Gibbs Energy Dynamic Yield Method (GEDYM): Predicting microbial growth yields under energy-limiting conditions

The final publication is available at Elsevier via https://dx.doi.org/10.1016/j.gca.2018.08.023 © 2018. This open-access version is made available under the CC-BY-NC-ND 4.0 license https://creativecommons.org/licenses/by-nc-nd/4.0/Biomass-explicit biogeochemical models assign microbial growth yields (Y) using values measured in the laboratory or predicted using thermodynamics-based methods. However, Y values are rarely measured under the low energy delivery conditions that often prevail in the subsurface, and existing predictive methods for calculating Y values when the catabolic energy supply rate is limited remain poorly tested. Here, we derive and validate a new semi-theoretical method for calculating Y values: the Gibbs Energy Dynamic Yield Method (GEDYM). Method validation relies on a compilation of 132 geochemically relevant literature Y values comprising predominantly (60%) low energy (> −25 kJ (mol e−)−1) metabolisms. GEDYM is based on estimating the Gibbs energy change of the metabolic reaction (ΔGmet), which links the Gibbs energy changes of the catabolic (ΔGcat) and anabolic (ΔGan) reactions of a microorganism through its growth yield. Given that the values of ΔGmet,ΔGcat and ΔGan all depend on their respective reaction quotients, the resulting Y values account for changes in the chemical environment surrounding the cells. GEDYM incorporates an empirical relationship that accurately estimates the extent to which ΔGmet deviates from its standard state value from the relative difference between ΔGcat and its corresponding standard state value. GEDYM yields Y values with lower relative errors and statistical bias than the existing Gibbs energy dissipation method (GEDM). Using dissimilatory iron reduction, sulfate reduction and methanogenesis as examples, we illustrate the importance of considering variations in ΔGcat and ΔGan when predicting Y values for individual metabolisms. Because of its ability to dynamically adjust the values of ΔGmet and Y to variable geochemical conditions, GEDYM yields a more realistic representation of geomicrobial activity in predictive reactive transport models.Canada Excellence Research Chairs, Government of CanadaU.S. Department of Energy ["DE-SC0005520"

Iron Isotope Fractionations Reveal a Finite Bioavailable Fe Pool for Structural Fe(III) Reduction in Nontronite

© 2016 American Chemical Society. This is an open access article published under an ACS AuthorChoice License, which permits copying and redistribution of the article or any adaptations for non-commercial purposes. The definitive version is available via: http://dx.doi.org/10.1021/acs.est.6b02019We report on stable Fe isotope fractionation during microbial and chemical reduction of structural Fe(III) in nontronite NAu-1. Fe-56/Fe-54 fractionation factors between aqueous Fe(II) and structural Fe(III) ranged from -1.2 to +0.8 parts per thousand. Microbial (Shewanella oneidensis and Geobacter sulfurreducens) and chemical (dithionite) reduction experiments revealed a two-stage process. Stage 1 was characterized by rapid reduction of a finite Fe(III) pool along the edges of the clay particles, accompanied by a limited release to solution of Fe(II), which partially adsorbed onto basal planes. Stable Fe isotope compositions revealed that electron transfer and atom exchange (ETAE) occurred between edge-bound Fe(II) and octahedral (structural) Fe(III) within the clay lattice, as well as between aqueous Fe(II) and structural Fe(III) via a transient sorbed phase. The isotopic fractionation factors decreased with increasing extent of reduction as a result of the depletion of the finite bioavailable Fe(III) pool. During stage 2, microbial reduction was inhibited while chemical reduction continued. However, further ETAE between aqueous Fe(II) and structural Fe(III) was not observed. Our results imply that the pool of bioavailable Fe(III) is restricted to structural Fe sites located near the edges of the clay particles. Blockage of ETAE distinguishes Fe(III) reduction of layered clay minerals from that of Fe oxyhydroxides, where accumulation of structural Fe(II) is much more limited.Ontario Early Researcher Award; NSERC; NASA Astrobiology Institute; Canada Excellence Research Chair (CERC) progra

Bacterial Stern layer diffusion: experimental determination with spectral induced polarization and sensitivity to nitrite toxicity

Spectral induced polarization signatures have been used as proxies for microbial abundance in subsurface environments, by taking advantage of the charged properties of microbial cell membranes. The method's applicability, however, remains qualitative, and signal interpretation ambiguous. The adoption of spectral induced polarization as a robust geo‐microbiological tool for monitoring microbial dynamics in porous media requires the development of quantitative relationships between biogeochemical targets and spectral induced polarization parameters, such as biomass density and imaginary conductivity (σ″). Furthermore, deriving cell density information from electrical signals in porous media necessitates a detailed understanding of the nature of the cell membrane surface charge dynamics. We present results from a fully saturated sand‐filled column reactor experiment where Shewanella oneidensis growth during nitrate reduction to ammonium was monitored using spectral induced polarization. While our results further confirm the direct dependence of σ″ on changing cell density, Cole–Cole derived relaxation times also record the changing surface charging properties of the cells, ascribed to toxic stress due to nitrite accumulation. Concurrent estimates of cell size yield the first measurement‐derived estimation of the apparent surface ion diffusion coefficient for cells (Ds = 5.4 ±1.3 µm2 s−1), strengthening the link between spectral induced polarization and electrochemical cell polarization. Our analysis provides a theoretical framework on which to build σ″–cell density relations using bench‐scale experiments, leading to eventual robust non‐destructive monitoring of in situ microbial growth dynamics.Canada Excellence Research Chair programmeWaterloo‐Technion University Cooperation Programm

Reductive Dissolution of Tl(I)–Jarosite by <i>Shewanella putrefaciens</i>: Providing New Insights into Tl Biogeochemistry

Thallium (Tl) is emerging as a metal of concern in countries such as China due to its release during the natural weathering of Tl-bearing ore deposits and mining activities. Despite the high toxicity of Tl, few studies have examined the reductive dissolution of Tl mineral phases by microbial populations. In this study we examined the dissolution of synthetic Tl­(I)–jarosite, (H₃O)_0.29Tl_0.71Fe_2.74(SO₄)₂(OH)_5.22(H₂O)_0.78, by <i>Shewanella putrefaciens</i> CN32 using batch experiments under anaerobic circumneutral conditions. Fe­(II) concentrations were measured over time and showed Fe­(II) production (4.6 mM) in inoculated samples by 893 h not seen in mineral and dead cell controls. Release of aqueous Tl was enhanced in inoculated samples whereby maximum concentrations in inoculated and cell-free samples reached 3.2 and 2.1 mM, respectively, by termination of the experiment. Complementary batch Tl/<i>S. putrefaciens</i> sorption experiments were conducted under experimentally relevant pH (5 and 6.3) at a Tl concentration of 35 μM and did not show significant Tl accumulation by either live or dead cells. Therefore, in contrast to many metals such as Pb and Cd, <i>S. putrefaciens</i> does not represent a sink for Tl in the environment and Tl is readily released from Tl–jarosite during both abiotic and biotic dissolution

Carbon turnover and microbial activity in an artificial soil under imposed cyclic drainage and imbibition

Water table fluctuations generate temporally and spatially dynamic physicochemical conditions that drive biogeochemical hot spots and hot moments in the vadose zone. However, their role in the cycling of soil C remains poorly known. Here, we present results from unvegetated column experiments filled with 45 cm of artificial soil containing 10% humus, and inoculated with a natural microbial extract. In one series of three replicate columns, five cycles, each consisting of a 4-wk drainage followed by a 4-wk imbibition period, were imposed, whereas in a second series, the water table remained static. Depth-resolved O-2 concentration profiles and headspace CO2 effluxes were markedly different between the two regimes. In the fluctuating regime, drainage periods yielded 2.5 times greater CO2 effluxes than imbibition periods. At the end of the experiment, the fluctuating water table columns exhibited a distinct zone of organic C (OC) depletion in the depth interval of 8-20 cm that was not observed under the static regime. Although this zone showed elevated levels of adenosine triphosphate (ATP), the microbial biomass was actually lower than at the corresponding depth interval of the static regime. A vertically stratified microbial community established in all columns that depended on oxygenation with depth. The 16S ribosomal RNA (rRNA) gene analyses showed a slightly higher diversity in the soil exposed to moisture fluctuations, but there was no clear difference in major taxa and microbial community composition between treatments. These results thus suggest that the localized enhancement of OC degradation induced by the water table fluctuations was driven by a more active, rather than a more abundant or compositionally very different, microbial community

Linking Spectral Induced Polarization (SIP) and Subsurface Microbial Processes: Results from Sand Column Incubation Experiments

Geophysical techniques, such as spectral induced polarization (SIP), offer potentially powerful approaches for in situ monitoring of subsurface biogeochemistry. The successful implementation of these techniques as monitoring tools for reactive transport phenomena, however, requires the deconvolution of multiple contributions to measured signals. Here, we present SIP spectra and complementary biogeochemical data obtained in saturated columns packed with alternating layers of ferrihydrite-coated and pure quartz sand, and inoculated with <i>Shewanella oneidensis</i> supplemented with lactate and nitrate. A biomass-explicit diffusion-reaction model is fitted to the experimental biogeochemical data. Overall, the results highlight that (1) the temporal response of the measured imaginary conductivity peaks parallels the microbial growth and decay dynamics in the columns, and (2) SIP is sensitive to changes in microbial abundance and cell surface charging properties, even at relatively low cell densities (<10⁸ cells mL^–1). Relaxation times (τ) derived using the Cole–Cole model vary with the dominant electron accepting process, nitrate or ferric iron reduction. The observed range of τ values, 0.012–0.107 s, yields effective polarization diameters in the range 1–3 μm, that is, 2 orders of magnitude smaller than the smallest quartz grains in the columns, suggesting that polarization of the bacterial cells controls the observed chargeability and relaxation dynamics in the experiments

The Cold Region Critical Zone in Transition: Responses to Climate Warming and Land Use Change

Global climate warming disproportionately affects high-latitude and mountainous terrestrial ecosystems. Warming is accompanied by permafrost thaw, shorter winters, earlier snowmelt, more intense soil freeze-thaw cycles, drier summers, and longer fire seasons. These environmental changes in turn impact surface water and groundwater flow regimes, water quality, greenhouse gas emissions, soil stability, vegetation cover, and soil (micro)biological communities. Warming also facilitates agricultural expansion, urban growth, and natural resource development, adding growing anthropogenic pressures to cold regions' landscapes, soil health, and biodiversity. Further advances in the predictive understanding of how cold regions' critical zone processes, functions, and ecosystem services will continue to respond to climate warming and land use changes require multiscale monitoring technologies coupled with integrated observational and modeling tools. We highlight some of the major challenges, knowledge gaps, and opportunities in cold region critical zone research, with an emphasis on subsurface processes and responses in both natural and agricultural ecosystems