CompLaB v1.0: a scalable pore-scale model for flow, biogeochemistry, microbial metabolism, and biofilm dynamics

Microbial activity and chemical reactions in porous media depend on the local conditions at the pore scale and can involve complex feedback with fluid flow and mass transport. We present a modeling framework that quantitatively accounts for the interactions between the bio(geo)chemical and physical processes and that can integrate genome-scale microbial metabolic information into a dynamically changing, spatially explicit representation of environmental conditions. The model couples a lattice Boltzmann implementation of Navier–Stokes (flow) and advection–diffusion-reaction (mass conservation) equations. Reaction formulations can include both kinetic rate expressions and flux balance analysis, thereby integrating reactive transport modeling and systems biology. We also show that the use of surrogate models such as neural network representations of in silico cell models can speed up computations significantly, facilitating applications to complex environmental systems. Parallelization enables simulations that resolve heterogeneity at multiple scales, and a cellular automaton module provides additional capabilities to simulate biofilm dynamics. The code thus constitutes a platform suitable for a range of environmental, engineering and – potentially – medical applications, in particular ones that involve the simulation of microbial dynamics

Porewater salinity in a southeastern United States salt marsh: controls and interannual variation

In coastal marsh ecosystems, porewater salinity strongly affects vegetation distribution and productivity. To simulate marsh porewater salinity, an integrated, spatially explicit model was developed, accounting for tidal inundation, evaporation, and precipitation, as well as lateral and vertical exchanges in both surface waters and the subsurface. It was applied to the Duplin River marsh, Sapelo Island, USA, over a 3-year period, which covered both drought and wet conditions. Simulated porewater salinity in the low and high marsh correlated with Duplin River salinity, with evapotranspiration and precipitation leading to substantial variations in porewater salinities across seasons, in particular in the high marsh. The model revealed substantial interannual variability in marsh soil conditions, and—due to its process-based approach linked to external forcings—can be used to explore effects of sea level rise and changes in hydrological forcings on marsh soil conditions

Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

About 382 Tg yr⁻¹ of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia

Intercellular Genomics of Subsurface Microbial Colonies

This report summarizes progress in the second year of this project. The objective is to develop methods and software to predict the spatial configuration, properties and temporal evolution of microbial colonies in the subsurface. To accomplish this, we integrate models of intracellular processes, cell-host medium exchange and reaction-transport dynamics on the colony scale. At the conclusion of the project, we aim to have the foundations of a predictive mathematical model and software that captures the three scales of these systems – the intracellular, pore, and colony wide spatial scales. In the second year of the project, we refined our transcriptional regulatory network discovery (TRND) approach that utilizes gene expression data along with phylogenic similarity and gene ontology analyses and applied it successfully to E.coli, human B cells, and Geobacter sulfurreducens. We have developed a new Web interface, GeoGen, which is tailored to the reconstruction of microbial TRNs and solely focuses on Geobacter as one of DOE’s high priority microbes. Our developments are designed such that the frameworks for the TRND and GeoGen can readily be used for other microbes of interest to the DOE. In the context of modeling a single bacterium, we are actively pursuing both steady-state and kinetic approaches. The steady-state approach is based on a flux balance that uses maximizing biomass growth rate as its objective, subjected to various biochemical constraints, for the optimal values of reaction rates and uptake/release of metabolites. For the kinetic approach, we use Karyote, a rigorous cell model developed by us for an earlier DOE grant and the DARPA BioSPICE Project. We are also investigating the interplay between bacterial colonies and environment at both pore and macroscopic scales. The pore scale models use detailed representations for realistic porous media accounting for the distribution of grain size whereas the macroscopic models employ the Darcy-type flow equations and up-scaled advective-diffusive transport equations for chemical species. We are rigorously testing the relationship between these two scales by evaluating macroscopic parameters using the volume averaging methodology applied to pore scale model results

Microbial interactions in the anaerobic oxidation of methane: Model simulations constrained by process rates and activity patterns

Proposed syntrophic interactions between the archaeal and bacterial cells mediating anaerobic oxidation of methane coupled with sulfate reduction include electron transfer through (1) the exchange of H2 or small organic molecules between methane‐oxidizing archaea and sulfate‐reducing bacteria, (2) the delivery of disulfide from methane‐oxidizing archaea to bacteria for disproportionation and (3) direct interspecies electron transfer. Each of these mechanisms was implemented in a reactive transport model. The simulated activities across different arrangements of archaeal and bacterial cells and aggregate sizes were compared to empirical data for AOM rates and intra‐aggregate spatial patterns of cell‐specific anabolic activity determined by FISH‐nanoSIMS. Simulation results showed that rates for chemical diffusion by mechanism (1) were limited by the build‐up of metabolites, while mechanisms (2) and (3) yielded cell specific rates and archaeal activity distributions that were consistent with observations from single cell resolved FISH‐nanoSIMS analyses. The novel integration of both intra‐aggregate and environmental data provided powerful constraints on the model results, but the similarities in model outcomes for mechanisms (2) and (3) highlight the need for additional observational data (e.g. genomic or physiological) on electron transfer and metabolic functioning of these globally important methanotrophic consortia

Transcriptional Changes Underlying Elemental Stoichiometry Shifts in a Marine Heterotrophic Bacterium

Marine bacteria drive the biogeochemical processing of oceanic dissolved organic carbon (DOC), a 750-Tg C reservoir that is a critical component of the global C cycle. Catabolism of DOC is thought to be regulated by the biomass composition of heterotrophic bacteria, as cells maintain a C:N:P ratio of ∼50:10:1 during DOC processing. Yet a complicating factor in stoichiometry-based analyses is that bacteria can change the C:N:P ratio of their biomass in response to resource composition. We investigated the physiological mechanisms of resource-driven shifts in biomass stoichiometry in continuous cultures of the marine heterotrophic bacterium Ruegeria pomeroyi (a member of the Roseobacter clade) under four element limitation regimes (C, N, P, and S). Microarray analysis indicated that the bacterium scavenged for alternate sources of the scarce element when cells were C-, N-, or P-limited; reworked the ratios of biomolecules when C- and P- limited; and exerted tighter control over import/export and cytoplasmic pools when N-limited. Under S limitation, a scenario not existing naturally for surface ocean microbes, stress responses dominated transcriptional changes. Resource-driven changes in C:N ratios of up to 2.5-fold and in C:P ratios of up to sixfold were measured in R. pomeroyi biomass. These changes were best explained if the C and P content of the cells was flexible in the face of shifting resources but N content was not, achieved through the net balance of different transcriptional strategies. The cellular-level metabolic trade-offs that govern biomass stoichiometry in R. pomeroyi may have implications for global carbon cycling if extendable to other heterotrophic bacteria. Strong homeostatic responses to N limitation by marine bacteria would intensify competition with autotrophs. Modification of cellular inventories in C- and P-limited heterotrophs would vary the elemental ratio of particulate organic matter sequestered in the deep ocean

Microbial interactions in the anaerobic oxidation of methane: Model simulations constrained by process rates and activity patterns

Proposed syntrophic interactions between the archaeal and bacterial cells mediating anaerobic oxidation of methane coupled with sulfate reduction include electron transfer through (1) the exchange of H2 or small organic molecules between methane‐oxidizing archaea and sulfate‐reducing bacteria, (2) the delivery of disulfide from methane‐oxidizing archaea to bacteria for disproportionation and (3) direct interspecies electron transfer. Each of these mechanisms was implemented in a reactive transport model. The simulated activities across different arrangements of archaeal and bacterial cells and aggregate sizes were compared to empirical data for AOM rates and intra‐aggregate spatial patterns of cell‐specific anabolic activity determined by FISH‐nanoSIMS. Simulation results showed that rates for chemical diffusion by mechanism (1) were limited by the build‐up of metabolites, while mechanisms (2) and (3) yielded cell specific rates and archaeal activity distributions that were consistent with observations from single cell resolved FISH‐nanoSIMS analyses. The novel integration of both intra‐aggregate and environmental data provided powerful constraints on the model results, but the similarities in model outcomes for mechanisms (2) and (3) highlight the need for additional observational data (e.g. genomic or physiological) on electron transfer and metabolic functioning of these globally important methanotrophic consortia

Intermittent bioirrigation and oxygen dynamics in permeable sediments: An experimental and modeling study of three tellinid bivalves

To explore the dynamic nature of geochemical conditions in bioirrigated marine permeable sediments, we studied the hydraulic activity of three tellinacean bivalve molluscs (the Pacific species Macoma nasuta and Macomona liliana, and the northern Atlantic and Pacific species Macoma balthica). We combined porewater pressure sensing, time-lapse photography and oxygen imaging to quantify the durations and frequencies of tellinid irrigation activity and the associated oxygen dynamics in the sediment. Porewater pressure records of all tellinids were dominated by intermittent porewater pressurization, induced by periodic water injection into the sediment through their excurrent siphons, which resulted in intermittent oxygen supply to subsurface sediments. The irrigation (two–12 minutes long) and intervals between subsequent irrigation bouts (1.5–13 minutes) varied among tellinid species and individual sizes. For large M. liliana and M. nasuta, the average intervals between irrigation bouts were sufficiently long (10 minutes and four minutes, respectively) to allow complete oxygen consumption in between irrigation bouts in all tested sediment types. Irrigation patterns of smaller conspecifics and the smaller species M. balthica were characterized by significantly shorter separation of irrigation bouts, which resulted in more continuous oxygenation of the sediment. Transport-reaction modeling confirmed these species- and size-specific geochemical signatures and indicated that the geochemical character of the sediment is largely conditioned by the interplay between temporal irrigation patterns and sedimentary oxygen consumption rates. For large tellinids, model simulations indicated that oscillatory rather than stationary geochemical conditions are prevalent in a wide range of sediment types, with oxic pockets collapsing completely between periods of active irrigation. Based on the model results we developed analytical approximations that allow estimation of spatio-temporal characteristics of sediment oxygenation for a wide range of sediment types and infaunal activity patterns. Our results emphasize the need to consider the intermittent nature of bioirrigation when studying the geochemical impact of infauna in permeable sediments