Spatial turnover in the composition of biological communities is governed by (ecological) Drift, Selection and Dispersal. Commonly applied statistical tools cannot quantitatively estimate these processes, nor identify abiotic features that impose these processes. For interrogation of subsurface microbial communities distributed across two geologically distinct formations of the unconfined aquifer underlying the Hanford Site in southeastern Washington State, we developed an analytical framework that advances ecological understanding in two primary ways. First, we quantitatively estimate influences of Drift, Selection and Dispersal. Second, ecological patterns are used to characterize measured and unmeasured abiotic variables that impose Selection or that result in low levels of Dispersal. We find that (i) Drift alone consistently governs B25% of spatial turnover in community composition; (ii) in deeper, finer-grained sediments, Selection is strong (governing B60% of turnover), being imposed by an unmeasured but spatially structured environmental variable; (iii) in shallower, coarser-grained sediments, Selection is weaker (governing B30% of turnover), being imposed by vertically and horizontally structured hydrological factors; (iv) low levels of Dispersal can govern nearly 30% of turnover and be caused primarily by spatial isolation resulting from limited exchange between finer and coarser-grain sediments; and (v) highly permeable sediments are associated with high levels of Dispersal that homogenize community composition and govern over 20% of turnover. We further show that our framework provides inferences that cannot be achieved using preexisting approaches, and suggest that their broad application will facilitate a unified understanding of microbial communities.
The authors wish to note the following: ''We wish to add direct references to a stochastic model of DNA replication previously applied to the Xenopus laevis early embryonic divisions. That model was applied to molecular combing experiments on cellfree extracts from Xenopus laevis embryos.'' The additional references appear below. www.pnas.org/cgi
Dissimilatory iron-reducing bacteria (DIRB) couple the oxidation of organic matter or H 2 to the reduction of iron oxides. The factors controlling the rate and extent of these reduction reactions and the resulting solid phases are complex and poorly understood. Batch experiments were conducted with amorphous hydrous ferric oxide (HFO) and the DIRB Shewanella putrefaciens, strain CN32, in well-defined aqueous solutions to investigate the reduction of HFO and formation of biogenic Fe(II) minerals. Lactate-HFO solutions buffered with either bicarbonate or 1,4-piperazinediethanesulfonic acid (PIPES) containing various combinations of phosphate and anthraquinone-2,6-disulfonate (AQDS), were inoculated with S. putrefaciens CN32. AQDS, a humic acid analog that can be reduced to dihydroanthraquinone by CN32, was included because of its ability to function as an electron shuttle during microbial iron reduction and as an indicator of pe. Iron reduction was measured with time, and the resulting solids were analyzed by X-ray diffraction, scanning electron microscopy (SEM), and transmission electron microscopy (TEM) with energy-dispersive X-ray spectroscopy (EDS) and selected area electron diffraction (SAED). In HCO 3 Ϫ buffered medium with AQDS, HFO was rapidly and extensively reduced, and the resulting solids were dominated by ferrous carbonate (siderite). Ferrous phosphate (vivianite) was also present in HCO 3 Ϫ medium containing P, and fine-grained magnetite was present as a minor phase in HCO 3 Ϫ medium with or without P. In the PIPESbuffered medium, the rate and extent of reduction was strongly influenced by AQDS and P. With AQDS, HFO was rapidly converted to highly crystalline magnetite whereas in its absence, magnetite mineralization was slower and the final material less crystalline. In PIPES with both P and AQDS, a green rust type compound [Fe (6-x) II Fe x III (OH) 12 ] xϩ [(A 2Ϫ) x/2 ⅐ yH 2 O] xϪ was the dominant solid phase formed; in the absence of AQDS a poorly crystalline product was observed. The measured pe and nature of the solids identified were consistent with thermodynamic considerations. The composition of aqueous media in which microbial iron reduction occurred strongly impacted the rate and extent of iron reduction and the nature of the reduced solids. This, in turn, can provide a feedback control mechanism on microbial metabolism. Hence, in sediments where geochemical conditions promote magnetite formation, two-thirds of the Fe(III) will be sequestered in a form that may not be available for anaerobic bacterial respiration.
Dissimilatory metal-reducing bacteria (DMRB) can utilize Fe(III) associated with aqueous complexes or solid phases, such as oxide and oxyhydroxide minerals, as a terminal electron acceptor coupled to the oxidation of H 2 or organic substrates. These bacteria are also capable of reducing other metal ions including Mn(IV), Cr(VI), and U(VI), a process that has a pronounced effect on their solubility and overall geochemical behavior. In spite of considerable study on an individual basis, the biogeochemical behavior of multiple metals subject to microbial reduction is poorly understood. To probe these complex processes, the reduction of U(VI) by the subsurface bacterium, Shewanella putrefaciens CN32, was investigated in the presence of goethite under conditions where the aqueous composition was controlled to vary U speciation and solubility. Uranium(VI), as the carbonate complexes UO 2 (CO 3) 3(aq) 4Ϫ and UO 2 (CO 3) 2(aq) 2Ϫ , was reduced by the bacteria to U(IV) with or without goethite [␣-FeOOH (s) ] present. Uranium(VI) in 1,4-piperazinediethhanesulfonic acid (PIPES) buffer that was estimated to be present predominantly as the U(VI) mineral metaschoepite [UO 3 ⅐ 2H 2 O (s) ], was also reduced by the bacteria with or without goethite. In contrast, only ϳ30% of the U(VI) associated with a synthetic metaschoepite was reduced by the organism in the presence of goethite with 1 mM lactate as the electron donor. This may have been due to the formation of a layer of UO 2(s) or Fe(OH) 3(s) on the surface of the metaschoepite that physically obstructed further bioreduction. Increasing the lactate to a non-limiting concentration (10 mM) increased the reduction of U(VI) from metaschoepite to greater than 80% indicating that the hypothesized surface-veneering effect was electron donor dependent. Uranium(VI) was also reduced by bacterially reduced anthraquinone-2,6-disulfonate (AQDS) in the absence of cells, and by Fe(II) sorbed to goethite in abiotic control experiments. In the absence of goethite, uraninite was a major product of direct microbial reduction and reduction by AH 2 DS. These results indicate that DMRB, via a combination of direct enzymatic or indirect mechanisms, can reduce U(VI) to insoluble U(IV) in the presence of solid Fe oxides.
Modern approaches for bioremediation of radionuclide contaminated environments are based on the ability of microorganisms to effectively catalyze changes in the oxidation states of metals that in turn influence their solubility. Although microbial metal reduction has been identified as an effective means for immobilizing highly-soluble uranium(VI) complexes in situ, the biomolecular mechanisms of U(VI) reduction are not well understood. Here, we show that c-type cytochromes of a dissimilatory metal-reducing bacterium, Shewanella oneidensis MR-1, are essential for the reduction of U(VI) and formation of extracelluar UO 2 nanoparticles. In particular, the outer membrane (OM) decaheme cytochrome MtrC (metal reduction), previously implicated in Mn(IV) and Fe(III) reduction, directly transferred electrons to U(VI). Additionally, deletions of mtrC and/or omcA significantly affected the in vivo U(VI) reduction rate relative to wild-type MR-1. Similar to the wild-type, the mutants accumulated UO 2 nanoparticles extracellularly to high densities in association with an extracellular polymeric substance (EPS). In wild-type cells, this UO 2-EPS matrix exhibited glycocalyx-like properties and contained multiple elements of the OM, polysaccharide, and heme-containing proteins. Using a novel combination of methods including synchrotron-based X-ray fluorescence microscopy and high-resolution immune-electron microscopy, we demonstrate a close association of the extracellular UO 2 nanoparticles with MtrC and OmcA (outer membrane cytochrome). This is the first study to our knowledge to directly localize the OM-associated cytochromes with EPS, which contains biogenic UO 2 nanoparticles. In the environment, such association of UO 2 nanoparticles with biopolymers may exert a strong influence on subsequent behavior including susceptibility to oxidation by O 2 or transport in soils and sediments.
Carbon tetrachloride (CT) was dechlorinated to chloroform (CF) under anoxic conditions by Fe(II) that was sorbed to the surface of goethite (α-FeOOH). No reaction occurred when Fe(II) was present and goethite was absent. Several abiotic experiments were conducted with goethite at 30 °C in which the total amount of Fe(II) in the system, the amount of sorbed Fe(II), the density of sorbed Fe(II), and the pH were varied. Regeneration of sorbed Fe(II) occurred when dissolved Fe2+ was available and maintained pseudo-first-order conditions with respect to CT. Analysis of the rates of CT loss for experiments with sorbed-Fe(II) regeneration showed the rate-determining-step to be first order with respect to CT, second order with respect to the volumetric concentration of sorbed Fe(II) (i.e., mmol sorbed Fe(II) L-1 suspension), and zero order with respect to H+ for pH between 4.2 and 7.3. The absolute rate constant for the reaction was determined to be 42 ± 5 M-2 s-1. Normalization of the observed rate constants to account for different goethite concentrations yielded reaction orders of one and zero, respectively, for CT and H+, and a second-order reaction with respect to the density of sorbed Fe(II) (i.e., mmol sorbed Fe(II) g-1 goethite). On the basis of the kinetic data, the rate-determining step is proposed to be a termolecular two-electron-transfer reaction involving two Fe2+ ions sorbed to adjacent sites on the goethite surface and a CCl4 molecule that approaches the surface. The primary role of the goethite surface, thus, is to catalyze the reaction by fixing the position of the two charged reactants in a geometry suitable for reaction with CT. In separate experiments, biogenic Fe(II) formed by the enzymatic reduction of goethite by the Fe(III)-reducing bacterium Shewanella alga, strain BrY, dechlorinated CT. Of the CT degraded by abiotic and biogenic Fe(II) on goethite, 83−90% was converted to chloroform (CF), which accumulated in the reaction vial. These results indicate that dechlorination reactions in Fe(III)-reducing environments may indirectly result from the enzymatic or chemical reduction of Fe(III)-bearing minerals such as goethite.
Environmental transitions often result in resource mixtures that overcome limitations to microbial metabolism, resulting in biogeochemical hotspots and moments. Riverine systems, where groundwater mixes with surface water (the hyporheic zone), are spatially complex and temporally dynamic, making development of predictive models challenging. Spatial and temporal variations in hyporheic zone microbial communities are a key, but understudied, component of riverine biogeochemical function. Here, to investigate the coupling among groundwater–surface water mixing, microbial communities and biogeochemistry, we apply ecological theory, aqueous biogeochemistry, DNA sequencing and ultra-high-resolution organic carbon profiling to field samples collected across times and locations representing a broad range of mixing conditions. Our results indicate that groundwater–surface water mixing in the hyporheic zone stimulates heterotrophic respiration, alters organic carbon composition, causes ecological processes to shift from stochastic to deterministic and is associated with elevated abundances of microbial taxa that may degrade a broad suite of organic compounds.
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