Biogeophysics. Sub-discipline of exploration geophysics focusing on the geophysical signatures resulting from microbial interactions with geologic media.
These geophysical signatures may arise from, (1) microbial cells and extracellular structures themselves, (2) growth of microorganisms (production of biomass) and biofilm formation, (3) generation of metabolic by-products and the interactions of these metabolites with the host material, and (4) microbially mediated processes. The geophysical signatures arising from each of these four source mechanisms are described below.
Geophysical detection of cells and biofilms
Microbial cells and biofilms exhibit distinct electrical properties, and certain (magnetotactic) bacteria also display unique magnetic characteristics. The membrane potential (the voltage drop across the membrane due to the negatively charged molecules inside cells) of live cells results in an accumulation of mobile electric-charge carriers at membrane surfaces. When live cells are placed in time-oscillating electric fields, these charges move on the surface of the membrane, giving rise to high polarizations for cellular suspensions that are readily measured with dielectric spectroscopy. As the mobility of these surface charges is relatively small, this effect is manifested at low frequencies, such that the relative dielectric permittivity of live-cell suspensions can be as high as 106 (Prodan et al., 2004; Stoy et al., 1982). The outer and inner cell radii, diffusion constants, and membrane potential all have a very distinct effect on broadband dielectric spectroscopy data (Prodan et al., 2008). Polarization enhancement is also observed when microbial cells are present in high concentrations in porous media (Ntarlagiannis et al., 2005), although additional polarization mechanisms associated with mineral surfaces may obscure the signal. This polarization is enhanced when cells are more preferentially adsorbed onto mineral surfaces (Abdel Aal et al., 2009).
The magnetic properties of soils and rock are altered by a diverse group of prokaryotes that exert a significant control over magnetite formation in two ways that differ mechanistically: biologically induced mineralization (BIM) and biologically controlled mineralization (BCM) (Jimenez-Lopez et al., 2010). Biologically induced magnetite formation is indistinguishable from magnetite formed by inorganic processes; however, biologically controlled magnetite formation is distinct and produced by magnetotactic bacteria (Jimenez-Lopez et al., 2010). These magnetotactic bacteria biomineralize intracellular, membrane-bound, single-magnetic-domain crystals of the magnetic minerals magnetite and/or greigite called magnetosomes (Bazylinski and Frankel, 2004). Magnetotactic bacteria are typically found in a wide variety of aquatic environments (e.g., fresh water lakes) with the highest numbers occurring mostly at oxic–anoxic interfaces. The presence of magnetotactic bacteria in sediments is often used as a proxy for paleoenvironmental/climatic conditions, and the presence of magnetosomes in sediments and other secondary magnetic minerals produced by microbial activity likely impacts the magnetic properties of the subsurface recorded with magnetic geophysical techniques as has been demonstrated at hydrocarbon contaminated sites (Rijal et al., 2010).
Biofilms (an attached state of cell growth, whereby cells are closely packed and firmly attached to each other) further alter the geophysical properties of soils. Low-frequency electrical measurements respond to self-limiting microbial growth/cell attachment and biofilm formation in porous media, as well as death and lyses of cells (Davis et al., 2006). Electrical polarization may result from the electrical properties of the biofilm itself or from the modification of grain surfaces due to cell attachment. Biofilms also alter the acoustic properties of porous media, with biofilm growth in soil columns resulting in spatial complexity of acoustic amplitudes (Davis et al., 2009). Such variations likely arise from a non-uniform distribution of microbial activity or heterogeneity in the biomass distribution and biofilm morphology (e.g., variations in biofilm thickness, roughness, hydration, etc.).
Geophysical detection of metabolic by-products and mineral weathering
Microbial metabolism enhances the weathering of minerals through the attachment, growth, and colonization of mineral surfaces by microorganisms (Bennett et al., 1996). Metabolic by-products, including biogenic gasses (e.g., CO2, H2S, CH4, etc.), organic acids, and biosurfactants, all affect electrical properties of porous media. Microbial production of organic acids and biosurfactants adds ions to solution, increasing electrolyte concentration of pore fluids (Cassidy et al., 2001). Organic acids enhance mobility of sparingly soluble metals and also increase the number of reaction sites, thus accelerating mineral weathering (Hiebert and Bennett, 1992). Enhanced mineral dissolution catalyzed by increased organic acid concentration can lead to physical changes in grain surface morphology, surface area, surface roughness and the generation of secondary porosity and increased permeability (McMahon et al., 1992). These changes in porosity affect acoustic wave propagation by altering grain contact coupling, and changes in surface area/roughness drive changes in electrical polarization. Biogenic gasses reduce bulk electrical conductivity and enhance attenuation of seismic signal amplitudes.
The effects of metabolic by-products on geophysical properties have been recorded in hydrocarbon contaminated environments (Abdel Aal et al., 2004; Werkema et al., 2003). Such sites are natural bioreactors where excess organic substrates stimulate microbial activity. Enhanced mineral weathering in hydrocarbon contaminated aquifers (Hiebert and Bennett, 1992; McMahon et al., 1995), increases pore fluid conductivity and thereby bulk conductivity sensed with a range of electromagnetic methods (Abdel Aal et al., 2004; Atekwana et al., 2004; Sauck et al., 1998). Elevated bulk conductivity is therefore found where intrinsic bioremediation and enhanced mineral weathering are occurring. These zones of highest bulk electrical conductivity may coincide with the highest percentages of oil degrading microbial populations, with spatial heterogeneity in the microbial community structure and shifts in the microbial community concomitant with vertical changes in bulk electrical conductivity (Allen et al., 2007). Biogenic methane production by archea in anaerobic soils can result in extensive free-phase gas production that reduces dielectric permittivity and electrical conductivity (Comas and Slater, 2007).
Geophysical detection of microbially mediated redox processes
Microbial metabolic activity is a critical driver of redox chemistry because microbes derive energy from oxidation-reduction reactions (the transfer of electrons from one reactant to the other). Terminal electron acceptors (TEAs) govern nutrient utilization by microbes during the breakdown of organic carbon (Cozzarelli et al., 1999). Microbial respiration consequently results in reduced conditions, and strong redox gradients in the Earth typically develop in the presence of heterotrophic bacteria. Significant changes in Eh and pH result in new mineral stability fields in which some minerals become unstable and are dissolved and mobilized, whereas others may precipitate from solution. As TEAs are consumed, changes in pore fluid chemistry may drive changes in pore fluid conductivity, thereby affecting bulk electrical conductivity.
Strong electrical potentials associated with current sources in the Earth are correlated with redox gradients recorded at sites where microbial degradation of hydrocarbons is occurring (Minsley et al., 2007; Naudet et al., 2003). Such large potentials require geobatteries traditionally invoked to explain very large (∼1.0 V) potential gradients due to internal current sources recorded over electronically conductive ore bodies straddling the large redox gradient provided by the water table (Sato and Mooney, 1960). Biogeobatteries may occur in conjunction with a strong redox gradient between highly reducing conditions below the water table within a contaminant plume and an oxidized zone above the water table if microbial activity can generate the required electron bridge (Revil et al., 2010). Possible mechanisms facilitating electron migration include iron oxides, clays, and conductive biological materials (Revil et al., 2010). Metal reducing organisms, such as Shewanella and Geobacter, produce electrically conductive appendages called bacterial nanowires that may facilitate electron transfer to solid-phase electron acceptors (Reguera et al., 2005). However, the ability of biofilms to facilitate electron transport over the scale of the groundwater interface is unknown although new evidence suggests that such electron transfer can take place at millimeter scales (Nielsen et al., 2010). Nonetheless, more studies are needed to confirm this new finding.
Geophysical detection of microbe-mineral transformations
Biogeochemical processes result in mineral precipitation that alters the physicochemical properties of the grain surfaces. When microbial-induced precipitation is extensive, the volumetric physical properties of porous media are modified. In anaerobic environments, iron-reducing bacteria and sulfate-reducing bacteria can use Fe(III) and sulfate respectively as terminal electron acceptors. Ferrous iron produced by iron reducing bacteria promotes the precipitation of electrically conductive secondary minerals such as siderite (FeCO3), magnetite (Fe3O4), and goethite (FeOOH) (Fredrickson et al., 1998). Sulfide produced during microbial sulfate reduction can react with iron (II) produced by iron reducing bacteria to precipitate iron sulfide minerals. Strong seismic and electrical signatures are generated as a result of microbe-induced ZnS and FeS precipitation (Williams et al., 2005). Decreases in seismic wave amplitude result from the development of differential elastic moduli associated with accumulation of metal sulfide-encrusted microbes within pores (Williams et al., 2005). Electrical signals result from the formation, movement and dissolution of electronically conductive biominerals that profoundly enhance the polarization of a porous medium. These electrical signals may be diagnostic of both the concentration and the distribution of the biominerals throughout a porous medium (Slater et al., 2007).
Geophysical signals also result when microbial processes involve the precipitation of semi-metallic or non-metallic minerals, e.g., metabolically induced calcite precipitation by bacterial hydrolysis of urea (Ferris et al., 1995). Relative to metallic minerals, smaller electrical signals result from changes in pore volume/pore tortuosity and/or surface area/surface roughness driven by precipitation of non-metallic minerals (Wu et al., 2010). Calcite precipitation induced by bacteria has been shown to form cements in porous media and affect subsurface fluid flow (Ferris et al., 1995). Such cements profoundly change the elastic properties of soils and rocks, particularly when ureolysis is stimulated to form calcite cement that acts to stiffen the soil matrix (DeJong et al., 2010). Shear waves are well suited to monitoring changes in the particle soil matrix due to precipitation as shear velocity (Vs) is largely unaffected by pore fluid composition and directly dependent on void ratio, coordination number (average number of surrounding particles a given particle is in contact with) and confining stress (DeJong et al., 2010). Large changes in shear-wave velocity accompany stiffening result from initial binding of microbes to the soil matrix, suggesting that relatively small volumes of precipitates can generate large geophysical signals.
Only a decade ago it seemed inconceivable to suggest that microbial processes could potentially impact geophysical signatures. However, today is it clear that geophysical signatures result from a range of microbial processes covering the scale of an individual cell to the scale of contaminant plumes in the Earth. A pressing question in Biogeophysics is how to quantify the geophysical signatures of microbial processes through the development of appropriate modeling frameworks. Success in this venture will likely involve multidisciplinary research between geophysicists, biogeochemists, and microbiologists.