3 Groundwater Systems as Habitats for Microbial Life

The types of places in which living organisms grow and multiply are often described as habitats. Each habitat is characterized by a set of physical and chemical features that are essential for sustaining life. In the context of hydrogeology, one of the most critical physical parameters for describing different habitats is by magnitude of the length scale. In groundwater systems, length scales extend over large distances of 103 m (1 km) all the way down to distances as small as 10-6 m (1 μm), depending on how habitat size is defined. Length scale is critical because it defines other important physical properties for habitability such as surface areas and relative volumes of solids, water, air, and other fluids. These factors determine not only where it is possible for life to take refuge but also influence water movement (with links to Darcy’s law through hydraulic conductivity), groundwater chemistry, and reactive mass transport processes (with links to advection, dispersion and reaction relationships).

On a global scale, the vast amount of water that exists underground is difficult to imagine with volume estimates soaring into, and above, tens of millions of cubic kilometers (Gleeson et al., 2015). This is almost as much water as there is in some ocean basins. But, remarkably, all of that groundwater is mostly invisible to macroscopic (> 10-4 m) observation because it is hidden away in microscopic (< 10-4 m) interstitial pore spaces between mineral grains in sediments, as well as along joints and fracture planes in bedrock. As a consequence, the mineral surface area to water volume ratio in groundwater systems far exceeds that of surface environments. Nevertheless, when it comes to actual living space, most subsurface environments are only accessible to microorganisms.

To get an idea of the limitations of physical space in subsurface environments, Figure 11 compares the size range of different life forms with pore diameters in unconsolidated clay and sands, along with corresponding values for shale, sandstone, dolomite, and aperture widths in fractured/jointed rocks. Apart from some wider fracture and joint apertures that occur in rocks, macro-eukaryotes are just too big to live in groundwater environments. Even the fit for micro-eukaryotes is tight as their size range is similar to pore diameters in sands, meaning there is very little room to grow and divide. On the other hand, the smaller size of prokaryotes allows them to live in comfort within most porous unconsolidated sands. While planktonic growth and movement between pores is possible, most cells grow in biofilms attached to mineral grains or rock surfaces. Overall, attached microorganisms dominate groundwater systems in terms of biomass and activity; however, there is a dynamic equilibrium between attachment and detachment processes as bacteria transition between planktonic and attached modes of growth in response to changes in environmental conditions such as nutrient availability or fluctuations in oxidation-reduction potential. In the tighter confines of pores in clays and consolidated sedimentary rocks such as shale, space begins to become a limiting factor not only for prokaryotic cells but also for individual virus particles (Rebata-Landa and Santamarina, 2006).

Figure comparing characteristic pore diameters in sediments and fracture/joint aperture widths in rocks with the size range of viruses, prokaryotes, micro-eukaryotes, and macro-eukaryotes

Figure 11 Comparison of characteristic pore diameters in sediments and fracture/joint aperture widths in rocks with the size range of viruses, prokaryotes, micro-eukaryotes, and macro-eukaryotes. The blue dashed line represents the upper size limit of all microorganisms, whereas the red dashed line defines the lower size limit of prokaryotes.

The steady decline of microbial cell concentrations with increasing depth underground is well documented. In near-surface groundwater systems at depths less than 100 m, cell numbers average 107/g in cores and around 105/mL in groundwater samples. These cellular concentrations decrease to respective mean values of about 104/g and 103/mL at depths of > 1000 m. Increasing ionic strength with depth has been identified as a particularly important factor contributing to lower cell numbers in the deep subsurface. Within the soil zone, declining microbial numbers over a depth interval from 1 to 2 m typically correlate with decreasing organic carbon concentration. This is because aerobic heterotrophs degrade and consume cellulose-rich organic matter derived from plants. At greater depths, the relationship between microbial cell concentrations and organic carbon weakens, implying an enhanced role of lithoautotrophic microorganisms in deep subsurface carbon cycling.

Another important physical parameter that defines habitats in groundwater systems is temperature (Amend and Teske, 2005; Taylor and Stefan, 2009; Bonte et al., 2013a,b). The reason temperature is so critical is that it controls when and where water exists in a liquid state, which is an absolute life requirement. For pure water, this is from 0 to 100°C at a standard pressure of 1 atm. Rates of metabolic processes and chemical reactions, as well as the stability of biomolecules, are all dependent on temperature. The density and viscosity of water are also sensitive to temperature, as is the transport of metabolites and other chemical substances by molecular diffusion.

In contrast to seasonal changes in climate above ground, the high specific heat capacity of water, insulating properties of geological materials, and lack of solar irradiance keep shallow groundwaters close to the mean annual air temperature (Menberg et al., 2014; Benz et al., 2017). With the exception of polar regions, this means that most shallow (no more than 60 m depth) groundwater systems around the world fall well inside the required habitat temperature range of microorganisms (Figure 12).

Map showing global temperature estimates for shallow (< 60 m) groundwater.

Figure 12 Global temperature estimates for shallow (< 60 m) groundwater (Reproduced under the terms of Creative Commons Attribution 3.0 license from Benz et al., 2017).

Temperature tends to increase with depth underground because of multiple heat sources inside the Earth, such as radioactive decay and latent heat from core crystallization. Although variable, especially in hot volcanic regions, the typical geothermal gradient in most areas of the world is about 25 to 30°C/km. This means that temperatures will approach 100°C at depths of 3 to 4 km, which gives a rough idea of the depth to which microbial life can exist in groundwater systems (Colwell and D’Hondt, 2013).

Numerous chemical properties are relevant to the characterization of microbial habitats in groundwater systems, including pH (Equation 2), Eh (redox) potential (Equation 4), and ionic strength (Equation 5). In addition, concentrations of different solid materials, gases, and dissolved solutes help define overall chemical conditions of a habitat, particularly in terms of nutrient availability and energy supply. These concentrations are often reported in different units, for example as percentages, parts per million, or molarity. Similarly, for gases, parts per million by volume and partial pressure are often used interchangeably. It is therefore important to be able to convert from one unit to another in any quantitative investigation of these parameters within groundwater systems.


Groundwater Microbiology Copyright © 2021 by F. Grant Ferris, Natalie Szponar, and Brock A. Edwards. All Rights Reserved.