DEEP SUBSURFACE MICROBIOLOGY AND MICROBIAL LIFE DEEP UNDERGROUND

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Soil is a complex habitat with numerous microenvironments and niches. Microorganisms are present in the soil primarily attached to soil particles. The most important factor influencing microbial activity in surface soil is the availability of water, whereas in deep soil (the subsurface environment) nutrient availability plays a major role. The deep soil surface, which can extend for several hundred meters below the soil surface, is not a biological wasteland. Although microbial numbers are much lower than in the A horizon soil (Figure 1), a variety of microorganisms, primarily prokaryotes, inhabit deep subsurface soils. For example, in samples collected aseptically from bore holes drilled down to 300 m, diverse populations of both bacteria and Archaea have been found, including anaerobes such as sulphate reducing bacteria (SRB), methanogens, and acetogens, as well as various aerobes and facultative aerobes.

Microorganisms in the deep subsurface have access to nutrients because groundwater flows through their habitats, but activity measurements indicate that the metabolic rates of these bacteria are rather low in their buried habitats (i.e., microbial life deep underground), compared to microorganisms in the upper layers of the soil, the biogeochemical significance of deep subsurface microorganisms may thus be minimal. However, over very long periods and because the volume of deep subsurface soils is so vast, the collective metabolic activities of these buried microorganisms are likely responsible for mineralizing large amounts of organic matter and releasing metabolic products into groundwater.

Microbial bioremediation (cleaning up polluted soils and waters) is a method for removing toxic substances such as aromatic and agricultural chemicals leached from soil into groundwaters and the deep subsurface. Two approaches have been considered. In one method, inorganic nutrients, especially nitrogen and phosphorus, are added to stimulate biodegradation of toxic organic chemicals by the resident microflora; in the other method, large numbers of specific bacterial cells are introduced into the deep subsurface to accelerate the biodegradation process.

Figure 1. Profile of a mature soil. The soil horizons are zones as defined by soil scientists.

Microbial Life Deep Underground

Microbiologists studying the deep terrestrial subsurface have found viable prokaryotic cells at depths of several thousand meters below the surface. How are these microorganisms making a living in these unusual habitats? Initial indicators were that these buried microorganisms were chemoorganotrophs that metabolize the organic carbon deposited within the sediments. However, studies of deep basalt aquifers have shown that sluggish chemoorganotrophs are not the only viable organisms deep underground. Chemoorganotrophs are defined as organisms that obtain their energy from the oxidation of organic compounds. Chemoorganotrophic prokaryotes are present there, too, and probably dominate microbial life underground.

Basalts are iron-rich volcanic rocks essentially devoid of organic matter. In certain basalts up to 1500 m deep from the Columbia River Basin (Washington, USA), large numbers of anaerobic, chemolithotrophic bacteria and Archaea have been discovered, including SRB, methanogens, and acetogens. Carbon stable isotope analyses showed that the methanogens were responsible for the methane (CH4) present I the rocks. Measurements showed a strong enrichment in the lighter isotope of carbon (12C) of the methane, which is indicative of biological methanogens. If the methanogens deep underground are active, it is likely that the other physiological groups are active as well. This is because in an organic –poor environment the common metabolic thread uniting these organisms is molecular hydrogen (H2).

H2 is an excellent electron donor for the energy-yielding metabolisms of methanogens, sulphate reducing bacteria and acetogens. H2 is a common product of the fermentative catabolism of organic matter. But if basalts contain very little organic material, where does the H2 to support metabolism of the H2 consumers come from? H2 in the Columbia River basalts apparently originates from the chemical interaction of water with iron minerals in the rocks. Such reactions are known from inorganic chemistry, and in laboratory studies in which crushed Columbia River basalt was mixed with sterile water under anoxic conditions, H2 evolved rapidly.

H2 was also detected directly in groundwater percolating through the basalts. It therefore appears that H2 formed within basalts is the electron donor for the anaerobic prokaryotes found there. If true, these organisms would be surviving strictly geochemically and totally divorced from any reliance on phototrophically generated organic materials. This  is because both their electron acceptors (CO2 in methanogens and acetogens and SO42- in sulphate reducing bacteria) and electron donor (H2) are derived from inorganic materials.

As sometimes happens in science, further research has questioned the Columbia River basalt findings. Although there is not much organic matter in these basalts, there is some, and this fermentation could be the source of some of the H2 used by the subsurface chemolithotrophs, as it is in anoxic surface communities. How ecologically significant are H2-based microbial ecosystems in the deep subsurface? This is an unanswered question. However, the fact that we  now suspect that total prokaryotic numbers in Earth’s deep subsurface are very large, larger in fact than the total number of prokaryotes present in all other environments, suggests that these buried microorganisms may be major catalysts for the cycling of carbon on Earth.  

Further reading

Madigan M.T., Martinko J.M., Dunlap P.V and Clark D.P (2009). Brock Biology of Microorganisms, 12th edition. Pearson Benjamin Cummings Inc, USA.

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