Microbial dynamics in natural aquifers

Abstract

Microorganisms in groundwater form ecosystems that can transform chemical compounds. Quantitatively understanding microbial dynamics in soils and groundwater is thus essential for pollutant dynamics and biogeochemistry in the subsurface. This dissertation addresses three factors influencing microbial dynamics in aquifers and soils, namely: (1) the influence of grazing on bacteria in eutrophic aquifers, posing the question whether the carrying capacity of bacteria, which has been observed in aquifers, is controlled by higher trophic levels of the groundwater ecosystem; (2) the influence of bioenergetic constraints on bacteria in oligotrophic aquifers posing the question how the energy supply controls the dynamics of microorganisms; and (3) the influence of fluctuating redox conditions on overall biogeochemical turnover, posing the question whether alteration of oxic and anoxic conditions benefits the efficiency of the microbial community in the degradation of natural complex substrates. To address the first question, I developed a numerical model simulating a groundwater ecosystem with three trophic levels: a growth substrate, bacteria, and grazers (signifying bacterivorous protozoa, flagellates, ciliates, or bacteriophages). The model is first tested for well-mixed conditions, representing retentostats, and is then coupled to transport to obtain a 1-D bioreactive transport model. In the model, the bacterial population increases, fluctuates, and finally plateaus at a steady-state concentration, which is independent of the substrate concentration. Increasing the substrate exclusively increase the steady-state grazer concentration. When coupled to transport, the same steady-state bacteria concentration is reached over a substantial length of the domain. The simulation results demonstrate that grazing can be a controlling factor in determining the carrying capacity of bacteria in aquifers. I present closed-form expressions for steady-state concentrations in both well-mixed and transport-affected regimes. To address the second question, I developed a bioenergetic model to simulate the survival of bacteria under energy-limiting conditions. The bacteria allocate the gained catabolic energy to growth, maintenance and the production of extracellular hydrolytic enzymes. The fraction of excess energy spent on hydrolytic enzyme production versus the fraction spent on growth is related to the coverage of the particulate organic matter by hydrolytic enzymes. Additionally, the catabolic energy flux governs the activation and deactivation of the microorganisms. The growth of steady state active microorganisms is balanced with the inactivation rate, which itself is balanced with the maintenance-energy requirement of the dormant microorganisms. Within the bioenergetics framework, kinetic rate laws are expressed in thermodynamic terms. The activity of microorganisms is constrained by thermodynamics, and the behavior of the microorganisms is determined by maximum catabolic energy use. I successfully use this conceptual model to illustrate the degradation of cellulose in an anaerobic environment via cellulolytic fermenting bacteria and sulfate reducing bacteria. I show that thermodynamic feedbacks are particularly important for the fermenting bacteria, which require utilization of their metabolic products by other bacteria to gain energy from fermentation. To address the third question, I conducted an experiment to observe the effect of alternating redox conditions on carbon turnover in organic-rich soil suspensions. The results are compared with the static (oxic and anoxic) redox environments. The results demonstrate that redox fluctuations initiate various microbial processes including fermentation, aerobic and anaerobic degradation, most likely performed by different bacteria within a very diverse community. Under oscillating redox conditions, the system always remains far from thermodynamic equilibrium thereby supplying labile organic carbon substrates for microbial energy-gain and growth. Carbon turnover is higher under fluctuating than under the anoxic conditions, and there is a high potential to degrade even more carbon than that under static oxic condition.