Oceanic lithosphere exposed at the sea floor undergoes seawater-rock alteration reactions involving the oxidation and hydration of glassy basalt. Basalt alteration reactions are theoretically capable of supplying sufficient energy for chemolithoautotrophic growth. Such reactions have been shown to generate microbial biomass in the laboratory, but field-based support for the existence of microbes that are supported by basalt alteration is lacking. Here, using quantitative polymerase chain reaction, in situ hybridization and microscopy, we demonstrate that prokaryotic cell abundances on seafloor-exposed basalts are 3-4 orders of magnitude greater than in overlying deep sea water. Phylogenetic analyses of basaltic lavas from the East Pacific Rise (9 degrees N) and around Hawaii reveal that the basalt-hosted biosphere harbours high bacterial community richness and that community membership is shared between these sites. We hypothesize that alteration reactions fuel chemolithoautotrophic microorganisms, which constitute a trophic base of the basalt habitat, with important implications for deep-sea carbon cycling and chemical exchange between basalt and sea water.
. 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.The mixing of hot, chemically reduced hydrothermal fluids with cold, oxygenated deep-sea water drives the dominant inorganic reactions of polymetallic sulphide precipitation and Fe oxidation and precipitation in plumes 6 . As a consequence of seawater entrainment into rising plumes, the entire volume of the global ocean must, on average, come into contact with hydrothermal fluids and particles in a relatively short time, 4000-8000 yr. Much of the trace element chemical reactivity observed in plumes is attributed, but has not been firmly linked, to the precipitation and surface reactivity of Fe oxyhydroxide minerals in both buoyant and neutrally buoyant plumes 7 . The rate of hydrothermal Fe(ii) oxidation has been correlated with the redox state of local deep waters 8 ; however, roles for dissolved organic carbon 9 (DOC) and microbial activity 10 have also been hypothesized. Although hydrothermal plume processes influence important global ocean elemental cycles, there is little mechanistic information available about these processes owing to the dynamic character of the plume environment and the complexity of plume particles. Most knowledge of plume mineral composition and reactivity is inferred from either bulk digestion of filtered solids 7 or scanning electron microscopy with elemental analysis 6 . Here we use synchrotron-based X-ray absorption spectromicroscopy to investigate Fe and C speciation at the
Here we examine Fe speciation within Fe-encrusted biofilms formed during 2-month seafloor incubations of sulfide mineral assemblages at the Main Endeavor Segment of the Juan de Fuca Ridge. The biofilms were distributed heterogeneously across the surface of the incubated sulfide and composed primarily of particles with a twisted stalk morphology resembling those produced by some aerobic Fe-oxidizing microorganisms. Our objectives were to determine the form of biofilm-associated Fe, and identify the sulfide minerals associated with microbial growth. We used micro-focused synchrotron-radiation X-ray fluorescence mapping (lXRF), X-ray absorption spectroscopy (lTXAFS), and X-ray diffraction (lXRD) in conjunction with focused ion beam (FIB) sectioning, and high resolution transmission electron microscopy (HRTEM). The chemical and mineralogical composition of an Fe-encrusted biofilm was queried at different spatial scales, and the spatial relationship between primary sulfide and secondary oxyhydroxide minerals was resolved. The Fe-encrusted biofilms formed preferentially at pyrrhotite-rich (Fe 1Àx S, 0 6 x 6 0.2) regions of the incubated chimney sulfide. At the nanometer spatial scale, particles within the biofilm exhibiting lattice fringing and diffraction patterns consistent with 2-line ferrihydrite were identified infrequently. At the micron spatial scale, Fe lEXAFS spectroscopy and lXRD measurements indicate that the dominant form of biofilm Fe is a short-range ordered Fe oxyhydroxide characterized by pervasive edge-sharing Fe-O 6 octahedral linkages. Double corner-sharing Fe-O 6 linkages, which are common to Fe oxyhydroxide mineral structures of 2-line ferrihydrite, 6-line ferrihydrite, and goethite, were not detected in the biogenic iron oxyhydroxide (BIO). The suspended development of the BIO mineral structure is consistent with Fe(III) hydrolysis and polymerization in the presence of high concentrations of Fe-complexing ligands. We hypothesize that microbiologically produced Fe-complexing ligands may play critical roles in both the delivery of Fe(II) to oxidases, and the limited Fe(III) oxyhydroxide crystallinity observed within the biofilm. Our research provides insight into the structure and formation of naturally occurring, microbiologically produced Fe oxyhydroxide minerals in the deep-sea. We describe the initiation of microbial seafloor weathering, and the morphological and mineralogical signals that result from that process. Our observations provide a starting point from which progressively older and more extensively weathered seafloor sulfide minerals may be examined, with the ultimate goal of improved interpretation of ancient microbial processes and associated biological signatures.
Manganese (Mn) oxides are among the most reactive minerals within the environment, where they control the bioavailability of carbon, nutrients, and numerous metals. Although the ability of microorganisms to oxidize Mn(II) to Mn(III/IV) oxides is scattered throughout the bacterial and fungal domains of life, the mechanism and physiological basis for Mn(II) oxidation remains an enigma. Here, we use a combination of compound-specific chemical assays, microspectroscopy, and electron microscopy to show that a common Ascomycete filamentous fungus, Stilbella aciculosa , oxidizes Mn(II) to Mn oxides by producing extracellular superoxide during cell differentiation. The reactive Mn oxide phase birnessite and the reactive oxygen species superoxide and hydrogen peroxide are colocalized at the base of asexual reproductive structures. Mn oxide formation is not observed in the presence of superoxide scavengers (e.g., Cu) and inhibitors of NADPH oxidases (e.g., diphenylene iodonium chloride), enzymes responsible for superoxide production and cell differentiation in fungi. Considering the recent identification of Mn(II) oxidation by NADH oxidase-based superoxide production by a common marine bacterium ( Roseobacter sp.), these results introduce a surprising homology between some prokaryotic and eukaryotic organisms in the mechanisms responsible for Mn(II) oxidation, where oxidation appears to be a side reaction of extracellular superoxide production. Given the versatility of superoxide as a redox reactant and the widespread ability of fungi to produce superoxide, this microbial extracellular superoxide production may play a central role in the cycling and bioavailability of metals (e.g., Hg, Fe, Mn) and carbon in natural systems.
Marine mammal mass strandings have occurred for millions of years, but their origins defy singular explanations. Beyond human causes, mass strandings have been attributed to herding behaviour, large-scale oceanographic fronts and harmful algal blooms (HABs). Because algal toxins cause organ failure in marine mammals, HABs are the most common mass stranding agent with broad geographical and widespread taxonomic impact. Toxin-mediated mortalities in marine food webs have the potential to occur over geological timescales, but direct evidence for their antiquity has been lacking. Here, we describe an unusually dense accumulation of fossil marine vertebrates from Cerro Ballena, a Late Miocene locality in Atacama Region of Chile, preserving over 40 skeletons of rorqual whales, sperm whales, seals, aquatic sloths, walrus-whales and predatory bony fish. Marine mammal skeletons are distributed in four discrete horizons at the site, representing a recurring accumulation mechanism. Taphonomic analysis points to strong spatial focusing with a rapid death mechanism at sea, before being buried on a barrier-protected supratidal flat. In modern settings, HABs are the only known natural cause for such repeated, multispecies accumulations. This proposed agent suggests that upwelling zones elsewhere in the world should preserve fossil marine vertebrate accumulations in similar modes and densities.
The upper Tennessee River Basin contains the highest density of our nation's caves; yet, little is known regarding speleogenesis or Fe and Mn biomineralization in these predominantly epigenic systems. Mn:Fe ratios of Mn and Fe oxide-rich biofilms, coatings, and mineral crusts that were abundant in several different caves ranged from ca. 0.1 to 1.0 as measured using ICP-OES. At sites where the Mn:Fe ratio approached 1.0 this represented an order of magnitude increase above the bulk bedrock ratio, suggesting that biomineralization processes play an important role in the formation of these cave ferromanganese deposits. Estimates of total bacterial SSU rRNA genes in ferromanganese biofilms, coatings, and crusts measured approximately 7×10 7 -9×10 9 cells/g wet weight sample. A SSU-rRNA based molecular survey of biofilm material revealed that 21% of the 34 recovered dominant (non-singleton) OTUs were closely related to known metal-oxidizing bacteria or clones isolated from oxidized metal deposits. Several different isolates that promote the oxidation of Mn(II) compounds were obtained in this study, some from high dilutions (10 ) of deposit material. In contrast to studies of caves in other regions, SSU rRNA sequences of Mn-oxidizing bacterial isolates in this study most closely matched those of Pseudomonas, Leptothrix, Flavobacterium, and Janthinobacterium. Combined data from geochemical analyses, molecular surveys, and culture-based experiments suggest that a unique consortia of Mn(II)-oxidizing bacteria are abundant and promoting biomineralization processes within the caves of the upper Tennessee River Basin.
Biologically active, passive treatment systems are commonly employed for removing high concentrations of dissolved Mn(II) from coal mine drainage (CMD). Studies of microbial communities contributing to Mn attenuation through the oxidation of Mn(II) to sparingly soluble Mn(III/IV) oxide minerals, however, have been sparse to date. This study reveals a diverse community of Mn(II)-oxidizing fungi and bacteria existing in several CMD treatment systems.Acidic, metal-laden mine drainage is a significant problem for many regions in the United States and throughout the world. In Appalachia, centuries of coal mining has left thousands of abandoned mines that are discharging waters containing elevated levels of metals-particularly Mn, with concentrations as high as 150 mg liter Ϫ1 (see reference 9 and references therein and reference 23). In the eastern United States, one of the most common methods to remediate coal mine drainage (CMD) is the use of biologically active limestone treatment beds. In essence, dissolved metals, such as Mn(II), are immobilized in the treatment bed via precipitation of sparingly soluble oxide minerals (23, 24) that effectively remove other metal contaminants (e.g., Ni, Co, and Zn) through coprecipitation and surface adsorption reactions (26,31,47).The importance of microbial activity in the remediation of Mn-contaminated waters has frequently been observed (6,20,21,24,25). Several strains of Mn(II)-oxidizing bacteria have even been used for treating manganiferous mine waters (49). Recently Mariner et al. (32) identified Mn(II)-oxidizing fungi, in addition to bacteria, successfully growing in a Mn-attenuating bioreactor for treatment of mine waters. We also observed that the addition of fungicides inhibited Mn(II) oxidation in laboratory-based CMD treatment simulations (W. D. Burgos, H. Tan, C. M. Santelli, and C. M. Hansel, presented at the National Meeting of the American Society of Mining and Reclamation, Pittsburgh, PA, 5 to 11 June 2010), suggesting a role for fungal activity in Mn remediation. The identities, growth characteristics, and oxidation mechanisms of the microbial community contributing to CMD remediation, however, remain largely unresolved. The objective of this study was to define the Mn(II)-oxidizing microbial community existing in passive treatment systems designed to remove dissolved Mn(II) from CMD. Because the mechanisms of microbial Mn(II) oxidation are not fully elucidated and are not genetically tractable (13, 18), we initiated an extensive culture survey to identify microorganisms that catalyze Mn(II) oxidation and precipitate Mn(III/IV) oxide minerals. These results provide the foundation for future explorations identifying the key players in CMD remediation and factors impacting their activity.In October 2007, we sampled four Mn attenuation bedsSaxman Run (SRC1) and DeSale phases I, II, and III (DS1 to DS3)-in central Pennsylvania that are currently treating exceptionally high Mn concentrations (up to 119 mg liter Ϫ1 ; 2.2 mM) generated from abandoned coal mines. Ea...
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