processes active within buoyant hydrothermal plumes are expected to modulate the flux of elements, such as Fe, to the deep ocean; however, they are yet to be described in a comprehensive manner through observations or models. In this study, we compare observed particulate Fe (pFe) speciation with thermodynamic (equilibrium) reaction path modeling for three vent fields in the Eastern Lau Spreading Center (ELSC). At each site, particles were collected from the buoyant rising portion of hydrothermal plumes using in situ filtration with a Remotely Operated Vehicle. Filter bound particles were analyzed by synchrotron micro-probe X-ray fluorescence mapping (XRF), X-ray diffraction (XRD), XRF spectroscopy, and X-ray absorption near edge structure (XANES) spectroscopy at the Fe 1 s edge, as well as XRF-based chemical speciation mapping for Fe. For buoyant plumes of the ELSC, diversity in solid-state chemistry was high, and poorly crystalline, meta-stable phases were common. We demonstrate that to fully describe the crystalline-to-noncrystalline character of plume pFe, a multi-modal XRD-XANES analytical approach is needed. We found that an equilibrium modeling approach worked well for pyrite but performed poorly for important families of meta-stable pFe, namely Fe (oxyhydr)oxides and monosulfides. Based on our findings, we recommend future field expeditions strategically explore sites representing a diversity of site-specific conditions to better capture the full range of processes active in plumes. We also recommend development of kinetic models, as well as expansion of thermodynamic databases to better reflect the solid-state composition of plumes. These steps should allow oceanographers to understand the processes controlling Fe speciation in plumes well enough to create realistic models of hydrothermal fluxes to the ocean

Sulfur oxidation genes in diverse deep-sea viruses

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of AAAS for personal use, not for redistribution. The definitive version was published in Science 344 (2014): 757-760, doi:10.1126/science.1252229.Viruses are the most abundant biological entities in the oceans and a pervasive cause of mortality of microorganisms that drive biogeochemical cycles. Although the ecological and evolutionary impacts of viruses on marine phototrophs are well-recognized, little is known about their impact on ubiquitous marine lithotrophs. Here we report 18 genome sequences of double-stranded DNA viruses that putatively infect widespread sulfur-oxidizing bacteria. Fifteen of these viral genomes contain auxiliary metabolic genes for the alpha and gamma subunits of reverse dissimilatory sulfite reductase (rdsr). This enzyme oxidizes elemental sulfur, which is abundant in the hydrothermal plumes studied here. Our findings implicate viruses as a key agent in the sulfur cycle and as a reservoir of genetic diversity for bacterial enzymes that underpin chemosynthesis in the deep oceans.This project is funded in part by the Gordon and Betty Moore Foundation Grant GBMF2609 and National Science Foundation Grant OCE1038006

Microbial iron uptake as a mechanism for dispersing iron from deep-sea hydrothermal vents

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Nature Publishing Group for personal use, not for redistribution. The definitive version was published in Nature Communications 5 (2014): 3192, doi:10.1038/ncomms4192.Deep-sea hydrothermal vents are a significant source of oceanic iron. Although hydrothermal iron rapidly precipitates as inorganic minerals upon mixing with seawater, it can be stabilized by organic matter and dispersed more widely than previously recognized. The nature and source of this organic matter is unknown. Here we show that microbial genes involved in cellular iron uptake are highly expressed in the Guaymas Basin deep-sea hydrothermal plume. The nature of these microbial iron transporters, taken together with the low concentration of dissolved iron and abundance of particulate iron in the plume, indicates that iron minerals are the target for this microbial scavenging and uptake. Our findings indicate that cellular iron uptake is a major process in plume microbial communities and suggest new mechanisms for generating Fe-C complexes. This “microbial iron pump” could represent an important mode of converting hydrothermal iron into bioavailable forms that can be dispersed through the oceans.This project is funded by the Gordon and Betty Moore Foundation through grant GBMF 2609 to GJD/JAB/BMT and by the National Science Foundation through grants OCE 1029242 to GJD, and R2K grant OCE1038055 to JAB/BMT. We thank the University of Michigan Rackham Graduate School Faculty Research Fellowship Program for their support.2014-08-0

Near-field iron and carbon chemistry of non-buoyant hydrothermal plume particles, Southern East Pacific Rise 15°S

Author Posting. © The Author(s), 2018. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Marine Chemistry 201 (2018): 183-197, doi:10.1016/j.marchem.2018.01.011.Iron (Fe)-poor surface waters limit phytoplankton growth and their ability to remove carbon (C) from the atmosphere and surface ocean. Over the past few decades, research has focused on constraining the global Fe cycle and its impacts on the global C cycle. Hydrothermal vents have become a highly debated potential source of Fe to the surface ocean. Two main mechanisms for transport of Fe over long distances have been proposed: Fe-bearing nanoparticles and organic C complexation with Fe in the dissolved (dFe) and particulate (pFe) pools. However, the ubiquity and importance of these processes is unknown at present, and very few vents have been investigated for Fe-Corg interactions or the transport of such materials away from the vent. Here we describe the near-field contributions (first ~100 km from ridge) of pFe and Corg to the Southern East Pacific Rise (SEPR) plume, one of the largest known hydrothermal plume features in the global ocean. Plume particles (> 0.2 μm) were collected as part of the U.S. GEOTRACES Eastern Pacific Zonal Transect cruise (GP16) by in-situ filtration. Sediment cores were also collected to investigate the properties of settling particles. In this study, X-ray absorption near edge structure (XANES) spectroscopy was used in two complementary X-ray synchrotron approaches, scanning transmission X-ray microscopy (STXM) and X-ray microprobe, to investigate the Fe and C speciation of particles within the near-field non-buoyant SEPR plume. When used in concert, STXM and X-ray microprobe provide fine-scale and representative information on particle morphology, elemental co-location, and chemical speciation. Bulk chemistry depth profiles for particulate Corg (POC), particulate manganese (pMn), and pFe indicated that the source of these materials to the non-buoyant plume is hydrothermal in origin. The plume particles at stations within the first ~100 km down-stream of the ridge were composites of mineral (oxidized Fe) and biological materials (organic C, Corg). Iron chemistry in the plume and in the core-top suspended sediment fluff layer were both dominated by Fe(III) phases, such as Fe(III) oxyhydroxides and Fe(III) phyllosilicates. Particulate sulfur (pS) was a rare component of our plume and sediment samples. When pS was detected, it was in the form of an Fe sulfide mineral phase, composing ≤ 0.4% of the Fe on a per atom basis. The resuspended sediment fluff layer contained a mixture of inorganic (coccolith fragments) and Corg bearing (lipid-rich biofilm-like) materials. The particle morphology and co-location of C and Fe in the sediment was different from that in plume particles. This indicates that if the Fe-Corg composite particles settle rapidly to the sediments, then they experience strong alteration during settling and/or within the sediments. Overall, our observations indicate that the particles within the first ~ 100 km of the laterally advected plume are S-depleted, Fe(III)-Corg composites indicative of a chemically oxidizing plume with strong biological modification. These findings confirm that the Fe-Corg relationships observed for non-buoyant plume particles within ~ 100 m of the vent site are representative of particles within this region of the non-buoyant plume (~100 km). These findings also point to dynamic alteration of Fe-Corg bearing particles during transport and settling. The specific biogeochemical processes at play, and the implications for nutrient cycling in the ocean are currently unknown and represent an area of future investigation

Low Temperature Geomicrobiology Follows Host Rock Composition Along a Geochemical Gradient in Lau Basin

The East Lau Spreading Center (ELSC) and Valu Fa Ridge (VFR) comprise a ridge segment in the southwest Pacific Ocean where rapid transitions in the underlying mantle chemistry manifest themselves as gradients in seafloor rock geochemistry. We studied the geology and microbial diversity of three silicate rock samples and three inactive sulfide chimney samples collected, from north to south, at the vent fields Kilo Moana, ABE, Tui Malila, and Mariner. This is the first study of microbial populations on basaltic andesite, which was sampled at Mariner vent field. Silicate rock geochemistry exhibits clear latitudinal trends that are mirrored by changes in bacterial community composition. α-proteobacteria, ε-proteobacteria, and Bacteroidetes are most common on a silicate collected from Kilo Moana and their proportions decrease linearly on silicates collected further south. Conversely, a silicate from Mariner vent field hosts high proportions of a unique lineage of Chloroflexi unrelated (<90% sequence similarity) to previously recovered environmental clones or isolates, which decrease at ABE and are absent at Kilo Moana. The exteriors of inactive sulfide structures are dominated by lineages of sulfur oxidizing α-proteobacteria, γ-proteobacteria, and ε-proteobacteria, while the interior of one chimney is dominated by putative sulfur-reducing δ-proteobacteria. A comparison of bacterial communities on inactive sulfides from this and previous studies reveals the presence of a clade of uncultured Bacteroidetes exclusive to sulfidic environments, and a high degree of heterogeneity in bacterial community composition from one sulfide structure to another. In light of the heterogeneous nature of bacterial communities observed here and in previous studies of both active and inactive hydrothermal sulfide structures, the presence of numerous niches may be detected on these structures in the future by finer scale sampling and analysis.Organismic and Evolutionary Biolog

Solid-phase arsenic speciation in aquifer sediments: A micro-X-ray absorption spectroscopy approach for quantifying trace-level speciation

Arsenic (As) is a geogenic contaminant affecting groundwater in geologically diverse systems globally. Arsenic release from aquifer sediments to groundwater is favored when biogeochemical conditions, especially oxidation-reduction (redox) potential, in aquifers fluctuate. The specific objective of this research is to identify the solid-phase sources and geochemical mechanisms of release of As in aquifers of the Des Moines Lobe glacial advance. The overarching concept is that conditions present at the aquifer-aquitard interfaces promote a suite of geochemical reactions leading to mineral alteration and release of As to groundwater. A microprobe X-ray absorption spectroscopy (μXAS) approach is developed and applied to rotosonic drill core samples to identify the solid-phase speciation of As in aquifer, aquitard, and aquifer-aquitard interface sediments. This approach addresses the low solid-phase As concentrations, as well as the fine-scale physical and chemical heterogeneity of the sediments. The spectroscopy data are analyzed using novel cosine-distance and correlation-distance hierarchical clustering for Fe 1s and As 1s μXAS datasets. The solid-phase Fe and As speciation is then interpreted using sediment and well-water chemical data to propose solid-phase As reservoirs and release mechanisms. The results confirm that in two of the three locations studied, the glacial sediment forming the aquitard is the source of As to the aquifer sediments. The results are consistent with three different As release mechanisms: (1) desorption from Fe (oxyhydr)oxides, (2) reductive dissolution of Fe (oxyhydr)oxides, and (3) oxidative dissolution of Fe sulfides. The findings confirm that glacial sediments at the interface between aquifer and aquitard are geochemically active zones for As. The diversity of As release mechanisms is consistent with the geographic heterogeneity observed in the distribution of elevated-As wells

Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume

Hydrothermal venting associated with mid-ocean ridge volcanism is globally widespread. This venting is responsible for a dissolved iron flux to the ocean that is approximately equal to that associated with continental riverine runoff. For hydrothermal fluxes, it has long been assumed that most of the iron entering the oceans is precipitated in inorganic forms. However, the possibility of globally significant fluxes of iron escaping these mass precipitation events and entering open-ocean cycles is now being debated, and two recent studies suggest that dissolved organic ligands might influence the fate of hydrothermally vented metals. Here we present spectromicroscopic measurements of iron and carbon in hydrothermal plume particles at the East Pacific Rise mid-ocean ridge. We show that organic carbon-rich matrices, containing evenly dispersed iron(II)-rich materials, are pervasive in hydrothermal plume particles. The absence of discrete iron(II) particles suggests that the carbon and iron associate through sorption or complexation. We suggest that these carbon matrices stabilize iron(II) released from hydrothermal vents in the region, preventing its oxidation and/or precipitation as insoluble minerals. Our findings have implications for deep-sea biogeochemical cycling of iron, a widely recognized limiting nutrient in the oceans